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Food Microbiology xxx (2013) 1e19

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Food Microbiology
journal homepage: www.elsevier.com/locate/fm

Microbial ecology of sourdough fermentations: Diverse or uniform?


L. De Vuyst a, *, S. Van Kerrebroeck a, H. Harth a, G. Huys b, H.-M. Daniel c, S. Weckx a
a
Research Group of Industrial Microbiology and Food Biotechnology (IMDO), Faculty of Sciences and Bioengineering Sciences, Vrije Universiteit Brussel,
Pleinlaan 2, B-1050 Brussels, Belgium
b
Laboratory of Microbiology and BCCM/LMG Bacteria Collection, Faculty of Sciences, Ghent University, K.L. Ledeganckstraat 35, B-9000 Gent, Belgium
c
Mycothque de lUniversit catholique de Louvain (MUCL), Belgian Coordinated Collection of Microorganisms (BCCM), Earth and Life Institute, Applied
Microbiology, Mycology, Universit catholique de Louvain, Croix du Sud 3, bte 6, B-1348 Louvain-la-Neuve, Belgium

a b s t r a c t
Keywords:
Microbial ecology
Lactic acid bacteria
Yeasts
Sourdough
Bakery

Sourdough is a specic and stressful ecosystem inhabited by yeasts and lactic acid bacteria (LAB), mainly
heterofermentative lactobacilli. On the basis of their inocula, three types of sourdough fermentation
processes can be distinguished, namely backslopped ones, those initiated with starter cultures, and those
initiated with a starter culture followed by backslopping. Typical sourdough LAB species are Lactobacillus
fermentum, Lactobacillus paralimentarius, Lactobacillus plantarum, and Lactobacillus sanfranciscensis.
Typical sourdough yeast species are Candida humilis, Kazachstania exigua, and Saccharomyces cerevisiae.
Whereas region specicity is claimed in the case of artisan backslopped sourdoughs, no clear-cut relationship between a typical sourdough and its associated microbiota can be found, as this is dependent on
the sampling, isolation, and identication procedures. Both simple and very complex consortia may
occur. Moreover, a series of intrinsic and extrinsic factors may inuence the composition of the sourdough microbiota. For instance, an inuence of the our (type, quality status, etc.) and the process parameters (temperature, pH, dough yield, backslopping practices, etc.) occurs. In this way, the presence of
Lb. sanfranciscensis during sourdough fermentation depends on specic environmental and technological
factors. Also, Triticum durum seems to select for obligately heterofermentative LAB species. Finally, there
are indications that the sourdough LAB are of intestinal origin.
2013 Elsevier Ltd. All rights reserved.

1. Introduction
The sourdough ecosystem consists of a mixture of our (fractions) and water that is fermented by yeasts and lactic acid bacteria
(LAB) (Corsetti and Settanni, 2007; De Vuyst and Neysens, 2005; De
Vuyst and Vancanneyt, 2007; De Vuyst et al., 2009). From a
microbiological point of view, it is a specic and stressful ecosystem
that is characterized by a low pH, high carbohydrate concentrations, oxygen limitation, and higher cell counts of LAB [108 colony
forming units (CFU)/g] compared to yeasts (107 CFU/g). The major
metabolic activities of the sourdough microbiota are acidication
(LAB), avor formation (LAB and yeasts), and leavening (yeasts and
heterofermentative LAB species). Sourdough provides the production of breads with technological advantages regarding dough
processing and bread texture, avor, and shelf-life. Also, nutritional
properties (sourdough is rich in nutrients), health-promoting effects (owing to endogenous enzymatic modications of the cereal

* Corresponding author. Tel.: 32 2 6293245; fax: 32 2 6292720.


E-mail address: ldvuyst@vub.ac.be (L. De Vuyst).

matrix and/or specic activities of certain LAB species that are, for
instance, reected in gluten-free products), and artisan features
(such as a natural status, traditional value, and gastronomic quality)
contribute to the success of sourdough use. Sourdoughs are produced worldwide (Table 1).
2. Types of sourdough fermentation processes
On the basis of their inocula, three types of sourdough
fermentation processes can be distinguished (Corsetti and Settanni,
2007; De Vuyst and Neysens, 2005; De Vuyst and Vancanneyt,
2007; De Vuyst et al., 2009). A rst type represents spontaneous
sourdough fermentation processes based on backslopping, i.e.,
repeated cyclic re-inoculation of a new batch of our and water
from a previous one derived from the so-called mother dough,
traditionally carried out at room temperature. Thanks to craftsmanship and maintenance of mother doughs for years, a huge variety of bakery products produced from backslopped sourdoughs
exists. These sourdoughs harbor mixtures of distinctive yeasts and
LAB species and/or strains, which actually represent a large diversity of natural sourdough starters. Apparently, they also reect

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http://dx.doi.org/10.1016/j.fm.2013.06.002

Please cite this article in press as: De Vuyst, L., et al., Microbial ecology of sourdough fermentations: Diverse or uniform?, Food Microbiology
(2013), http://dx.doi.org/10.1016/j.fm.2013.06.002

Country

Cereal our type


Method of identication

LAB and/or yeast species reported

Reference(s)

Belgium

Wheat
Molecular

LAB: Lb. acidifarinae, Lb. brevis, Lb. buchneri, Lb. crustorum, Lb. hammesii, Lb. helveticus, Lb. nantensis, Lb.
parabuchneri, Lb. paracasei, Lb. paralimentarius, Lb. plantarum, Lb. pontis, Lb. rossiae, Lb. sakei, Lb.
sanfranciscensis, Lb. spicheri, Leuc. mesenteroides, P. pentosaceus, W. cibaria, W. confusa
Yeasts: S. cerevisiae, K. barnettii, K. unispora, T. delbrueckii, W. anomalus
LAB: Lb. brevis, Lb. hammesii, Lb. nantensis, Lb. paralimentarius, Lb. plantarum
Yeasts: S. cerevisiae, W. anomalus

Scheirlinck et al., 2007b,c,


2008; Vrancken et al.,
2010

Rye
Molecular
Wheat-rye
Molecular
Spelt
Molecular
Wheat rye spelt
Molecular

Denmark
Estonia

Ethiopia

Rye
Phenotypical
Rye e use of a starter (LAB: Lb. helveticus, Lb. panis, Lb. pontis, Lb.
vaginalis)
Molecular
Teff (enjera)
Phenotypical
Teff
Molecular
Teff (enjera)
Phenotypical

LAB: Lb. fermentum, Lb. plantarum


Yeasts: C .glabrata, W. anomalus
LAB: Lb. brevis, Lb. paraplantarum, Lb. plantarum, Lb. rossiae
Yeasts: C. glabrata, S. cerevisiae, W. anomalus
LAB: Lb. curvatus, Lb. fermentum, Lb. plantarum, P. pentosaceus
LAB: Lb. fermentum, Lb. plantarum, P. pentosaceus, W. confusa

Weckx et al., 2010a

LAB: Lb. brevis, Lb. fermentum, Lb. plantarum, P. pentosaceus


Yeasts: C. glabrata, S. cerevisiae, W. anomalus
LAB: E. durans, Lb. brevis, Lb. crustorum, Lb. curvatus, Lb. fermentum, Lb. guizhouensis, Lb. helveticus, Lb.
mindensis, Lb. paralimentarius, Lb. plantarum, Lb. rossiae, Lb. sanfranciscensis, Lb. zeae, Lc. lactis, Leuc. citreum,
Leuc. mesenteroides, W. cibaria, W. confusa
Yeasts: C. humilis, C. parapsilosis, K. exigua, Meyerozyma guilliermondii, P. kudriavzevii, S. cerevisiae,
T. delbrueckii, W. anomalus
LAB: Lb. amylovorus, Lb. panis, Lb. reuteri
Yeasts: S. cerevisiae
LAB: Lb. helveticus, Lb. panis, Lb. pontis

Weckx et al., 2010b

Rosenquist and Hansen,


2000
Viiard et al., 2012

LAB: E. faecalis, Lb. brevis, Lb. fermentum, Lb. plantarum, Leuc. mesenteroides, P. cerevisiae

Gashe, 1985

LAB: Lb. fermentum, Lb. graminis, Lb. parabuchneri, Lb. plantarum

Nigatu, 2000
Desiye and Abegaz, 2013

LAB: E. mundtii, Lb. brevis, Lb. curvatus, Lb. fermentum, Lb. paracasei, Lb. paralimentarius, Lb. plantarum, Lb.
pontis, Lb. rossiae, Lb. sanfranciscensis, P. acidilactici, P. pentosaceus, W. confusa
Yeasts: S. cerevisiae, T. delbrueckii
LAB: Lb. brevis, Lb. curvatus, Lb. hammesii, Lb. nantensis, Lb. paralimentarius, Lb. plantarum, Lb. pontis, Lb.
rossiae, Lb. sakei, Lb. sanfranciscensis, P. pentosaceus, W. cibaria
Yeasts: S. cerevisiae
LAB: Lb. brevis, Lb. hammesii, Lb. namurensis, Lb. paralimentarius, Lb. plantarum
Yeasts: W. anomalus

Finland

Rye
Phenotypical molecular

LAB: E. casseliavus, Lb. fermentum, Lc. piscium, Lc. plantarum, Lc. rafnolactis, Leuc. mesenteroides,
P. acidilactici, P. pentosaceus
Yeasts: C. humilis, C. tropicalis, K. exigua, P. norvegensis, S. cerevisiae
LAB: Lb. acidophilus, Lb. casei, Lb. plantarum
Yeasts: C. humilis, C. stellata, K. exigua, K. unispora, S. cerevisiae, W. anomalus

France

Wheat
Phenotypical
Wheat
Phenotypical
Wheat
Molecular
Wheat
Molecular

LAB: Lb. acidophilus, Lb. brevis, Lb. casei, Lb. curvatus, Lb. delbrueckii subsp. delbrueckii, Lb. plantarum, Leuc.
mesenteroides subsp. dextranicum, Leuc. mesenteroides subsp. mesenteroides, P. pentosaceus
LAB: Lb. brevis, Lb. curvatus, Lb. plantarum, Lb. rhamnosus, Leuc. mesenteroides, P. pentosaceus
Yeasts: K. exigua, S. cerevisiae, T. delbrueckii, W. anomalus
LAB: Lb. frumenti, Lb. hammesii, Lb. nantensis, Lb. panis, Lb. paralimentarius, Lb. pontis, Lb. sanfranciscensis, Lb.
spicheri, Leuc. mesenteroides subsp. mesenteroides
LAB: Lb. frumenti, Lb. hammesii, Lb. nantensis, Lb. panis, Lb. paralimentarius, Lb. sanfranciscensis, Lb. spicheri,
Leuc. mensenteroides subsp. mensenteroides

Zhang et al., 2011

Salovaara and Savolainen,


1984; Mntynen et al.,
1999
Infantes and Tourneur,
1991
Infantes and Schmidt,
1992; Gabriel et al., 1999
Ferchichi et al., 2007
Ferchichi et al., 2008

L. De Vuyst et al. / Food Microbiology xxx (2013) 1e19

China

Wheat (laboratory)
Molecular
Spelt (laboratory)
Molecular
Wheat (laboratory)
Molecular microarray
Spelt (laboratory)
Molecular microarray
Rye (laboratory)
Molecular
Wheat
Molecular

Scheirlinck et al., 2007c,


2008; Vrancken et al.,
2010
Scheirlinck et al., 2007c,
2008; Vrancken et al.,
2010
Scheirlinck et al., 2007c,
2008; Vrancken et al.,
2010
Scheirlinck et al., 2007a,
2008; Vrancken et al.,
2010
Van der Meulen et al.,
2007
Van der Meulen et al.,
2007
Weckx et al., 2010a

Please cite this article in press as: De Vuyst, L., et al., Microbial ecology of sourdough fermentations: Diverse or uniform?, Food Microbiology
(2013), http://dx.doi.org/10.1016/j.fm.2013.06.002

Table 1
Non-exhaustive overview of the species diversity of lactic acid bacteria (LAB) and/or yeasts in sourdoughs made from various ours and of different geographical origins. The methods of identication (phenotypical or molecular)
of the LAB and yeast species are indicated. This table is an extended version of the one published in Huys et al. (2013).

Rye (sourdough starter)


Phenotypical
Wheat (Panettone, wheat bread from Germany, Italy, Sweden, and
Switzerland)
Phenotypical
Rye
Molecular
Rye (bran) e use of a starter (LAB: Lb. brevis, W. confusa, Lb. crispatus,
Lb. curvatus, Lb. fermentum, Lb. mindensis, Lb. paracasei, Lb.
plantarum, Lb. sanfranciscensis, W. viridescens e Yeasts: C. humilis,
D. hansenii, S. cerevisiae, S. uvarum)
Phenotypical, molecular
Rice e use of a starter [LAB: Lb. paracasei, Lb. paralimentarius, Lb.
perolens, Lb. spicheri e Yeasts: S. cerevisiae (mother sponge)]
Phenotypical molecular
Rice e use of a starter (LAB: Lb. fermentum, Lb. gallinarum, Lb. pontis
e Yeasts: P. membranifaciens, S. cerevisiae)
Wheat
Molecular
Rye
Molecular
Amaranth (from India, Peru, Mexico, Germany)
Molecular
Amaranth (from India, Peru, Mexico, Germany) e use of a starter
(Lb. plantarum, Lb. sakei, P. pentosaceus)
Molecular
Amaranth e use of a starter (LAB: Lb. acetotolerans, Lb. brevis, Lb.
casei, Lb. curvatus, Lb. fermentum, Lb. helveticus, Lb. paracasei, Lb.
paralimentarius, Lb. plantarum, Lb. pontis, Lb. sanfranciscensis, Lb.
spicheri, Leuc. paramesenteroides, Lc. lactis e Yeasts: C. humilis,
P. anomala, P. kudriavzevii, S. cerevisiae, Torulaspora sp.)
Barley e use of a starter (LAB: Lb. acetotolerans, Lb. brevis, Lb. casei,
Lb. curvatus, Lb. fermentum, Lb. helveticus, Lb. paracasei, Lb.
paralimentarius, Lb. plantarum, Lb. pontis, Lb. sanfranciscensis, Lb.
spicheri, Leuc. paramesenteroides, Lc. lactis e Yeasts: C. humilis,
P. anomala, P. kudriavzevii, S. cerevisiae, Torulaspora sp.)
Buckwheat e use of a starter (LAB: Lb. acetotolerans, Lb. brevis, Lb.
casei, Lb. curvatus, Lb. fermentum, Lb. helveticus, Lb. paracasei, Lb.
paralimentarius, Lb. plantarum, Lb. pontis, Lb. sanfranciscensis, Lb.
spicheri, Leuc. paramesenteroides, Lc. lactis e Yeasts: C. humilis,
P. anomala, P. kudriavzevii, S. cerevisiae, Torulaspora sp.)
Cassava e use of a starter (LAB: Lb. acetotolerans, Lb. brevis, Lb. casei,
Lb. curvatus, Lb. fermentum, Lb. helveticus, Lb. paracasei, Lb.
paralimentarius, Lb. plantarum, Lb. pontis, Lb. sanfranciscensis, Lb.
spicheri, Leuc. paramesenteroides, Lc. lactis e Yeasts: C. humilis,
P. anomala, P. kudriavzevii, S. cerevisiae, Torulaspora sp.)
Maize e use of a starter (LAB: Lb. acetotolerans, Lb. brevis, Lb. casei,
Lb. curvatus, Lb. fermentum, Lb. helveticus, Lb. paracasei, Lb.
paralimentarius, Lb. plantarum, Lb. pontis, Lb. sanfranciscensis, Lb.
spicheri, Leuc. paramesenteroides, Lc. lactis e Yeasts: C. humilis,
P. anomala, P. kudriavzevii, S. cerevisiae, Torulaspora sp.)

LAB: E. hirae, Lb. brevis, Lb. casei/paracasei, Lb. curvatus, Lb. paraplantarum, Lb. pentosus, Lb. plantarum, Lb.
sakei, Lb. sanfranciscensis, Lc. lactis, Leuc. citreum, Leuc. mesenteroides, P. pentosaceus, W. cibaria, W. confusa
LAB: Lb. acetotolerans, Lb. amylolyticus, Lb. frumenti, Lb. panis

Robert et al., 2009


Vera et al., 2012

LAB: Lb. brevis, Lb. buchneri, Lb. casei, Lb. delbrueckii, Lb. fermentum, Lb. plantarum

Spicher, 1959

LAB: Lb. acidophilus, Lb. alimentarius, Lb. brevis, Lb. buchneri, Lb. casei, Lb. farciminis, Lb. fermentum, Lb.
fructivorans, Lb. plantarum, Lb. sanfranciscensis
Yeasts: K. exigua, P. kudriavzevii, S. cerevisiae
LAB: Lb. acidophilus, Lb. brevis, Lb. buchneri, Lb. casei, Lb. farciminis, Lb. fermentum, Lb. fructivorans, Lb.
plantarum, Lb. sanfranciscensis, Pediococcus spp.
LAB: Lb. brevis, Lb. casei, Lb. farciminis, Lb. hilgardii, Lb. homohiochii, Lb. plantarum (spontaneous)
Lb. brevis, Lb. hilgardii, Lb. sanfranciscensis, W. viridescens (masa madre)

Spicher and Schrder,


1978

LAB: Lb. amylovorus, Lb. frumenti, Lb. pontis, Lb. reuteri (type II)

Mller et al., 2001

LAB: Lb. mindensis, Lb. sanfranciscensis (rye, type I)


Lb. crispatus, Lb. fermentum, Lb. frumenti, Lb. panis, Lb. pontis (rye, type II)
Lb. johnsonii, Lb. reuteri (rye bran, type II)
Yeasts: C. glabrata, C. humilis, P. kudriavzevii, S. cerevisiae

Meroth et al., 2003a,b

LAB: Lb. paracasei, Lb. paralimentarius, Lb. spicheri


Yeasts: S. cerevisiae

Meroth et al., 2004

LAB: Lb. curvatus, Lb. fermentum, Lb. gallinarum, Lb. kimchii, Lb. plantarum, Lb. pontis
Yeasts: P. kudriavzevii, S. cerevisiae
LAB: E. faecium, Lb. casei, Lb. fermentum, Lb. plantarum, Lb. sanfranciscensis, P. pentosaceus, W. confusa

Meroth et al., 2004


Kitahara et al., 2005

LAB: Lb. pontis, Lb. sanfranciscensis

Kitahara et al., 2005

LAB: Lb. paralimentarius, Lb. plantarum, Lb. sakei, P. pentosaceus

Sterr et al., 2009

LAB: Lb. plantarum, Lb. sakei, P. pentosaceus

Sterr et al., 2009

LAB: Lb. fermentum, Lb. helveticus, Lb. paralimentarius, Lb. plantarum, Lb. spicheri
Yeasts: C. glabrata, S. cerevisiae

Vogelmann et al., 2009

LAB: Lb. fermentum, Lb. helveticus, Lb. paralimentarius, Lb. pontis


Yeasts: S. cerevisiae

Vogelmann et al., 2009

LAB: Lb. fermentum, Lb. helveticus, Lb. paralimentarius, Lb. plantarum


Yeasts: -

Vogelmann et al., 2009

LAB: Lb. fermentum, Lb. paralimentarius, Lb. plantarum, Lb. spicheri


Yeasts: S. cerevisiae

Vogelmann et al., 2009

LAB: Lb. fermentum, Lb. helveticus, Lb. paralimentarius, Lb. pontis


Yeasts: P. kudriavzevii, S. cerevisiae

Vogelmann et al., 2009

Spicher, 1984
Spicher, 1987

L. De Vuyst et al. / Food Microbiology xxx (2013) 1e19

Please cite this article in press as: De Vuyst, L., et al., Microbial ecology of sourdough fermentations: Diverse or uniform?, Food Microbiology
(2013), http://dx.doi.org/10.1016/j.fm.2013.06.002

Germany

Wheat
Molecular
Wheat (mother sponge)
Phenotypical molecular
Wheat
Phenotypical
Rye (sourdough starter)
Phenotypical

(continued on next page)

Country

Greece

Italy

Cereal our type


Method of identication

LAB and/or yeast species reported

Reference(s)

Millet e use of a starter (LAB: Lb. acetotolerans, Lb. brevis, Lb. casei,
Lb. curvatus, Lb. fermentum, Lb. helveticus, Lb. paracasei, Lb.
paralimentarius, Lb. plantarum, Lb. pontis, Lb. sanfranciscensis, Lb.
spicheri, Leuc. paramesenteroides, Lc. lactis e Yeasts: C. humilis,
P. anomala, P. kudriavzevii, S. cerevisiae, Torulaspora sp.)
Oat e use of a starter (LAB: Lb. acetotolerans, Lb. brevis, Lb. casei, Lb.
curvatus, Lb. fermentum, Lb. helveticus, Lb. paracasei, Lb.
paralimentarius, Lb. plantarum, Lb. pontis, Lb. sanfranciscensis, Lb.
spicheri, Leuc. paramesenteroides, Lc. lactis e Yeasts: C. humilis,
P. anomala, P. kudriavzevii, S. cerevisiae, Torulaspora sp.)
Quinoa e use of a starter (LAB: Lb. acetotolerans, Lb. brevis, Lb. casei,
Lb. curvatus, Lb. fermentum, Lb. helveticus, Lb. paracasei, Lb.
paralimentarius, Lb. plantarum, Lb. pontis, Lb. sanfranciscensis, Lb.
spicheri, Leuc. paramesenteroides, Lc. lactis e Yeasts: C. humilis,
P. anomala, P. kudriavzevii, S. cerevisiae, Torulaspora sp.)
Wheat e use of a starter (LAB: Lb. acetotolerans, Lb. brevis, Lb. casei,
Lb. curvatus, Lb. fermentum, Lb. helveticus, Lb. paracasei, Lb.
paralimentarius, Lb. plantarum, Lb. pontis, Lb. sanfranciscensis, Lb.
spicheri, Leuc. paramesenteroides, Lc. lactis e Yeasts: C. humilis,
P. anomala, P. kudriavzevii, S. cerevisiae, Torulaspora sp.)
Wheat, rye (laboratory e use of a starter; LAB: Lb. fermentum, Lb.
helveticus, Lb. johnsonii, Lb. reuteri, Lb. pontis, Lb. sanfranciscensis e
Yeasts: C. humilis, P. kudriavzevii, S. cerevisiae) Molecular
Wheat, rye, rye bran (laboratory e use of a starter; LAB: Lb.
fermentum, Lb. helveticus, Lb. johnsonii, Lb. reuteri, Lb. pontis, Lb.
sanfranciscensis e Yeasts: C. humilis, P. kudriavzevii, S. cerevisiae)
Molecular
Maize
Phenotypical
Wheat
Phenotypical molecular
Wheat
Phenotypical molecular
Wheat (panettone, brioche)
Phenotypical
Wheat (Umbria)
Phenotypical
Pizza from Naples
Phenotypical
Wheat (Molise, Umbria, Venise)
Molecular
Mother sponges (Lombardy)
Phenotypical molecular
Wheat (Apulia)
Phenotypical molecular

LAB: Lb. fermentum, Lb. helveticus, Lb. pontis


Yeasts: S. cerevisiae

Vogelmann et al., 2009

LAB: Lb. fermentum, Lb. helveticus Lb. paralimentarius, Lb. pontis


Yeasts: e

Vogelmann et al., 2009

LAB: Lb. fermentum, Lb. helveticus, Lb. paralimentarius, Lb. plantarum, Lb. pontis
Yeasts: P. kudriavzevii, S. cerevisiae

Vogelmann et al., 2009

LAB: Lb. fermentum, Lb. helveticus, Lb. pontis


Yeasts: S. cerevisiae

Vogelmann et al., 2009

LAB: Lb. sanfranciscensis


Yeasts: C. humilis

Vogelmann and Hertel,


2011

LAB: Lb. johnsonii, Lb. reuteri


Yeasts: P. kudriavzevii

Vogelmann and Hertel,


2011

Yeasts: C. tropicalis, Kl. marxianus, P. kudriavzevii, S. cerevisiae

Obiri-Danso, 1994

LAB: Lb. plantarum, Lb. sanfranciscensis, P. pentosaceus


Yeasts: P. membranifaciens, S. cerevisiae, T. delbrueckii
LAB: Lb. brevis, Lb. paralimentarius, Lb. sanfranciscensis, Lb. zymae, W. cibaria

Paramithiotis et al., 2000,


2010
De Vuyst et al., 2002

LAB: Lb. fermentum, Lb. plantarum, Lb. sanfranciscensis, Leuc. mesenteroides, Pediococcus spp.
Yeasts: C. humilis, C. stellata, K. exigua, S. cerevisiae
LAB: Lb. farciminis, Lb. plantarum, Lb. sanfranciscensis
Yeasts: K. exigua, P. kudriavzevii, S. cerevisiae, W. anomalus
LAB: Lb. plantarum, Lb. sakei, Leuc. gelidum, Leuc. mesenteroides

Galli et al., 1988

Sicilian sourdoughs
Phenotypical molecular
Wheat (Southern Italy)
Molecular
Wheat
Molecular
Wheat (Molise)
Phenotypical molecular
Wheat (panettone, pandoro, cornetto, colomba)
Phenotypical molecular

LAB: Lb. sanfranciscensis


LAB: Lb. sanfranciscensis
Yeasts: K. exigua, S. cerevisiae
LAB: Lb. acidophilus, Lb. alimentarius, Lb. brevis, Lb. delbrueckii subsp. delbrueckii, Lb. fermentum, Lb.
plantarum, Lb. sanfranciscensis, Lc. lactis subsp. lactis, Leuc. citreum, W. confusa
Yeasts: K. exigua, P. kudriavzevii, S. cerevisiae
Yeasts: C. humilis, P. kudriavzevii, S. cerevisiae

Gobbetti et al., 1994b


Coppola et al., 1996
Zapparoli et al., 1996,
1998
Foschino et al., 1999
Corsetti et al., 2001

Pulvirenti et al., 2001

LAB: Lb. alimentarius, Lb. brevis, Lb. farciminis, Lb. fermentum, Lb. fructivorans, Lb. plantarum, Lb.
sanfranciscensis, W. confusa
Yeasts: C. humilis

Corsetti et al., 2003


Gullo et al., 2003

Yeasts: C. glabrata, P. kudriavzevii, P. membranifaciens, S. cerevisiae, T. delbrueckii

Succi et al., 2003

Yeasts: C. humilis, S. cerevisiae, S. pastorianus

Foschino et al., 2004

L. De Vuyst et al. / Food Microbiology xxx (2013) 1e19

Ghana

Please cite this article in press as: De Vuyst, L., et al., Microbial ecology of sourdough fermentations: Diverse or uniform?, Food Microbiology
(2013), http://dx.doi.org/10.1016/j.fm.2013.06.002

Table 1 (continued )

Veneto sourdoughs
Molecular
Wheat (Panettone from Central Italy)
Molecular
Wheat (Cornetto, Basilicata)
Phenotypical molecular
Wheat
Phenotypical molecular
Wheat (Marche)
Phenotypical molecular

Wheat
Molecular
Wheat e use of a starter (LAB: Lb. sanfranciscensis)
Molecular
Barley e use of a starter (LAB: Lb. brevis, Lb. curvatus, Lb. helveticus,
Lb. paralimentarius, Lb. plantarum, Lb. sanfranciscensis, Leuc. citreum,
Leuc. pseudomesenteroides, W. confusa, W. kimchii e Yeasts:
C. humilis, S. cerevisiae)
Molecular
Barley wheat e use of a starter (LAB: Lb. brevis, Lb. curvatus, Lb.
helveticus, Lb. paralimentarius, Lb. plantarum, Lb. sanfranciscensis,
Leuc. citreum, Leuc. pseudomesenteroides, W. confusa, W. kimchii e
Yeasts: C. humilis, S. cerevisiae)
Molecular
Emmer e use of a starter (LAB: Lb. plantarum, W. confusa)
Molecular
Spelt e use of a starter (LAB: Lb. brevis, Lb. plantarum, W. confusa)
Molecular
Wheat
Molecular
Wheat e use of a starter (LAB: Lb. plantarum)
Molecular
Wheat e use of a starter (LAB: Lb. plantarum, Lb. sanfranciscensis)
Molecular
Wheat germ e use of a starter (LAB: Lb. plantarum, Lb. rossiae,
P. pentosaceus, W. confusa)
Molecular

LAB: Lb. arizonensis/plantarum, Lb. brevis, Lb. kimchii/paralimentarius, Lb. paraplantarum,


Lb. sanfranciscensis
Yeasts: C. humilis, K. exigua, P. kudriavzevii, S. cerevisiae

Pulvirenti et al., 2004

Yeasts: C. humilis, S. cerevisiae

Vernocchi et al., 2004a

Yeasts: C. humilis, S. cerevisiae

Vernocchi et al., 2004b

LAB: Lb. casei, Lb. alimentarius/kimchii, Lb. plantarum, Lb. sanfranciscensis

Randazzo et al., 2005

LAB: Lb. brevis, Lb. fermentum, Lb. plantarum, Lb. sanfranciscensis

Reale et al., 2005

LAB: Lb. brevis, Lb. casei, Lb. graminis, Lb. paracasei, Lb. plantarum, Leuc. mesenteroides

Ricciardi et al., 2005

LAB: Lb. alimentarius, Lb. brevis, Lb. casei, Lb. farciminis, Lb. pentosus, Lb. plantarum, Lb. sakei, Lb.
sanfranciscensis, Lb. zeae, Leuc. citreum, P. pentosaceus, W. confusa
LAB: Lb. alimentarius, Lb. brevis, Lb. curvatus/graminis/sakei, Lb. fermentum, Lb. paralimentarius, Lb. plantarum,
Lb. rossiae, Lb. sanfranciscensis, Leuc. citreum, P. pentosaceus, W. cibaria
Yeasts: C. humilis, K. exigua, P. kudriavzevii, S. cerevisiae, T. delbrueckii
Yeasts: C. humilis, S. cerevisiae

Catzeddu et al., 2006

LAB: Lb. brevis, Lb. farciminis, Lb. plantarum, Lb. sanfranciscensis, Leuc. mesenteroides
Yeasts: C. humilis, S. cerevisiae
LAB: Lb. curvatus, Lb. paraplantarum, Lb. pentosus, Lb. plantarum, Leuc. mensenteroides, W. cibaria
LAB: Lb. brevis, Lb. paralimentarius, Lb. plantarum, Lb. sanfranciscensis, Lc. lactis, Leuc. durionis, Leuc. fructosus,
P. pentosaceus, W. cibaria
Yeasts: C. humilis, S. cerevisiae
LAB: E. faecalis, Lb. brevis, Lb. casei, Lb. curvatus, Lb. fermentum, Lb. gallinarum, Lb. helveticus, Lb. paracasei
subsp. paracasei, Lb. paralimentarius, Lb. plantarum, Lb. rhamnosus, Lb. sakei, Lb. salivarius, Lb. sanfranciscensis,
Leuc. citreum, Leuc. pseudomesenteroides, W. cibaria, W. confusa
Yeasts: C. humilis, S. cerevisiae
LAB: Lb. sanfranciscensis, W. confusa

Gatto and Torriani, 2004

Valmorri et al., 2006,


2010
Lombardi et al., 2007
Garofalo et al., 2008
Zotta et al., 2008
Iacumin et al., 2009

Osimani et al., 2009

Siragusa et al., 2009

LAB: Lb. paralimentarius, Lb. plantarum, Lb. rossiae, Lb. sanfranciscensis, Lc. lactis subsp. lactis, P. pentosaceus,
W. cibaria, W. cibaria/confusa
LAB: Lb. brevis, Lb. plantarum
Yeasts: S. cerevisiae

Siragusa et al., 2009

LAB: Lb. alimentarius, Lb. brevis, Lb. paralimentarius, Lb. plantarum


Yeasts: S. cerevisiae

Zannini et al., 2009

LAB: Lb. plantarum, W. confusa

Coda et al., 2010

LAB: Lb. brevis, Lb. plantarum, W. confusa

Coda et al., 2010

LAB: Lb. plantarum, Lb. rossiae

Minervini et al., 2010

LAB: Lb. plantarum, P. pentosaceus

Minervini et al., 2010

LAB: Lb. plantarum, Lb. sanfranciscensis

Minervini et al., 2010

LAB: Lb. plantarum, Lb. rossiae, P. pentosaceus, W. confusa

Rizzello et al., 2010

Zannini et al., 2009

(continued on next page)

L. De Vuyst et al. / Food Microbiology xxx (2013) 1e19

Please cite this article in press as: De Vuyst, L., et al., Microbial ecology of sourdough fermentations: Diverse or uniform?, Food Microbiology
(2013), http://dx.doi.org/10.1016/j.fm.2013.06.002

Wheat (Molise)
Phenotypical molecular
Home-made sourdoughs
Phenotypical molecular
Wheat (Ferrara)
Phenotypical molecular
Wheat (panettone, pandoro, cornetto, colomba)
Phenotypical molecular
Wheat (Sicily)
Molecular
Wheat (Molise)
Phenotypical molecular
Wheat (Altamura, Apulia)
Phenotypical molecular
Wheat (Sardinia)
Molecular
Wheat (Abruzzo)
Physiological molecular

Country

Cereal our type


Method of identication

LAB and/or yeast species reported

Reference(s)

Wheat (Campania)
Molecular

LAB: Lactobacillus sp., Lb. casei, Lb. coryniformis, Lb. curvatus, Lb. plantarum, Lb. sakei/curvatus, Lb.
sanfranciscensis, Lc. lactis, Leuconostoc sp., Leuc. lactis, Leuc. (pseudo)mesenteroides, S. thermophilus, W. cibaria
Yeasts: S. cerevisiae, M. pulcherrima
LAB: Lb. brevis, Lb. casei, Lb. paracasei, Lb. plantarum

Palomba et al., 2011

Wheat (Molise)
Phenotypical molecular
Wheat (Pane di Altamura PDO)
Wheat (Pane di Laterza)
Wheat (Pane di Matera PGI)
Wheat (Pane Casereccio, Calabria)
Wheat (Pane Casereccio, Molise)
Wheat (Pane Casereccio, Genzano, PGI)
Wheat (Bozza Pratese)
Wheat (Pane di Altopascio Tradizionale)
Wheat (Pane di Terni)
Wheat (Bastone di Padova)
Wheat (Coppia Ferrarese, PGI)
Wheat (Pane Casereccio Marchigiano)
Wheat (Pane di Cappelli)
Wheat (Moddizzosu)
Wheat (Pane Carasau)
Wheat
Wheat
Wheat
Wheat

(Pane nero di Castelvetrano)


(Pane di Lentini)
(Pagnotta del Dittaino, PDO)
(South Italy)

Wheat (laboratory)

Iran
Ireland

Mexico

Wheat (mother sponges of Lagaccio from Liguria and Panettone


from Piemonte)
Phenotypical molecular
Wheat (sangak)
Phenotypical
Oat
Molecular
Oat e use of a starter (LAB: Lb. coryniformis, Leuc. argentinum,
P. pentosaceus, W. cibaria)
Molecular
Buckwheat e use of a starter (LAB: Lb. amylovorus, Lb. fermentum, Lb.
frumenti, Lb. helveticus, Lb. paracasei, Lb. paralimentarius, Lb.
plantarum, Lb. pontis, Lb. reuteri, Lb. sanfranciscensis, Leuc.
argentinum e Yeasts: C. humilis, S. pasteurianus)
Molecular
Teff e use of a starter (LAB: Lb. amylovorus, Lb. fermentum, Lb.
frumenti, Lb. helveticus, Lb. paracasei, Lb. paralimentarius, Lb.
plantarum, Lb. pontis, Lb. reuteri, Lb. sanfranciscensis, Leuc.
argentinum e Yeasts: C. humilis, S. pasteurianus)
Molecular
Buckwheat
Molecular
Teff
Molecular
Maize (pozol)
Phenotypical

Reale et al., 2011

LAB: W. cibaria, W. confusa


LAB: Lb. sanfranciscensis, Leuc. citreum
LAB: Lb. plantarum, Lb. sanfranciscensis, Leuc. citreum
LAB: Lb. sakei, Leuc. mesenteroides, Lb. sanfranciscensis
LAB: Lb. sanfranciscensis
LAB: Lb. plantarum, P. pentosaceus
LAB: Lb. paralimentarius, Lb. sanfranciscensis
LAB: Lb. gallinarum, Lb. sanfranciscensis
LAB: Lb. brevis, Lb. plantarum, Lb. sanfranciscensis, Lc. lactic subsp. lactis
LAB: Lb. paralimentarius, Lb. plantarum, Leuc. mesenteroides subsp. mesenteroides
LAB: Lb. paralimentarius, Lb. plantarum
LAB: Lb. casei, Lb. plantarum, Lb. sanfranciscensis, P. inopinatus
LAB: Lb. plantarum, Lb. sanfranciscensis
LAB: Lb. brevis, Lb. plantarum, Lb. rossiae, Lb. sanfranciscensis, P. argentinicus
LAB: Lb. brevis, Lb. plantarum, Lc. lactis subsp. lactis, Leuc. mesenteroides subsp. mesenteroides, P. pentosaceus,
W. paramesenteroides
LAB: Lb. paralimentarius, Lb. spicheri
LAB: Lb. namurensis, Lb. paralimentarius, Lb. plantarum, Lb. sanfranciscensis
LAB: Lb. sanfranciscensis, E. durans
LAB: Lb. casei, Lb. curvatus, Lb. plantarum, Lb. sakei, Lb. sanfranciscensis, Lc. lactis subsp. lactis, Leuc. citreum,
P. pentosaceus, W. cibaria
LAB: Lb. brevis, Lb. curvatus, Lb. parabrevis, Lb. plantarum, Lb. rossiae, Lb. sanfranciscensis, Lc. lactis subsp. lactis,
Leuc. citreum, P. pentosaceus
LAB: Lb. sanfranciscensis
Yeasts: C. milleri, S. cerevisiae

Minervini
Minervini
Minervini
Minervini
Minervini
Minervini
Minervini
Minervini
Minervini
Minervini
Minervini
Minervini
Minervini
Minervini
Minervini

et
et
et
et
et
et
et
et
et
et
et
et
et
et
et

al.,
al.,
al.,
al.,
al.,
al.,
al.,
al.,
al.,
al.,
al.,
al.,
al.,
al.,
al.,

2012a
2012a
2012a
2012a
2012a
2012a
2012a
2012a
2012a
2012a
2012a
2012a
2012a
2012a
2012a

Minervini
Minervini
Minervini
Minervini

et
et
et
et

al.,
al.,
al.,
al.,

2012a
2012a
2012a
2012b

LAB: Lb. brevis, Lb. plantarum, Leuc. mesenteroides, P. cerevisiae

Azar et al., 1977

LAB: Lb. coryniformis, Leuc. argentinum, P. pentosaceus, W. cibaria

Httner et al., 2010

LAB: Lb. coryniformis, Leuc. argentinum, P. pentosaceus, W. cibaria

Httner et al., 2010

LAB: Lb. amylovorus, Lb. brevis, Lb. fermentum, Lb. frumenti, Lb. paralimentarius, Lb. plantarum, Lb.
sanfranciscensis, Leuc. argentinum, W. cibaria
Yeasts: -

Moroni et al., 2010

LAB: Lb. amylovorus, Lb. brevis, Lb. fermentum, Lb. frumenti, Lb. paralimentarius, Lb. plantarum, Lb. pontis, Lb.
reuteri, Lb. sanfranciscensis, P. acidilactici
Yeasts: K. barnettii, S. cerevisiae

Moroni et al., 2010

LAB: Lb. crispatus, Lb. fermentum, Lb. gallinarum, Lb. graminis, Lb. plantarum, Lb. sakei, Lb. vaginalis, Leuc.
holzapfelii, P. pentosaceus, W. cibaria
Yeasts: K. barnettii
LAB: Lb. fermentum, Lb. gallinarum, Lb. pontis, Lb. vaginalis, Leuc. holzapfelii, P. pentosaceus
Yeasts: C. glabrata, S. cerevisiae
LAB: Lb. confusa, Lb. plantarum, Lc. lactis, Lc. rafnolactis, Leuc. mesenteroides

Moroni et al., 2011

LAB: E. saccharolyticus, Lb. casei, Lb. delbrueckii, Lb. fermentum, Lb. plantarum, S. bovis

Minervini et al., 2012b


Venturi et al., 2012b

Moroni et al., 2011


Nuraida et al., 1995

L. De Vuyst et al. / Food Microbiology xxx (2013) 1e19

Please cite this article in press as: De Vuyst, L., et al., Microbial ecology of sourdough fermentations: Diverse or uniform?, Food Microbiology
(2013), http://dx.doi.org/10.1016/j.fm.2013.06.002

Table 1 (continued )

Nigeria
Pakistan
Portugal

Romania

Russia
Spain

South Korea
Sudan

Sweden

Thailand
Turkey
USA

Maize rye (broa, Northern Portugal)


Phenotypical
Rye (laboratory e use of a starter; LAB: Lb. brevis, Lb. helveticus, Lb.
plantarum, Lc. lactis subsp. lactis, W. confusa e Yeasts: Kl. marxianus)
Rye (laboratory e use of a starter; LAB: Lb. helveticus e Yeasts: Kl.
marxianus)
Rye
Phenotypical
Wheat
Phenotypical
Wheat
Phenotypical
Wheat (laboratory e use of a starter; LAB: Leuc. citreum,
W. koreensis)
Sorghum (kisra)
Phenotypical
Sorghum (kisra)
Molecular
Rye-wheat
Phenotypical
Rye
Phenotypical
Wheat e use of a starter (LAB: Lb. casei, Lb. plantarum)
Phenotypical molecular
Wheat
Phenotypical
Wheat
Phenotypical
Wheat
Molecular

LAB: Lb. alimentarius, Lb. casei, Lb. delbrueckii, Lb. plantarum, Lc. lactis, S. suis

ben Omar and Ampe,


2000
Escalante et al., 2001

LAB: Lb. brevis, Lb. buchneri, Lb. casei, Lb. plantarum, Leuc. mesenteroides, Pediococcus spp.
Yeasts: C. humilis, S. cerevisiae
LAB: Lb. buchneri, Lb. casei, Lb. delbrueckii, Lb. plantarum, Lb. sanfranciscensis, Leuc. mesenteroides,
P. pentosaceus
LAB: Lb. brevis, Lb. casei, Lb. fermentum, Lb. plantarum, Leuc. mesenteroides, P. acidilactici

Edema and Sanni, 2006

Yeasts: S. cerevisiae

Saeed et al., 2009

Yeasts: Kl. marxianus, P. kudriavzevii, P. membranifaciens, S. cerevisiae, T. delbrueckii, W. anomalus

Almeida and Pais, 1996

LAB: E. casseliavus, E. durans, E. faecium, Lb. brevis, Lb. curvatus, Lc. lactis subsp. lactis, Leuconostoc spp.,
S. constellatus, S. equines
Yeasts: S. cerevisiae, T. delbrueckii, W. anomalus
LAB: Enterococci, lactobacilli, lactococci, leuconostocs, streptococci

Rocha and Malcata, 1999

LAB: Lb. brevis, Lb. helveticus, Lb. plantarum, Lc. lactis subsp. lactis, W. confusa
Yeasts: S. cerevisiae, Kl. marxianus
LAB: Lb. helveticus
Yeasts: Kl. marxianus
LAB: Lb. brevis, Lb. fermentum, Lb. plantarum
LAB: Lb. brevis, Lb. plantarum
Yeasts: S. cerevisiae
LAB: Lb. brevis, Lb. cellobiosus, Lb. plantarum, Leuc. mesenteroides
Yeasts: Meyerozyma guilliermondii, S. cerevisiae
Leuc. citreum, W. koreensis

Boraam et al., 1993


Faid et al., 1994

Rocha and Malcata, 2012


Banu et al., 2011
Banu and Aprodu, 2012
Kazanskaya et al., 1983
Barber et al., 1983
Barber and Bguena,
1988, 1989
Choi et al., 2012

LAB: Lb. amylovorus, Lb. fermentum, Lb. reuteri


Yeasts: P. kudriavzevii
LAB: E. faecalis, Lb. fermentum, Lb. helveticus, Lb. reuteri, Lb. vaginalis, Lc. lactis

Hamad et al., 1992

LAB: Lb. acidophilus, Lb. brevis, Lb. delbrueckii, Lb. farciminis, Lb. fermentum, Lb. plantarum, Lb. rhamnosus, Lb.
sanfranciscensis, W. viridescens
LAB: Lactobacillus sp., P. pentosaceus

Spicher and Lnner, 1985

LAB: Lb. casei/paracasei/zeae, Lb. paraplantarum/pentosus/plantarum


Yeasts: C. parapsilosis, C. tropicalis, P. kudriavzevii, S. cerevisiae
LAB: C. divergens, Lb. acetotolerans, Lb. amylophilus, Lb. brevis, Lb. plantarum, Lb. sakei, P. acidilactici,
P. pentosaceus, T. halophilus
LAB: Lb. sanfranciscensis
Yeasts: C. humilis
LAB: Lb. paralimentarius, Lb. plantarum, Lb. sanfranciscensis

Hamad et al., 1997

Lnner et al., 1986

L. De Vuyst et al. / Food Microbiology xxx (2013) 1e19

Please cite this article in press as: De Vuyst, L., et al., Microbial ecology of sourdough fermentations: Diverse or uniform?, Food Microbiology
(2013), http://dx.doi.org/10.1016/j.fm.2013.06.002

Morocco

Maize (pozol)
Phenotypical
Maize (pozol)
Molecular
Sourdough ferments, traditional starter sponges
Phenotypical
Soft wheat our
Phenotypical
Maize
Molecular
Wheat
Phenotypical
Rye maize wheat
Phenotypical
Maize (broa, Northern Portugal)
Phenotypical

Luangsakul et al., 2009


Gl et al., 2005
Kline and Sugihara, 1971;
Sugihara et al., 1971
Kitahara et al., 2005

LAB: C., Carnobacterium; E., Enterococcus; Lb., Lactobacillus; Lc., Lactococcus; Leuc., Leuconostoc; P., Pediococcus; S., Streptococcus; W., Weissella.
Yeasts: C., Candida; D., Debaryomyces; K., Kazachstania; Kl., Kluyveromyces; M., Metschnikowia; P., Pichia; S., Saccharomyces; T., Torulaspora; W., Wickerhamomyces.

L. De Vuyst et al. / Food Microbiology xxx (2013) 1e19

certain region-specic bakery products that are based on the use of


these stable characteristic sourdoughs, as backslopping results in
the prevalence of strains that are best adapted to the sourdough
ecosystem (Minervini et al., 2012b; Scheirlinck et al., 2009a).
Backslopped sourdough fermentation processes of this rst type
that are carried out in the laboratory, whereby our acts as the sole
non-sterile component, are characterized by a three-phase evolution of the growing microbial communities toward a stable ripe
active sourdough (Van der Meulen et al., 2007; Weckx et al., 2010b).
Whereas the our harbors several microorganisms, encompassing
several yeasts and bacteria including diverse LAB species, stability
of the sourdough ecosystem is reached within one week (Siragusa
et al., 2009; Van der Meulen et al., 2007; Weckx et al., 2010a, 2011).
Thereby, the type and quality (enzymatic, microbiological, nutritional, and textural qualities) of the cereal our used is of utmost
importance, as this raw material is indeed an important source of
nutrients (amino acids, fatty acids, minerals, vitamins, and other
growth factors), endogenous enzymes, and autochthonous LAB and
yeasts, the activity of some of which depends on the quality status of
the our and will determine the stability of the mature sourdoughs
(Van der Meulen et al., 2007; Vrancken et al., 2010). A combination
of culture-dependent (selective plating and incubation followed by
classication and identication of puried colonies with molecular
techniques) and culture-independent analyses [denaturing gradient
gel electrophoresis (DGGE) of rRNA-PCR amplicons of sample
community DNA] has been used to monitor the succession of the
microbiota in sourdough fermentation samples during backslopping. Atypical sourdough LAB such as Enterococcus species (also
present in the our) are found during the rst three days, followed
by gradual prevalence of typical sourdough LAB species belonging to
lactobacilli, leuconostocs, pediococci, and weissellas during the next
two days, and ultimately the prevalence of highly adapted and
sourdough-specic LAB species (e.g., Lactobacillus fermentum,
Lactobacillus plantarum, and Lactobacillus sanfranciscensis) after ve
to ten days of backslopping (Siragusa et al., 2009; Van der Meulen
et al., 2007; Weckx et al., 2010a,b). Also, microarray-based cultureindependent analysis based on metatranscriptome samples of
backslopped sourdough conrms this three-phase evolution of
sourdough fermentations toward a stable sourdough microbiota,
namely prevalence of Enterococcus spp., Lactococcus lactis, and
Leuconostoc mesenteroides in a rst phase; Pediococcus pentosaceus
in a second phase; and Lb. fermentum and Lb. plantarum in a third
phase of backslopping (Weckx et al., 2011).
A second type of sourdough fermentation processes based on
their inocula is the result of the addition of a starter culture to the
our-water mixture. In general, such fermentations are carried out
at higher temperature than backslopped ones and usually last for
one to three days. The nished sourdoughs are commercialized as
semi-liquid, heat-treated, or dried products (Gaggiano et al., 2007).
To this end, dened starter culture strains of, for instance, Lb. fermentum, Lb. plantarum, or Lb. sanfranciscensis are used, whether or
not accompanied with Saccharomyces cerevisiae. Most of these LAB
strains have been selected mainly based on their capacity to rapidly
acidify the our-water mixture and/or their ability to produce
specic avors. The latter property is of added value, which is reected in the commercialization of dried sourdough powders that
are used as non-living avor ingredients in bread production.
Alternatively, bakers can also buy starter cultures and perform
starter culture-added sourdough fermentations in their bakeries.
A third type of sourdough fermentation processes according to
the inoculum represents so-called mixed sourdough fermentation
processes, i.e., sourdoughs initiated with a LAB starter culture, followed by traditional backslopping. As is the case for backslopped
laboratory sourdough fermentations, starter culture-added backslopped sourdough fermentation processes are characterized by a

three-step evolution of the LAB communities, as described above


(Siragusa et al., 2009). In some cases, competition between the
spontaneously growing microbiota and the added sourdough
starter culture may lead to the dominance of autochthonous LAB
species and/or strains and hence eliminate the added started culture. This is possibly due to lack of adaptation of the starter culture
to the environmental conditions of the particular sourdough
ecosystem (Minervini et al., 2010; Moroni et al., 2010; Siragusa
et al., 2009).
3. Sourdough microbiota
The stable sourdough microbiota consists of particular yeast and
LAB species. Given the peculiarities of the sourdough ecosystem,
only ascomyceteous yeasts are found, because of their fermentative
ability in contrast to basidiomycetous yeasts and dimorphic ascomycetes. A review of 40 publications from 1970 onwards reveals the
following six yeast species that are often encountered in stable
sourdoughs: S. cerevisiae, Kazachstania exigua [synonym (syn.)
Saccharomyces exiguus; anamorph Candida (Torulopsis) holmii],
Candida humilis (syn. Candida milleri), Pichia kudriavzevii (syn.
Issatchenkia orientalis; anamorph Candida krusei), Torulaspora delbrueckii (anamorph Candida colliculosa), and Wickerhamomyces
anomalus (syn. Pichia anomala and Hansenula anomala; anamorph
Candida pelliculosa) (Huys et al., 2013). Only K. exigua (as S. exiguus)
was originally isolated from sourdough (Sugihara et al., 1971). Most
of these yeast species are found in other ecosystems as well. A
single sourdough usually harbors only one or two yeast species at a
given time, among which C. humilis (and K. exigua), P. kudriavzevii,
and S. cerevisiae occur most frequently (reported in >12 studies;
Vrancken et al., 2010).
Whereas the stability of some sourdoughs depends on the
specic cooperation between certain species of yeasts and LAB, the
presence of S. cerevisiae (bakers yeast) in most sourdoughs may be
ascribed to its presence in the bakery environment, at least when
bakers yeast is used. Also, bakery sourdoughs often harbor
W. anomalus, Kazachstania barnettii, Kazachstania unispora, and
T. delbrueckii (Daniel et al., 2011; Vrancken et al., 2010). In contrast,
backslopped laboratory sourdough fermentation processes are
dominated by W. anomalus, Candida glabrata, and S. cerevisiae
(Vrancken et al., 2010). Both S. cerevisiae and W. anomalus are
maltose-positive and to a certain extent tolerant toward a low pH
and high osmotic pressure. As K. exigua, K. barnettii is maltosenegative, implying a possible trophic relationship with Lb. sanfranciscensis (Vrancken et al., 2010).
With respect to the LAB communities, mostly heterofermentative LAB e in particular lactobacilli e occur in stable
sourdough ecosystems (Huys et al., 2013). Up to now, more than 60
species of lactobacilli (obligately homofermentative, facultatively
heterofermentative, and obligately heterofermentative ones) have
been isolated from sourdoughs. Obligately heterofermentative
lactobacilli are characteristic for sourdough fermentation processes, because of their highly adapted carbohydrate metabolism
(e.g., maltose fermentation ability of Lb. fermentum, Lactobacillus
reuteri, and Lb. sanfranciscensis), dedicated amino acid assimilation
[e.g., the arginine deiminase (ADI) pathway in Lb. fermentum and Lb.
reuteri], and stress responses (e.g., acidic stress response associated
with the ADI pathway and production of stress proteins) (Gnzle
et al., 2007; Gobbetti et al., 2005; Rollan et al., 2003). Whereas
weissellas (obligately heterofermentative; Weissella cibaria, Weissella confusa), pediococci (facultatively heterofermentative; Pediococcus acidilactici, P. pentosaceus), and leuconostocs (obligately
heterofermentative; Leuc. mesenteroides, Leuconostoc citreum) are
less predominant in sourdoughs, homofermentative lactococci,
enterococci, and streptococci are subdominant.

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Before 2000, the obligately homofermentative Lactobacillus


amylovorus, the facultatively heterofermentative Lactobacillus (par)
alimentarius and Lb. plantarum, and the obligately heterofermentative Lactobacillus brevis, Lb. fermentum, Lb. reuteri, Lactobacillus panis, Lactobacillus pontis, and Lb. sanfranciscensis
constituted the majority of the known sourdough LAB species. The
occurrence of these LAB species reects both their adaptability to
the prevailing sourdough fermentation conditions and their intraspecic heterogeneity. Whereas Lb. sanfranciscensis and Lb. (par)
alimentarius are almost solely associated with sourdoughs, Lb.
brevis and Lb. plantarum occur frequently in sourdoughs but have
often been isolated from other fermented foods as well. After 2000,
several new species of Lactobacillus have been isolated from sourdoughs, namely the homofermentative Lactobacillus crustorum,
Lactobacillus mindensis, Lactobacillus nantensis, and Lactobacillus
nodensis, the facultatively heterofermentative Lactobacillus spicheri,
and the obligately heterofermentative Lactobacillus acidifarinae,
Lactobacillus frumenti, Lactobacillus hammesii, Lactobacillus namurensis, Lactobacillus rossiae, Lactobacillus secaliphilus, Lactobacillus
siliginis, and Lactobacillus zymae. These LAB species were rst isolated from a sourdough habitat. Whether these LAB species are
specic for sourdoughs has to be unraveled further through
exploration of other fermented food ecosystems. For instance, it has
already been shown that Lb. namurensis can be retrieved from
diverse fermented foods (Miyashita et al., 2012; Sakamoto et al.,
2011). Nevertheless, Lb. rossiae is widespread in sourdoughs, being isolated from various sourdoughs in Central and Southern Italy,
Belgium, and elsewhere (Scheirlinck et al., 2009b). A single sourdough usually harbors several LAB species, which together represent a simple or a very complex microbial consortium.
Alternatively, competitiveness owing to the production of specic
antimicrobials may result in sourdoughs dominated by a single
species and/or strain, as is for instance the case for sourdoughs
harboring reutericyclin-producing Lb. reuteri (Gnzle and Vogel,
2003).
When considering the total microbial communities rather than
individual species, sourdough ecosystems are characterized by
stable associations of yeast and LAB species and/or of LAB species.
These microbial associations reect the metabolic capabilities of
the species involved and point toward trophic relationships that are
of importance in the sourdough ecosystem. Examples of stable
yeast-LAB associations are K. exigua (maltose-negative, acidtolerant) and Lb. sanfranciscensis (maltose-positive), C. humilis
(maltose-negative, acid-tolerant) and Lb. sanfranciscensis,
K. barnettii (maltose-negative) and Lb. sanfranciscensis, S. cerevisiae
(maltose-positive) and Lb. plantarum (prefers glucose and fructose)
(Corsetti and Settanni, 2007; Iacumin et al., 2009; Vrancken et al.,
2010), as well as the unique combination of S. cerevisiae, C. milleri
and Lb. sanfranciscensis (Venturi et al., 2012b). Examples of stable
LAB species associations include Lb. sanfranciscensis and either Lb.
plantarum, Lb. (par)alimentarius, or Lb. brevis (Corsetti et al., 2001;
Garofalo et al., 2008; Paramithiotis et al., 2010; Scheirlinck et al.,
2007c; Siragusa et al., 2009).
4. Region specicity seems to be an artifact
Whereas it has been initially thought that a relationship exists
between the geographical origin of a particular sourdough and its
associated microbiota, this apparent region specicity seems to be a
consequence of the interpretation of the concomitant research results (De Vuyst and Neysens, 2005; De Vuyst and Vancanneyt,
2007; De Vuyst et al., 2009). This can be ascribed to the methodology used for the isolation and the validity of the taxonomy of the
yeast and LAB genera/species involved. Hence, factors determining
sampling and identication procedures are of great inuence on

the correctness of the detection of the microorganisms involved


(Huys et al., 2013).
4.1. Sampling
As sourdough ecosystems harbor simple to very complex microbial consortia, it is likely that the constituting microorganisms
will vary in abundance and diversity in the sourdough raw materials, in the direct environment, and during processing. Hence,
appropriate sampling is of utmost importance, in particular with
respect to the number of samples as a whole. Moreover, the
analysis of a dynamic process such as a sourdough fermentation
requires multiple samples at different time points, taking into
account important factors such as the backslopping procedure, the
dough characteristics (temperature, pH, dough yield, etc.), and
parameters of the production environment (temperature, hygienic
status, house microbiota, etc.). In addition, single isolations of
yeast and LAB species and/or strains should be avoided, either by
an appropriate ad random isolation (not always based on colony
morphology) or e much better e according to a statistically relevant procedure (e.g., always picking up the same percentage of
colonies of a certain dilution). In addition, isolates from single
habitats should not be linked to that habitat after one study. As an
example, the direct association of Lb. spicheri with German rice
sourdoughs (Meroth et al., 2004) represents an accidental discovery (Vogelmann et al., 2009).
4.2. Isolation and identication
Another factor determining the correctness of the microbiotasourdough link is the way that the microorganisms are characterized taxonomically, either through culture-dependent or cultureindependent approaches (De Vuyst and Vancanneyt, 2007; Huys
et al., 2013). Culture-dependent techniques assume cultivability
of the sourdough microorganisms to make their isolation possible,
which is based on prior knowledge of their presence, the use of
appropriate and selective culture media (taking into account specic nutrients, interactive effects, etc.), the application of appropriate incubation conditions (temperature, pH, atmosphere, etc.),
and the occurrence of microbial interdependence (cf. yeast-LAB and
LABeLAB associations). Furthermore, accurate identication of
unknown isolates requires specic expertise, e.g., the use of
methods that offer sufcient taxonomic resolution and the correct
interpretation of the identication results by comparison with
complete up-to-date accurate databases. Identication of pure
colonies may involve phenotypic characterizations, encompassing
morphological and physiological characteristics (e.g., assimilation/
fermentation of carbon/nitrogen sources) in the case of yeasts and
physiological tests (e.g., major fermentation pathways, carbohydrate utilization patterns, and enzymatic properties) in the case of
LAB. Molecular DNA-based methods (DNA ngerprinting and
sequencing) have become the essential complement for the identication of yeasts and LAB. Compared to phenotyping methods,
molecular DNA-based identication methods offer a much higher
taxonomic resolution at species up to strain level. Cultureindependent methods are based on the phylogenetic dissection of
metagenomic DNA extracted directly from the sample. This DNA
should be of high quality. A possible disadvantage is that it may also
include free extracellular DNA and DNA from dead microorganisms.
These methods allow sequence-based community proling (species diversity, community dynamics, adaptation ability, source
tracking) and/or functional gene assessment. Noteworthy, DGGE
may miss subdominant species, offers inadequate resolution of
phylogenetically closely related species, and may be subjected to
bias by differences in 16S rRNA gene copy number, preferential PCR

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L. De Vuyst et al. / Food Microbiology xxx (2013) 1e19

amplication, inadequately standardized electrophoresis conditions, and the occurrence of heteroduplex bands for the same
species. The use of microarrays is limited to the identication of
known species because of prior probe design, during which
attention should go to the avoidance of inter-species cross-hybridization events. Finally, next-generation sequencing results are
biased by the choice and selectivity of the primers used in the case
of targeted approaches, sequencing depth and read length, and
algorithms and databases available and used for post-sequencing
data analysis.
4.3. Problematic identications
Based on the literature review of sourdough yeasts mentioned
above and comparing studies using phenotypic identication
techniques (n 19) with those using DNA-based techniques
(n 23), the incidence of C. humilis isolates has increased markedly
in the latter studies, probably at the cost of a decreased frequency of
detecting K. exigua. These two phylogenetically closely related yeast
species may be mistaken for each other when only phenotypical
identication methods are used. For instance, originally, S. exiguus
was isolated from San Francisco sourdough (Sugihara et al., 1971),
while C. milleri was reported from various sourdoughs produced in
Italy (Ottogalli et al., 1996; Valmorri et al., 2010; Venturi et al.,
2012b). Some strains of S. exiguus from the study of Sugihara
et al. (1971) that were preserved in culture collections later
served for the description of C. milleri, currently a synonym of
C. humilis. The reassignment of S. exiguus strains to C. milleri was
based on the signicantly higher guanine-plus-cytosine contents in
selected San Francisco sourdough strains compared to the type and
other reference strains of S. exiguus. However, the sourdough
isolate M14 initially reported as S. exiguus (and also deposited as
CBS 7901) was later considered as a member of C. humilis after
DNA-based analyses (Gobbetti et al., 1994a; Meroth et al., 2003a).
Actually, the yeast species complex C. humilis/C. milleri was placed
in the articial genus Candida, because no sexual reproduction
could be found. Phylogenetically, C. humilis/C. milleri belongs to the
same group as the genus Kazachstania (Kurtzman, 2003), but it has
not yet been transferred to this genus mainly because the phylogenetic reclassication of yeasts is treating sexually reproducing
taxa with priority. Anyway, C. humilis and C. milleri are indicated to
be conspecic (Daniel and Meyer, 2003; Meyer et al., 1998;
Vaughan-Martini, 1995). Moreover, a continuum of internal transcribed spacer (ITS) sequence variants between both type strains
exists, making allocation of sourdough isolates of these species to
one of them difcult. These data suggest that C. humilis and
C. milleri may be considered as one species, and because C. humilis
and K. exigua are closely related phylogenetically, it is likely that
K. exigua may be a sourdough-specic yeast species. Additionally,
K. barnettii might have been misidentied as K. exigua or
S. cerevisiae in studies only using phenotypical identication
methods.
Similarly, the LAB species responsible for acidication of San
Francisco sourdough was named Lactobacillus sanfrancisco (Kline
and Sugihara, 1971; Sugihara et al., 1971), whereas that responsible for the acidication of various sourdoughs produced in Italy
was identied as Lb. brevis var. lindneri (Gobbetti et al., 1994b;
Ottogalli et al., 1996). However, both LAB species have been
shown to be synonymous and now considered members of Lb.
sanfranciscensis (Weiss and Schillinger, 1984). Although Lb. sanfranciscensis can be misidentied as Lb. brevis (De Vuyst et al.,
2002), molecular techniques exist for its unequivocal identication (Picozzi et al., 2006; Zapparoli and Torriani, 1997). Furthermore, Lb. plantarum, Lactobacillus paraplantarum, and Lactobacillus
pentosus are phylogenetically closely related, whose taxonomic

resolution requires sequence analysis of the DNA repair and


maintenance gene, recA (de las Rivas et al., 2006; Torriani et al.,
2001; Settanni et al., 2005). Similarly, the LAB species pairs Lb.
alimentarius and Lactobacillus paralimentarius (De Vuyst et al.,
2002), Lactobacillus sakei and Lactobacillus curvatus (Berthier
and Ehrlich, 1999; Chaillou et al., 2009), P. acidilactici and
P. pentosaceus (Nigatu et al., 1998), and W. cibaria and W. confusa
(Bjrkroth et al., 2002; De Vuyst et al., 2002) all require appropriate DNA ngerprint- or sequence-based methods for an
adequate identication. Therefore, it is likely to assume that some
of the Lactobacillus species previously reported in sourdough
ecosystems may have been misidentied at the species or even at
the genus level.
Finally, also intra-species heterogeneity may contribute to difculties with identication. For instance, in the case of Lb. rossiae,
sub-specic clusters can be distinguished based on sequencing of
the phenylalanyl-tRNA synthase gene, pheS, which however do not
correlate with the sourdough origin (Di Cagno et al., 2007;
Scheirlinck et al., 2009b). Also, Lb. sanfranciscensis (Foschino et al.,
2001; Kitahara et al., 2005; Picozzi et al., 2010; Siragusa et al.,
2009; Venturi et al., 2012a; Zapparoli et al., 1998), Lb. plantarum
(Minervini et al., 2010; Pepe et al., 2004; Reale et al., 2011; Siezen
et al., 2010), Lb. sakei (Chaillou et al., 2009; Ravyts and De Vuyst,
2011), Lactobacillus helveticus (Viiard et al., 2012), Leuc. mesenteroides (Villani et al., 1997), and P. acidilactici (Mora et al., 2000)
display an intra-species heterogeneity, making technologically
relevant applications strain-dependent. In this context, it is worth
to mention that also a large strain diversity of S. cerevisiae occurs in
single sourdoughs (as it is the case in many other ecosystems),
suggesting an autochthonous wheat/rye our origin of this yeast
species (Meroth et al., 2003a; Pulvirenti et al., 2001, 2004).
5. Region-specic considerations
The (unique) presence of Lb. sanfranciscensis in San Francisco
sourdough should be ascribed to factors that are mainly based on
the fermentation technology and practical conditions applied.
Although initially associated with wheat sourdoughs solely (Picozzi
et al., 2006), this LAB species has also been found in rye (Spicher
and Schrder, 1978), spelt (Scheirlinck et al., 2007c, 2008), and
teff sourdoughs (H. Harth & L. De Vuyst, unpublished results). In
addition, it has been isolated from the insect gut (Groenewald et al.,
2006). Lb. sanfranciscensis optimally grows at 32  C (Brandt et al.,
2004; Gnzle et al., 1998), at pH 5.0 (but not below pH 3.8e4.0;
Brandt et al., 2004; Gnzle et al., 1998), is sensitive to a low water
activity (Venturi et al., 2012b), and is involved in a mutualistic
interaction with C. humilis (optimal at 25e30  C, stable at 20e30  C;
Gnzle et al., 1998; Vogelmann and Hertel, 2011). These properties
are reected in the fermentation technology applied for sourdough
production involving Lb. sanfranciscensis, namely backslopping
practices with short fermentation times and long resting times at
low temperature (or long fermentation times with temperature
adaptation) and specic bakery conditions (dough yield, temperature of dough incubation, dough pH, .). Hence, the presence of Lb.
sanfranciscensis during sourdough fermentation depends on specic environmental and technological factors.
Rye sourdoughs are typical sourdoughs of Northern Europe,
bakeries making use of the local rye cereal. Rye our needs to be
fermented to inhibit endogenous amylase activity and to improve
its baking quality for breadmaking. As one of the prevalent sourdoughs, they are studied since many years (Table 1). Several multistep processes exist, differing in the number of steps, the applied
fermentation temperatures and times, dough yield, etc. A typical
German three-step process starts from an initial starter, which allows build-up of the sourdough through three refreshments

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L. De Vuyst et al. / Food Microbiology xxx (2013) 1e19

11

(Neumann et al., 2006). Rye sourdoughs are characterized by the


presence of Lb. brevis, Lb. fermentum, Lb. plantarum, and Lb. sanfranciscensis; also, amylolytic LAB species, such as Lb. acidophilus
and Lb. amylovorus, are sometimes reported (Banu et al., 2011;
Kazanskaya et al., 1983; Kitahara et al., 2005; Lnner et al., 1986;
Mller et al., 2001; Rosenquist and Hansen, 2000; Salovaara and
Savolainen, 1984; Spicher, 1984; Spicher and Lnner, 1985;
Spicher and Schrder, 1978; Vogelmann and Hertel, 2011).
Belgian bakery sourdoughs have been analyzed extensively only
recently (Table 1; Scheirlinck et al., 2007c, 2008, 2009a,b). They are
characterized by simple to very complex communities of LAB species, encompassing Lb. fermentum, Lb. hammesii, Lb. paralimentarius,
Lb. plantarum, Lb. pontis, Lb. sanfranciscensis, and W. cibaria. S. cerevisiae and W. anomalus are the dominating yeasts in Belgian bakery sourdoughs. Sourdoughs with both stable large and stable
restricted species diversities occur. In this way, it has been shown
that previous introduction of our into the bakery environment
helps to build up a so-called house microbiota that serves as an
important inoculum for subsequent sourdough fermentations
(Scheirlinck et al., 2009a). Indeed, LAB strains adapted to the
sourdough and bakery environment (apparatus, air, etc.), which
have been shown to be genetically indistinguishable, may be
repetitively introduced in consecutive sourdough batches during
backslopping (Scheirlinck et al., 2009a). No obvious correlation
with the type of our or technological factors (temperature, pH,
fermentation time) occurs (Scheirlinck et al., 2007c).
Italian sourdoughs have been studied for years (Table 1). Several
recent studies have dealt with region-specic sourdoughs, claiming
a specic sourdough microbiota, such as in the case of Pane di
Matera with protected geographic indication (Lb. plantarum, Leuc.
mesenteroides; Zotta et al., 2008), Molise sourdough (Lb. brevis, Lb.
plantarum; Reale et al., 2011), and Pane di Altamura with protected
designation of origin (PDO) (Lb. plantarum; Ricciardi et al., 2005).
However, this relationship between region-specic sourdoughs
and their associated microbiota is not clear-cut. In contrast, as for
the Belgian sourdoughs, Italian sourdoughs can harbor simple to
very complex communities of LAB species, depending on the nal
products examined, among which Lb. brevis, Lb. fermentum, Lb. (par)
alimentarius, Lb. plantarum, Lb. sanfranciscensis, P. pentosaceus, and
W. confusa are widespread (reported in >30 studies). The nineteen
Italian sourdoughs dealt with in the recent study of Minervini et al.
(2012a) conrm the presence of various numbers of LAB species, in
particular Lb. sanfranciscensis, Lb. plantarum, and Lb. paralimentarius, thereby indicating that there are no common LAB species
found. Moreover, their results either conrm or contradict those of
earlier studies. For instance, this study reports that Pane di Altamura PDO sourdough is dominated by W. cibaria instead of Lb.
plantarum. Finally, C. humilis, K. barnettii, K. exigua, and S. cerevisiae
are the dominating yeasts in Italian bakery sourdoughs. Based on all
these studies, it is interesting to see that S. cerevisiae mostly occurs
in sourdoughs from Central and South Italy, perhaps because of the
use of bakers yeast (Succi et al., 2003). Also, an interesting nding
is that sourdoughs made from Triticum durum mainly harbor obligately heterofermentative LAB species and are characterized by low
yeast counts and high levels of maltose, glucose, fructose and free
amino acids that contribute to this LAB/yeast ratio. In contrast,
sourdoughs made from Triticum aestivum harbor mainly facultatively heterofermentative LAB species. Hence, the Italian sourdough
studies indicate an inuence of the our type on the sourdough
microbiota, supported by the bakery technologies applied.

and bakery practices applied determine the stability and persistence of the yeast and LAB communities involved in (region-specic) sourdough fermentation processes. Of course, the use of
certain raw materials, encompassing cereal types and other ingredients such as adjunct carbohydrates, salt, yoghurt, herbs, fruits,
etc., and process parameters such as dough yield and refreshment
times, may be part of specic recipes of a region and hence be
linked to local traditions of that region. Also, they may favor
particular microorganisms as a result of trophic and metabolic
cooperations and interactions and, hence, may associate specic
LAB and/or yeast species with specic sourdoughs of certain
geographical regions. As an example, the presence of the yeast
Metschnikowia pulcherrima in a sourdough destined for a sweet
baked product has been linked with its occurrence on fruits present
in the bakery environment (Palomba et al., 2011).
Whether the nature of the our mainly directs the growth of
sourdough LAB species remains controversial. Of course, the our
plays a key role in establishing stable microbial consortia within a
short time, as described above, and only species and/or strains
adapted to the sourdough environment with respect to the nutrient
availability in and physicochemical parameters of the our will
thrive in this ecosystem. Therefore, among other mechanisms,
competitiveness may explain the apparent prevalence of certain
LAB species and/or strains in specic sourdough fermentations, as
evidenced by single reports on Lb. helveticus in sorghum sourdoughs (Hamad et al., 1997), Lb. amylovorus or Lb. helveticus in rye
sourdoughs (Mller et al., 2001; Viiard et al., 2012), Lb. sakei in
amaranth sourdoughs (Sterr et al., 2009), and Lb. pontis in teff
sourdoughs (Moroni et al., 2011). Particular conditions may have
selected for these microorganisms; for instance, the presence of bglucan may select for b-glucan-degrading LAB species such as Lb.
brevis during barley fermentation (Zannini et al., 2009). However,
these LAB species are not specic for the concomitant sourdough
ecosystems. In contrast, it has been shown that the LAB species Lb.
fermentum and Lb. plantarum dominate the majority of sourdough
fermentation processes, irrespective of the type of our or the
addition of starter cultures that are not robust enough (Moroni
et al., 2010; Van der Meulen et al., 2007; Vogelmann et al., 2009).
It indicates their presence in the cereal ours and on the surfaces of
the concomitant plants. In contrast, the prevalence of Lb. sanfranciscensis depends on appropriate environmental conditions,
albeit that logically it should be present in the our to be found in
the ripe sourdough. Hence, the microbial composition of the our is
of great importance. Also, accidental contamination of the our
from the direct environment (apparatus, air, etc.) determines its
microbial load and thus that of the sourdough fermentation
(Scheirlinck et al., 2009a). Finally, it is likely to assume that sourdough LAB, such as Lactobacillus acidophilus, Lactobacillus johnsonii
as well as Lb. rossiae and Lb. sanfranciscensis, may be of intestinal
origin, owing to fertilization practices on the grain elds;
contamination with mouse and rodent feces of elds, mills, and
apparatus, or the presence of insects in the our mills; as well as to
fecal contamination of the direct sourdough environment (bakerys
hygiene) (De Angelis et al., 2006; Du Toit et al., 2001, 2003;
Ehrmann and Vogel, 2005; Groenewald et al., 2006; Park and
Itoh, 2005; Vrancken et al., 2011). In this way, it is interesting to
see that the frequent sourdough inhabitant, Lb. reuteri, may originate from rodent intestines (Su et al., 2012).

6. Origin of the sourdough microbiota

For details, the reader is referred to Table 1.


Most sourdoughs are prepared from wheat and rye our. Also,
maize and cassava are used for the production of sourdough-like
fermented food products. Few reports exist on the use of barley,

From the above, it is likely to assume that the dedicated use of


certain basic raw materials as well as the technological procedures

7. Inuence of our

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L. De Vuyst et al. / Food Microbiology xxx (2013) 1e19

emmer, millet, oat, rice, and teff to perform sourdough fermentations. Besides cereals, pseudocereals such as buckwheat, amaranth,
and quinoa can be used as the raw material for sourdough
fermentation. In contrast to wheat, rye, and barley, where different
parts of the kernel can be fractionated, the whole kernel is used in
the case of teff because of its small size. However, bran fermentation may have a different impact on the resulting ripe sourdough,
given the presence of dietary ber and bioactive compounds that
are concentrated in the bran fraction (Katina et al., 2007, 2012;
Liukkonen et al., 2003; Poutanen et al., 2009; Rizzello et al., 2010;
Ross et al., 2004).
As mentioned above, the chemical composition and quality
status of the our determine the community dynamics and
metabolite kinetics of sourdough fermentation processes. With
respect to the microorganisms involved, on the basis of a survey of
87 publications, Lb. plantarum, Lb. brevis, Lb. fermentum, and Lb.
sanfranciscensis are the prevailing LAB species during sourdough
fermentation, irrespective of the our type used. In particular, Lb.
plantarum, Lb. brevis, Lb. sanfranciscensis, Lb. fermentum, and Leuc.
mesenteroides are reported in 38 publications on wheat sourdough
and Lb. plantarum, Lb. brevis, Lb. fermentum, and Lb. sanfranciscensis
are reported in 12 publications on rye sourdough.
Concerning the microbial diversity in buckwheat, amaranth, and
quinoa, no straightforward conclusions can be made due to the low
number of publications available. Overall, the presence of Lb.
plantarum, Lb. fermentum, Lb. paralimentarius, and Lb. helveticus has
been reported. In addition, Lb. fermentum and Lb. plantarum are
found in teff, spelt, rice, oat, millet, maize, cassava, barley and
amaranth sourdoughs, but are never found in emmer sourdoughs.
Also, Lb. brevis has been isolated from teff, spelt, maize, and barley
sourdoughs, but is not found in rice, oat, millet, emmer, cassava,
and amaranth sourdoughs. Isolates identied as Lb. sanfranciscensis
have been retrieved from teff and spelt sourdoughs but not from
rice, oat, millet, maize, emmer, cassava, barley, and amaranth
sourdoughs. Although Lb. helveticus has been found in rye, barley,
cassava, oat, millet, and maize sourdoughs, it has not been found in
rice, spelt, teff, and emmer sourdoughs. Lb. paralimentarius, one of
the most abundant LAB species in sourdough fermentations, has
not been found in oat, emmer, and cassava sourdoughs.
8. Inuence of process parameters
For details, the reader is referred to Tables 2 and 3.
According to the process technology applied, distinction can be
made between type 0, I, II, and III sourdoughs (Huys et al., 2013).
Type 0 sourdoughs are pre-doughs, in which LAB contaminating
the faster growing bakers yeast develop to favor avor formation.
Type I or traditional sourdoughs are usually rm doughs with a low
dough yield that are daily backslopped at ambient temperature to
keep the microorganisms in an active state. Type II sourdoughs are
industrial semi-liquid sourdoughs that are usually performed as
one-step propagation processes of long duration and with high
water content at temperatures above 30  C to enhance acidication.
They are used as dough acidiers or avor ingredients. Type III
sourdoughs are dried sourdoughs to be used as a non-living acidier supplement and avor carrier. In contrast to type I doughs,
doughs of types II and III require the addition of bakers yeast for
leavening.
Process parameters such as, but not limited to, fermentation
temperature and time, leavening temperature and time, storage
temperature and time; pH, redox potential, water activity, dough
yield; refreshment time and number of refreshment steps, mixing,
and aeration of the initial dough determine the progress and
outcome of (backslopped) sourdough fermentation processes (De
Vuyst and Neysens, 2005; Gnzle et al., 2007; Gobbetti et al.,

2005; Hammes et al., 2005). It is, however, difcult to study the


inuence of these factors independently, irrespective of the use of
simulation media or actual sourdoughs, either laboratory sourdoughs or bakery sourdoughs, as some inuences cannot easily be
accounted for (kneading practices, disinfection procedures, irregularities in refreshments, temperature proles, etc.) (Minervini
et al., 2012b; Picozzi et al., 2010; Vera et al., 2012; Vernocchi
et al., 2008; Viiard et al., 2012). In fact, every treatment or manipulation might inuence the microorganisms involved by acting as
an additional stress factor (Serrazanetti et al., 2009). Finally, despite
the dynamic nature of sourdough fermentations, a lack of dynamic
studies impedes the elucidation of the exact relationships between
the application of certain process factors and the nal microbial
communities in the resulting ripe sourdoughs (Mller et al., 2001;
Vera et al., 2012).
8.1. Temperature
The fermentation temperature is an important determinant of
the community dynamics and metabolite kinetics of a sourdough
fermentation process (Banu et al., 2011; Decock and Cappelle,
2005; Katina et al., 2006; Vogelmann and Hertel, 2011). It affects the ratio of lactic acid to acetic acid, the so-called fermentation quotient, whereby a shift toward lactic acid production
occurs at high fermentation temperatures, favoring acidication.
Alternatively, low fermentation temperatures favor yeast growth,
ethanol production, and avor formation. Indeed, homofermentative (and facultatively heterofermentative) LAB species,
often prevailing in sourdoughs produced at high temperatures
and with short fermentation times, cause a fast acidication of the
our-water mixture and produce mainly lactic acid. Heterofermentative LAB species prevail in sourdoughs at low temperatures and with long fermentation times and produce a mixture of
lactic acid, acetic acid, and/or ethanol upon fermentation. In this
way, literature data indicate a positive correlation between low to
moderate fermentation temperatures (<30  C) and the presence
of Lb. sanfranciscensis and a negative correlation between these
fermentation temperatures and the presence of Lb. fermentum and
Lb. plantarum. This is in accordance with the prevalence of Lb.
sanfranciscensis in artisan type I sourdoughs, whereby the association Lb. sanfranciscensiseC. humilis is optimal at 25e30  C. In
contrast, Lb. fermentum prefers higher temperatures (as in type II
sourdoughs) (Gnzle et al., 1998; Moroni et al., 2011; Vogelmann
and Hertel, 2011). This has been illustrated by backslopping experiments of liquid wheat sourdoughs at laboratory scale, which
lead to the dominance of Lb. fermentum at 30  C and 37  C, while
Leuc. citreum prevails at 23  C (Vrancken et al., 2011). This has also
been demonstrated for bakery wheat sourdoughs (Ferchichi et al.,
2008). Similarly, rye fermentations initiated with commercial
sourdough starter cultures maintain the presence of Lb. mindensis
and Lb. sanfranciscensis at 25  C (type I), but select for other LAB
species at 30  C and 40  C (both type II) (Meroth et al., 2003b).
Nevertheless, seasonal or daily temperature changes might inuence the resulting community dynamics as well, as illustrated
by the presence of Lb. frumenti and Lb. panis in a French type I
wheat sourdough made at environmental temperature (Vera et al.,
2012). Similarly, the fermentation temperature may be responsible for the selection toward Lb. helveticus during Sudanese sorghum sourdough fermentations at high ambient temperature
(Hamad et al., 1997) and toward Lb. amylovorus during rye sourdough fermentations at high temperature (Mller et al., 2001).
Finally, high fermentation temperatures might be detrimental for
the yeast metabolism, due to the high acidity caused by an
enhanced LAB metabolism at these temperatures, as sourdough
yeasts tend to be sensitive to non-dissociated acetic acid and, to a

Please cite this article in press as: De Vuyst, L., et al., Microbial ecology of sourdough fermentations: Diverse or uniform?, Food Microbiology
(2013), http://dx.doi.org/10.1016/j.fm.2013.06.002

L. De Vuyst et al. / Food Microbiology xxx (2013) 1e19

13

Table 2
Lactic acid bacteria species diversity in (backslopped) bakery or household sourdoughs grouped as a function of the process parameters dough yield, temperature and
fermentation time (nd: not dened; 0: spontaneous; 1: starter culture added; RT: room temperature). Entries are ranked as a function of dough yield, temperature, and
fermentation time. Species are ranked in order of the number of sourdoughs in which they were detected, as indicated by the number between brackets; no number is
mentioned for single detections.
Dough
yield

Temperature
( C)

Fermentation
time (h)

Number of
sourdoughs
analyzed

Species diversity

Reference

nd
nd
nd
nd
nd
nd
nd
nd
nd
nd
nd
nd

7e8
8e10
9
11
13
16
18
20
20
20
20e25
20e28

14
15e17
24
15
20
12
24
18
20
24
4e5
nd

1
1
1
1
1
1
1
1
1
2
1
18

Ferchichi et al., 2007


Osimani et al., 2009
Minervini et al., 2012a
Minervini et al., 2012a
Venturi et al., 2012b
Minervini et al., 2012a
Ferchichi et al., 2007
Corsetti et al., 2001
Osimani et al., 2009
Corsetti et al., 2001
Osimani et al., 2009
Robert et al., 2009;
Reale et al., 2011

nd

20e30

16

nd

22

nd

nd
nd
nd
nd
nd
nd

22
22
22
22
22
22

5
6
10
11
12
14

1
1
1
1
1
2

nd
nd
nd

22
23
23e28

16
6
6

2
1
20

nd
nd
nd

24
24
25

14
24
3

1
2
7

nd
nd
nd
nd
nd

25
25
25
25
25

5
6
7e8
9
10

1
2
1
1
4

nd
nd
nd
nd
nd

25
25
25
25
25

11
12
15
24
48

1
2
1
3
1

nd

26

nd

nd
nd
nd
nd
nd

26
26
26
27
27

4
8
10
4
11

1
1
1
1
1

nd

27

18

nd
nd

27
28

24
nd

1
9

nd
nd

28
30

6
nd

1
4

nd
nd
nd

30
30
30

3e24
6e7
48e72

3
1
1

Leuc. mesenteroides, Lb. sanfranciscensis


Lb. fermentum, Lb. plantarum, W. confusa
Lb. gallinarum, Lb. sanfranciscensis
Lb. paralimentarius, Lb. sanfranciscensis
Lb. sanfranciscensis
Lb. brevis, Lb. plantarum, Lb. sanfranciscensis, Lc. lactis
Lb. hammesii, Lb. nantensis, Lb. panis, Lb. sanfranciscensis
Lb. plantarum
Lb. casei, Lb. curvatus, Lb. plantarum, Lb. sanfranciscensis, Leuc. citreum
Lb. plantarum (2/2), Lb. alimentarius, Lb. brevis, Lb. fermentum, Lb. sanfranciscensis
Lb. curvatus, Lb. plantarum, S. salivarius, W. cibaria, W. confusa
Lb. plantarum (13/18), Lb. brevis (7/18), P. pentosaceus (7/18), Lb. casei (4/18), Leuc.
citreum (4/18), Leuc. mesenteroides (4/18), Lb. curvatus (3/18), Lb. sanfranciscensis
(3/18), W. cibaria (2/18), Lb. casei/paracasei, Lb. paraplantarum, Lb. pentosus, Lb. sakei,
Lc. lactis, W. confusa
W. cibaria (3/5), Lb. plantarum (2/5), Lb. sanfranciscensis (2/5), Lactobacillus sp. (2/5),
Leuc. lactis (2/5), Lb. casei, Lb. coryniformis, Lb. curvatus, Lb. curvatus/sakei, Lc. lactis,
Leuc. mesenteroides, Leuc. pseudomesenteroides, Leuconostoc sp., S. thermophilus
Lb. plantarum (2/3), Lb. sanfranciscensis (2/3), P. pentosaceus (2/3), W. cibaria (2/3), Lb.
sakei, Lb. paralimentarius, Lb. curvatus
E. durans, Lb. sanfranciscensis
Lb. sakei, Lb. sanfranciscensis, Leuc. mesenteroides
Lb. sanfranciscensis
Lb. brevis, Lb. plantarum, Lb. rossiae, Lb. sanfranciscensis, P. argentinicus
Lb. paralimentarius, Lb. plantarum
Lb. brevis (2/2), Lb. plantarum (2/2), Lb. sanfranciscensis (2/2), Lb. paralimentarius,
Leuc. durionis, P. pentosaceus, W. cibaria
Lb. brevis (2/2), Lb. plantarum (2/2), Lb. sanfranciscensis (2/2), F. fructosus, Lc. lactis
Lb. casei, Lb. plantarum, Lb. sanfranciscensis, P. inopinatus
Lb. plantarum (16/20), Lb. sanfranciscensis (15/20), Lb. brevis (13/20), Lb.
paralimentarius (6/20), Lb. curvatus/graminis/sakei (6/20), Lb. fermentum (3/20), Lb.
rossiae (3/20), W. cibaria (2/20), Lb. alimentarius
Lb. sanfranciscensis
Lb. alimentarius (2/2), Lb. sanfranciscensis (2/2)
Lb. sanfranciscensis (4/7), Leuc. citreum (4/7), Lb. alimentarius (2/7), Lb. brevis (2/7), Lc.
lactis (2/7), Lb. plantarum, W. confusa
Lb. sanfranciscensis
Lb. sanfranciscensis (2/2), Leuc. citreum (2/2), Lb. plantarum
E. faecalis, Lb. gallinarum, Lb. paralimentarius, Lb. plantarum
Lb. alimentarius
W. cibaria (3/4), Lb. plantarum (2/4), P. pentosaceus (2/4), E. hirae, Lb. brevis, Lb.
curvatus, Lb. fermentum, Lb. sanfranciscensis, Leuc. citreum, Leuc. mesenteroides,
W. confusa
Lb. namurensis, Lb. paralimentarius, Lb. plantarum, Lb. sanfranciscensis
Lb. acidophilus, Lb. alimentarius, Lb. brevis, Lb. plantarum, Lc. lactis
Lb. brevis, Lb. sanfranciscensis, Leuc. citreum
Lb. sanfranciscensis (3/3), Lb. alimentarius (2/3), Lb. brevis, Leuc. citreum
Lb. helveticus, Lb. paracasei, Lb. paralimentarius, Lb. plantarum, Leuc.
pseudomesenteroides
Lb. brevis (3/3), Lb. paralimentarius (3/3), Lb. fermentum (2/3), Lb. pontis (2/3), Lb.
paracasei, Lb. rossiae, P. acidilactici, P. pentosaceus, W. confusa
Lb. plantarum, Lb. sanfranciscensis
Lb. pontis, Lb. sanfranciscensis, Lb. spicheri
Lb. paralimentarius, Lb. spicheri
Lb. sanfranciscensis
Lb. brevis, Lb. plantarum, Lc. lactis, Leuc. mesenteroides, P. pentosaceus,
W. paramesenteroides
Lb. paralimentarius, Lb. plantarum, Lb. sanfranciscensis, Leuc. citreum, Leuc.
mesenteroides, W. confusa
Lb. sanfranciscensis, Leuc. citreum
Lb. sanfranciscensis (9/9), Lb. pontis (5/9), Lb. helveticus (2/9), P. pentosaceus (2/9), Lb.
crustorum, Lb. paracasei
Lb. delbrueckii, Lb. sanfranciscensis
Lb. crustorum (4/4), Lb. paralimentarius (4/4), Lb. plantarum (4/4), Lb. spicheri (4/4), Lb.
helveticus (3/4), Lb. pontis (3/4), Lb. rossiae, Lb. paracasei
Lb. brevis (3/3), Lb. sanfranciscensis (3/3), Lb. plantarum (2/3), Leuc. mesenteroides
Lb. plantarum, P. pentosaceus
Lb. frumenti, Lb. hammesii, Lb. paralimentarius

Palomba et al., 2011

Scheirlinck et al., 2007c,


2008
Minervini et al., 2012a
Minervini et al., 2012a
Minervini et al., 2012a
Minervini et al., 2012a
Minervini et al., 2012a
Iacumin et al., 2009
Iacumin et al., 2009
Minervini et al., 2012a
Valmorri et al., 2006

Venturi et al., 2012b


Corsetti et al., 2001
Corsetti et al., 2001
Corsetti et al., 2001
Minervini et al., 2012a
Osimani et al., 2009
Corsetti et al., 2001
Corsetti et al., 2001;
Robert et al., 2009;
Minervini et al., 2012a
Minervini et al., 2012a
Corsetti et al., 2001
Corsetti et al., 2001
Corsetti et al., 2001
Osimani et al., 2009
Scheirlinck et al., 2007c,
2008
Minervini et al., 2012a
Ferchichi et al., 2007
Minervini et al., 2012a
Corsetti et al., 2001
Minervini et al., 2012a
Minervini et al., 2012a;
Corsetti et al., 2001
Corsetti et al., 2001
Scheirlinck et al., 2007c,
2008, 2009a
Corsetti et al., 2001
Scheirlinck et al., 2007c,
2008, 2009a
Garofalo et al., 2008
Minervini et al., 2012a
Ferchichi et al., 2007
(continued on next page)

Please cite this article in press as: De Vuyst, L., et al., Microbial ecology of sourdough fermentations: Diverse or uniform?, Food Microbiology
(2013), http://dx.doi.org/10.1016/j.fm.2013.06.002

14

L. De Vuyst et al. / Food Microbiology xxx (2013) 1e19

Table 2 (continued )
Dough
yield

Temperature
( C)

Fermentation
time (h)

Number of
sourdoughs
analyzed

Species diversity

Reference

nd

30e40

15

10

Lb. plantarum (5/10), Lb. sanfranciscensis (5/10), P. pentosaceus (3/10)

nd

RT

nd

26

nd

RT

6e8

nd
nd
nd

RT
RT
RT

20
22
24

1
1
4

nd
150
150
160
160
160
160
161
168
169
195
225e250

RT
25
25
7
8
18
26
25
25
25
28
28e34

120e168
5
13
14
16
24
8
6
4
3e4
24
6e13

2
1
1
1
1
1
1
1
1
2
1
3

Lb. plantarum (13/26), Lb. sanfranciscensis (11/26), Lb. hammesii (10/26), Lb. brevis
(9/26), Lb. paralimentarius (8/26), Lb. nantensis (7/26), Lb. rossiae (4/26), Lb.
alimentarius (3/26), Lb. pentosus (3/26), Lb. pontis (3/26), Lb. sakei (3/26), Lb.
farciminis (2/26), Lb. namurensis (2/26), W. confusa (2/26), Lb. buchneri, Lb. curvatus,
Lb. fermentum, Lb. parabuchneri, Leuc. citreum, Leuc. mesenteroides, P. acidilactici,
P. pentosaceus
Lb. alimentarius, Lb. brevis, Lb. casei, Lb. pentosus, Lb. plantarum, Lb. sakei, Lb.
sanfranciscensis, Lb. zeae
Lb. paracasei, Lb. plantarum, Lb. sanfranciscensis, Leuc. pseudomesenteroides
Lb. curvatus, Lb. plantarum, Lb. sakei, Lb. sanfranciscensis, Leuc. citreum, S. salivarius
Lb. fermentum (3/4), Lb. alimentarius/kimchii (2/4), Lb. paralimentarius (2/4), Lb.
plantarum (2/4), Lb. sanfranciscensis (2/4), Lb. brevis, Lb. paracasei, Lb. rhamnosus,
W. confusa
Lb. spicheri (2/2), Lb. paralimentarius (2/2), Lb. paracasei (2/2), Lb. perolens
W. cibaria
Lb. plantarum, Lb. sanfranciscensis
Lb. sanfranciscensis, Leuc. mesenteroides
Lb. frumenti, Lb. hammesii, Lb. paralimentarius
Lb. pontis, Lb. sanfranciscensis, Lb. spicheri
Lb. hammesii, Lb. nantensis, Lb. panis, Lb. sanfranciscensis
Lb. plantarum, Lb. sanfranciscensis
Lb. sanfranciscensis
Lb. plantarum (2/2), Lb. sakei, Leuc. citreum, P. pentosaceus
Lb. amolyticus, Lb. acetotolerans, Lb. frumenti, Lb. panis
Lb. panis (3/3), Lb. amylovorus (2/3), Lb. reuteri (2/3), Lb. helveticus, Lb. pontis

Paramithiotis et al.,
2010
Catzeddu et al., 2006;
Scheirlinck et al., 2007c,
2008

251
500

24
40

4
48

1
1

Lb. casei, Lb. plantarum


Lb. amylovorus, Lb. frumenti, Lb. pontis, Lb. reuteri

Catzeddu et al., 2006


Osimani et al., 2009
Osimani et al., 2009
Osimani et al., 2009;
Randazzo et al., 2005
Meroth et al., 2004
Minervini et al., 2012b
Minervini et al., 2012b
Ferchichi et al., 2008
Ferchichi et al., 2008
Ferchichi et al., 2008
Ferchichi et al., 2008
Minervini et al., 2012b
Minervini et al., 2012b
Minervini et al., 2012b
Vera et al., 2012
Rosenquist and Hansen,
2000; Viiard et al., 2012
Minervini et al., 2012b
Mller et al., 2001

LAB: E., Enterococcus; F., Fructobacillus; Lb., Lactobacillus; Lc., Lactococcus; Leuc., Leuconostoc; P., Pediococcus; S., Streptococcus; W., Weissella.

lesser extent, lactic acid (Gnzle et al., 1998). As C. humilis cannot


grow above 35  C (optimal at 27e28  C), a high temperature will
inuence the mutualistic growth of LAB as well, which may also
explain the lack of competitiveness of Lb. sanfranciscensis at this
temperature (Brandt et al., 2004; Gnzle et al., 1998; Vogelmann
and Hertel, 2011).
8.2. Dough yield, water activity, and pH
The dough yield (DY) is of direct inuence on the water activity
and acidity of the ripe sourdough (Banu et al., 2011; Vogelmann and
Hertel, 2011). For example, a low DY amplies the effect of the our
by providing the growing microbiota with a higher amount of carbohydrates available for fermentation and allowing a higher buffering capacity, thereby slowing down the rate of acidication, as
compared to a high DY. At low pH, acid-tolerant lactobacilli prevail,
while higher pH values allow the prevalence of enterococci, lactococci, leuconostocs, pediococci, and weissellas (Corsetti et al.,
2007b; Minervini et al., 2012a; Vrancken et al., 2011; Zotta et al.,
2009). For instance, the retrieval of P. pentosaceus and Leuconostoc
and Weissella species from French type I sourdoughs, which display
pH values typically above 4.0, might be due to this relatively high pH
(Robert et al., 2009). As these LAB species are acid-sensitive, they die
off when a signicant pH decrease occurs upon fermentation of the
our-water mixture (Corsetti et al., 2007a,b; Van der Meulen et al.,
2007; Weckx et al., 2010b). Similarly, the rate of acidication of the
dough will determine the level of Lb. sanfranciscensis in the dough,
as this species optimally grows at pH 5.0, whereas C. humilis is not
affected by pH (Brandt et al., 2004; Gnzle et al., 1998).
The higher the DY the faster and stronger the relative acidication is, although the production of acetic acid is negatively affected
in uid sourdoughs (Decock and Cappelle, 2005; Banu et al., 2011).
This is in accordance with the prevalence of acid-tolerant Lb.

fermentum, Lb. plantarum, and Lb. reuteri in uid high-DY type II


sourdoughs (Vrancken et al., 2008; Vogelmann and Hertel, 2011).
Especially Lb. fermentum is often associated with strongly acidied
doughs, due to its high pH tolerance (Van der Meulen et al., 2007;
Vrancken et al., 2011; Weckx et al., 2010b). In contrast, Lb. sanfranciscensis that does not grow below pH 3.8 is mainly associated
with low-DY type I sourdoughs (Vogelmann and Hertel, 2011).
A high osmotic pressure or low water activity as a result of a low
DY has a more pronounced effect on the lactobacilli than on the
yeasts (Venturi et al., 2012b). A high osmotolerance of W. anomalus
may explain its dominance in spontaneous laboratory sourdoughs
compared with S. cerevisiae (Daniel et al., 2011; Vrancken et al.,
2010). Similarly, an increased ionic strength as a result of the
addition of salt (NaCl) is expected to favor yeasts. Illustratively, Lb.
sanfranciscensis is inhibited by the addition of 4% salt, while
C. humilis is not affected (Gnzle et al., 1998; Brandt et al., 2004),
although the opposite effect has been described as well (Wick et al.,
2003). Alternatively, the growth and/or competitiveness of Lb.
amylovorus DCE 471 is favored in the presence of salt (Neysens et al.,
2003).
8.3. Oxygen tension and redox potential
Although sourdough fermentation proceeds semi-anaerobically,
the introduction of oxygen through refreshment of the sourdough
and kneading, in particular at the beginning of the fermentation
cycle and during small-scale production, may favor certain LAB and
yeast species (Mihhalevski et al., 2011; Viiard et al., 2012). Certain
yeast species, such as P. kudriavzevii, can only grow when oxygen is
available during fermentation and, hence, will occur in less rm
doughs or at the surface of the dough (Vogelmann and Hertel,
2011). Similarly, mild aeration can have a positive effect on the
growth and/or competitiveness of certain LAB species, such as in

Please cite this article in press as: De Vuyst, L., et al., Microbial ecology of sourdough fermentations: Diverse or uniform?, Food Microbiology
(2013), http://dx.doi.org/10.1016/j.fm.2013.06.002

L. De Vuyst et al. / Food Microbiology xxx (2013) 1e19

15

Table 3
Lactic acid bacteria species diversity in end-samples of backslopped laboratory sourdoughs grouped as a function of the process parameters dough yield, temperature and
fermentation time (nd: not dened; 0: spontaneous; 1: starter culture or mother sponge added; RT: room temperature). Entries are ranked as a function of dough yield,
temperature, and fermentation time. Species are ranked in order of the number of sourdoughs in which they were detected, as indicated by the number between brackets; no
number is mentioned for single detections.
Spontaneous/
starter culture

Dough
yield

Temperature
( C)

Fermentation
time (h)

nd

28e35

24

1
1
1
0

187
150
150
160

30
25
25
30

24
5
13
8

3
1
1
2

160

30

23

1
1
1
0

161e169
200
200
200

25e28
20
20
25

3e6
12
24
12

4
1
1
2

200

25

12

1
0
1
1
0

200
200
200
200
200

25
28
28
30
30

24
24
24
12
24

1
1
6
5

200

30

24

29

1
1
0
1
1

200
200
200
200
200

35
35
37
37
37

12
24
24
24
24

2
2
1
1
3

1
1
1
0

200
200
251
275

40
40
24
35

12
24
4
24

1
1
1
2

275

35

24

0
1
0
0

300
367
400
400

37
40
23
30

42
48
24
24

1
1
1
13

1
0
0
1
1
1
1

400
400
400
400
500
500
500

30
30
37
37
34
40
46

24
48
24
24
48
48
48

1
1
1
1
1
1
1

Number of
sourdoughs
analyzed

Species diversity

Reference

Lb. curvatus, Lb. gallinarum, Lb. kimchii, Lb. fermentum,


Lb. plantarum
Lb. plantarum (3/3), Lb. brevis, Lb. paralimentarius
Leuc. citreum
Lb. sanfranciscensis
Lb. sanfranciscensis, Lb. rossiae, Lb. plantarum, W. cibaria/
confusa
Lb. sanfranciscensis (14/23), Lb. plantarum (9/23),
W. confusa (8/23), Lb. rossiae (3/23), P. pentosaceus
(2/23), Lb. paralimentarius, Lc. lactis
Leuc. citreum (2/4), Lb. plantarum, Lb. sanfranciscensis
Lb. sanfranciscensis
Lb. sanfranciscensis
Leuc. holzapfelii (2/2), P. pentosaceus (2/2), Lb. graminis,
Lb. plantarum, Lb. sakei, W. cibaria
Lb. sanfranciscensis (4/4), Lb. brevis (2/4), Lb.
paralimentarius (2/4), Lb. plantarum (2/4), Lb. mindensis,
Leuc. argentinum, W. cibaria
Lb. sanfranciscensis
Leuc. argentinum, P. pentosaceus, W. cibaria
Leuc. argentinum, P. pentosaceus, W. cibaria
Lb. sanfranciscensis (6/6), Lb. fermentum, Lb. reuteri
Lb. plantarum (5/5), P. pentosaceus (3/5), Lb. sakei (2/5),
Lb. paralimentarius
Lb. fermentum (16/29), Lb. pontis (15/29), Lb. helveticus
(12/29), Lb. paralimentarius (12/29), Lb. plantarum
(11/29), Lb. sanfranciscensis (8/29), Lb. crispatus, Lb.
spicheri, P. pentosaceus
Lb. johnsonii (2/2), Lb. reuteri (2/2)
Lb. johnsonii (2/2), Lb. reuteri (2/2)
Lb. coryniformis
Lb. coryniformis
Lb. johnsonii (2/3), Lb. reuteri (2/3), Lb. crispatus, Lb.
frumenti, Lb. panis
Lb. johnsonii, Lb. reuteri
Lb. johnsonii, Lb. reuteri
Lb. casei
Lb. fermentum (2/2), Lb. vaginalis (2/2), Lb. gallinarum
(2/2), Lb. crispatus, Lb. plantarum, Lb. pontis
Lb. amylovorus (2/2), Lb. fermentum (2/2), Lb. frumenti
(2/2), Lb. brevis, Lb. paralimentarius, Lb. plantarum, Lb.
pontis, Lb. reuteri, Leuc. argentinum, P. acidilactici
Lb. fermentum, Lb. reuteri
Lb. johnsonii, Lb. reuteri
Lb. fermentum, Leuc. citreum, P. pentosaceus
Lb. plantarum (12/13), Lb. fermentum (11/13), Lb. brevis
(3/13), P. pentosaceus (2/13), Lb. curvatus, Lb.
paraplantarum, Lb. rossiae, W. confusa
Lb. sanfranciscensis
Lb. fermentum, Lb. plantarum
Lb. fermentum
Lb. johnsonii, Lb. reuteri
Lb. amylovorus, Lb. frumenti
Lb. amylovorus, Lb. frumenti
Lb. amylovorus, Lb. frumenti, Lb. pontis

Meroth et al., 2004


Zannini et al., 2009
Minervini et al., 2012b
Minervini et al., 2012b
Siragusa et al., 2009 Minervini
et al., 2010
Siragusa et al., 2009; Minervini
et al., 2010
Minervini et al., 2012b
Vogelmann and Hertel, 2011
Vogelmann and Hertel, 2011
Moroni et al., 2011
Meroth et al., 2003b; Moroni
et al., 2010; Vogelmann and
Hertel, 2011
Vogelmann and Hertel, 2011
Httner et al., 2010
Httner et al., 2010
Vogelmann and Hertel, 2011
Sterr et al., 2009
Meroth et al., 2003b; Sterr et al.,
2009; Vogelmann et al., 2009;
Vogelmann and Hertel, 2011
Vogelmann and Hertel,
Vogelmann and Hertel,
Httner et al., 2010
Httner et al., 2010
Meroth et al., 2003b;
Vogelmann and Hertel,
Vogelmann and Hertel,
Vogelmann and Hertel,
Minervini et al., 2012b
Moroni et al., 2011

2011
2011

2011
2011
2011

Moroni et al., 2010

Hamad et al., 1997


Meroth et al., 2003b
Vrancken et al., 2011
Van der Meulen et al., 2007;
Vrancken et al., 2011; Weckx
et al., 2010a,b
Vogelmann and Hertel, 2011
Vrancken et al., 2011
Vrancken et al., 2011
Vogelmann and Hertel, 2011
Mller et al., 2001
Mller et al., 2001
Mller et al., 2001

LAB: Lb., Lactobacillus; Lc., Lactococcus; Leuc., Leuconostoc; P., Pediococcus; W., Weissella.

the case of the Lb. amylovorus DCE 471 strain (Leroy et al., 2007).
Also, the use of oxygen as alternative external electron acceptor
may be responsible for a shift of the production from ethanol toward acetate (Gobbetti et al., 2005: Martinez-Anaya et al., 1994).
8.4. Backslopping procedure
Whereas backslopping generally selects for heterofermentative
lactobacilli, the amount of backslopped sourdough as well as the

frequency and duration of the backsloppings inuence the community dynamics and stability of the sourdough microbiota
(Minervini et al., 2012b). The amount of backslopping dough denes the initial pH and hence inuences the growth and acidication rates of the LAB species involved, as this is correlated with
the DY and hence the availability of water, as described above
(Brandt et al., 2004; Van der Meulen et al., 2007). It is anticipated
that short refreshment times select for rapidly growing, fastacidifying LAB species, at least under a given set of environmental

Please cite this article in press as: De Vuyst, L., et al., Microbial ecology of sourdough fermentations: Diverse or uniform?, Food Microbiology
(2013), http://dx.doi.org/10.1016/j.fm.2013.06.002

16

L. De Vuyst et al. / Food Microbiology xxx (2013) 1e19

conditions (Vogelmann and Hertel, 2011). Further, it is noteworthy


that the generation time of Lb. sanfranciscensis is between 4 and 6 h,
allowing it to thrive in fast backslopped sourdoughs too (Ferchichi
et al., 2008; Garofalo et al., 2008; Picozzi et al., 2010; Venturi et al.,
2012b). The length of the propagation steps and, hence, the frequency of the refreshment times determines the growth intensity of
LAB and yeasts (Vogelmann and Hertel, 2011; Vrancken et al., 2011).
Long backslopping times and fermentations without backslopping
seem to benet acid-tolerant LAB species that are highly adapted to
a nutrient-poor, hostile environment, such as Lb. fermentum, Lb.
plantarum, and Lb. reuteri (Parente et al., 2010; Serrazanetti et al.,
2009; Vrancken et al., 2008; Vogelmann and Hertel, 2011). As an
example, Lb. fermentum dominates a type II wheat sourdough at
30  C with backslopping every 24 h, while a mixture of Lb. fermentum and Lb. plantarum prevails at 30  C with backslopping every
48 h (Vrancken et al., 2011). Concerning yeasts, fast refreshments
may be disadvantageous, as their growth lags behind that of the LAB
communities (Venturi et al., 2012b; Wick et al., 2003), although the
growth of C. humilis seems to be favored under such conditions
compared to S. cerevisiae (Vogelmann and Hertel, 2011).
8.5. Resting time
A storage of the mother sponge at reduced temperatures between refreshments is a common practice in, for example, the
preparation of Italian sweet baked goods (Palomba et al., 2011;
Siragusa et al., 2009; Venturi et al., 2012b). This so-called resting
time might inuence the community dynamics and metabolite
kinetics of the resulting sourdoughs by selecting toward coldtolerant strains that are able to survive periods of cold stress and/
or starvation. Among others, Lb. sanfranciscensis might benet from
this situation, as it might prevent excessive acidication and
nutrient depletion (Venturi et al., 2012b). As a consequence, a
stable and non-competitive association of S. cerevisiae, C. milleri,
and Lb. sanfranciscensis occurs during the manufacture of Lagaccio,
as the growth rates of the microbial communities are similar and a
continuous delivery of carbohydrates occurs through malt extract
addition in the beginning of the mother sponge regeneration phase,
as well as during Panettone manufacturing because of a moderate
refrigeration of the mother sponge (Venturi et al., 2012b).
9. Conclusions
As sourdough is a specic and stressful ecosystem and given the
fact that there is no clear-cut relationship between a typical sourdough and its associated microbiota, it will be interesting to see if
sourdough-specic LAB and yeast species exist. Therefore, not only
different sourdough ecosystems need to be studied, but also other
ecosystems need to be searched for species that were found in
sourdoughs for the rst time. For these studies, statistically relevant
sampling and isolation methodologies have to be followed and
accurate identication procedures have to be carried out. Finally, it
will be interesting to know what the real origin of the sourdough
microbiota is.
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