You are on page 1of 5

Euglena Advanced article

Dennis E Buetow, University of Illinois, Urbana, Illinois, USA Article Contents


. Introduction
. Description and Taxonomy

. Reasons for Popularity

. Significance for Research

. Impact on Human Welfare

Online posting date: 15th April 2011

Euglena is a genus of single-celled, free-living micro- known Euglena species are asexual. A very large literature
organisms that show both plant- and animal-like exists on the morphology, physiology and biochemistry of
characteristics. Members of the genus are found widely Euglena, but much of the information comes from only a
in nature and mainly in fresh waters. Most are aerobic few species, with the easily grown Euglena gracilis being the
and use photosynthesis or many organic compounds as
most studied (Buetow, 19681989). See also: Ehrenberg,
Christian Gottfried; Leeuwenhoek, Antoni van
interchangeable sources of carbon and energy. The most
studied species is the easily grown E. gracilis which, in spite
of its relatively rigid surface, can be subfractionated to
yield nuclei, mitochondria, chloroplasts, flagella and pel-
Description and Taxonomy
licles. Subfractions show some unusual characteristics:
The nuclear envelope remains intact throughout mitosis
Morphology
and chromosomes are permanently condensed at all Euglena cells range in size from 12 mm long  5 mm wide
phases of the cell cycle, the mitochondrial respiratory for E. minuta to 530 mm  40 mm for E. oxyuris and vary
chain has two terminal oxidases, and chloroplasts have in shape from almost spherical to nearly cylindrical.
three membranes reflecting their endosymbiotic evo- The largest numbers are spindle shaped. Locomotion is
lutionary history. Various Euglena and some of their accomplished by the beating of the long agellum.
constituent molecules are useful for environmental bio- Metaboly, or euglenoid movement, also occurs in most if
not all species and, therefore, the overall shape of the cell
mediation and potentially useful biomedically.
may change at any time. Figure 1 (Leedale, 1982) depicts
that a Euglena cell of the E. gracilis type showing its
main organelles. E. gracilis cells are approximately 50 mm
Introduction long  10 mm wide and spindle-shaped. The majority of
Euglena species are green due to the presence of chloro-
Antoni van Leeuwenhoek in 1674 was the rst to describe plasts containing chlorophylls a and b. The chloroplasts of
a microorganism which was green in the middle. This E. gracillis are labile and easily lost being readily bleached
organism later was named Euglena viridis by CG Ehrenberg by a variety of agents including antibiotics and tempera-
(1830) who started the study of the genus Euglena. More tures of 348C or above. About a dozen species are coloured
than 250 Euglena species have been described. The actual by red granules. When the granules are concentrated at its
number is not known, however, because the size and shape centre, the cell appears green because of the peripheral
of a cell in a given species can vary greatly depending on arrangements of its chloroplasts. When the granules are
nutritional status, phase of the growth cycle (lag, exponen- dispersed, the cell appears red. The surface of most, per-
tial or stationary) and environmental factors such as pH and haps all, Euglena cells is coated with a mucilage that is
the quantity and quality of light available. Therefore, some secreted from muciferous bodies via canals to the outside.
species described may only be size variants of other better- May species encyst especially under unfavourable envir-
dened species. In any case, the single-celled organisms onmental conditions. See also: Cilia and Flagella
comprising the genus Euglena are structurally complex
and show both plant- and animal-like characteristics. All Ecology
Members of the genus Euglena are found widely in nature.
ELS subject area: Microbiology The species are free living and inhabit freshwater pools,
ponds and lakes. Apparently, there are no saltwater
How to cite: forms, though some Euglena occasionally are found in
Buetow, Dennis E (April 2011) Euglena. In: Encyclopedia of Life
marine sediments and some survive in up to 40% seawater.
Sciences (ELS). John Wiley & Sons, Ltd: Chichester.
DOI: 10.1002/9780470015902.a0001964.pub3
Euglena species generally are aerobic, but some tolerate
anaerobic conditions. Various species are indicators of

ENCYCLOPEDIA OF LIFE SCIENCES & 2011, John Wiley & Sons, Ltd. www.els.net 1
Euglena

species to species and even from strain to strain. At one


extreme is E. pisciformis, an obligate phototroph, and at
the other are the articially bleached strains of Euglena,
which are obligate heterotrophs. The Vischer strain grows
more rapidly in light than on any of several organic
substrates. E. gracilis strain Z and variety bacillaris can
grow on a variety of media. Minimally, they require several
inorganic salts as sources of phosphorus, sulfur, nitrogen
and minerals, vitamins B1 and B12 and white light or any
one of the many organic compounds as a source of carbon
(Cook, 1968).

Taxonomy
How to classify Euglena has been a long-standing problem
(Linton et al., 2010). The genus has been claimed as
photosynthetic protozoa by zoologists and as algae by
botanists. However, inclusion of the genus among the
algae or the protozoa may no longer be tenable. Molecular
phylogeny based on the nucleotide sequences of genes
encoding small-subunit ribosomal ribonucleic acids (RNAs)
(Sogin et al., 1986) shows E. gracilis diverging from the
main eukaryotic line far before a period of massive
evolutionary radiation that gave rise to the algae, plants,
animals and fungi. The free-living organisms of the genus
Euglena have been placed in the Phylum Euglenozoa, which
interestingly also includes the extant parasitic trypanosomes
(Von der Heyden et al., 2004; Ahmadinejad et al., 2007)
See also: Protozoan Taxonomy and Systematics

Reasons for Popularity


E. gracilis was among the rst of the photosynthetic
eukaryotic microorganisms domesticated for laboratory
Figure 1 A Euglena cell of the Euglena gracilis type showing the main
organelles. From Leedale (1982).
use. It is easy to grow, with various strains showing gen-
eration times of 10 to about 25 h at 258C. The biochemical
and physiological exibility of this species, together with a
organically polluted water. E. gracilis survives high levels morphological exibility that is readily visualised via light
of highly energetic ionising radiation (Hayashi et al., 2004). and electron microscopy, contribute to its popularity. It is
An unusual degree of adaptability to diverse environments amenable to single-cell studies as well as studies using large-
characterises the genus, with species found in vegetable scale fermenter-size cultures. The cell cycle of E. gracilis can
cannery and citrus waste-lagoons, in raw sewage, in water be studied in mass cultures synchronised for cell division
in tree holes, on snow and in high mountain lakes, on the through the use of alternating light and dark cycles or heat
bark of the honey locust tree, in alkaline marshes and in and cold shock. This species is a prominent example that
acid coal-mine water with a pH as low as 0.9 (Lacky, 1968). circadian and infradian rhythms exist and can be investi-
E. gracilis survives temperatures from about 18C to 388C gated readily in single-celled organisms. Further, in spite of
and pHs ranging from 2.3 to 11. The most thermotolerant its relatively rigid pellicle, E. gracilis can be subfractionated
(up to 408C) chloroplast-bearing Euglena strain known to yield pure preparations of nuclei, chloroplasts, mito-
lives in acidic hot mud pools in a volcanic area in Costa chondria, agella and pellicles. See also: Cell Cycle;
Rica (Sittenfeld et al., 2002). See also: Protozoan Ecology Tetrahymena

Nutrition
Significance for Research
As a group, Euglena are able to use photosynthesis and
heterotrophic oxidative assimilation as interchangeable Studies on the genus Euglena, and especially E. gracilis,
and apparently equivalent sources of carbon and energy. have been signicant for understanding the biochemistry
The degree of interchangeability, however, can vary from and molecular biology of nuclei and subcellular organelles.

2 ENCYCLOPEDIA OF LIFE SCIENCES & 2011, John Wiley & Sons, Ltd. www.els.net
Euglena

Also, some unusual features of these subcellular particles At a normal level of oxygen (21%), it functions in the
in Euglena distinguish them from their counterparts in TCA cycle, while at limiting oxygen (essentially anaerobic)
higher eukaryotes and, so, have furthered our knowledge conditions, it functions in wax ester fermentation. No
of evolutionary diversity. adenosine triphosphate (ATP) is lost by this unique process
of wax fermentation. Therefore, the ATP generated by
Nucleus glycolysis remains as a net gain and apparently allows the
cells to survive anaerobiosis. The Euglena OGD converts
The Euglena nucleus has been isolated and its ultrastucture 2-oxoglutarate to succinate semialdehyde (SSA) in con-
extensively investigated. The number of chromosomes trast to the 1-oxoglutarate dehydrogenase which provides
varies with the species, e.g., E. gracilis has 45 while the for the formation of succinyl-coenzyme A in the TCA cycle
higher ploidy E. spirogyra has 86. The chromosomes, of other mitochondria. The SSA of Euglena also is part of a
unlike those in higher cells, appear permanently condensed unique g-aminobutyric acid (GABA) shunt similar to the
at all phases of the cell cycle (Leedale, 1967). Even so, GABA shunt found in mammalian brain mitochondria. In
chromatin can be isolated from interphase Euglena nuclei addition to oxidative phosphorylation, ATP is also gen-
with over 60% being highly condensed heterochromatin erated in the Euglena mitochondrion by adenylate kinase
and the rest being the less condensed, transcriptionally and by a catalatic-type activity (but not catalase-driven)
active euchromatin. The usual histones are present. that converts hydrogen peroxide to water and oxygen with
Nuclear division in Euglena is by mitosis, but a peculiar one the energy released used to drive the formation of ATP. The
in that the nuclear envelope persists throughout the entire respiratory chain contains two terminal oxidases and sep-
process; the nucleolus (also called an endosome, Figure 1) arate entry points for oxidation of NADH, succinate and
also remains intact, elongates along the division axis and lactate. The alternative oxidase is inducible, highly resist-
divides into two daughter nucleoli; and the chromosomes ant to cyanide and contains haem B as do bacterial quinol
are arranged parallel to the division axis at metaphase. oxidases (Devars et al., 1998). Glyoxylate cycle enzymes
Some species appear to have several nucleoli, and these are present in mitochondria rather than in glyoxysomes
fuse into a single body at mitosis. Many Euglena nuclear (Ono et al., 2003). The Euglena mitochondrion unites
mRNAs, are subject to trans-splicing rather than the more biochemical properties of aerobic and anaerobic mito-
common cis-splicing found in higher eukaryotes (Tessier chondria and of hydrogenosomes (Homeister et al.,
et al., 1991; Frantz et al., 2000). See also: Eukaryotic 2004). See also: Citric Acid Cycle; Mitochondria: Structure
Chromosomes; Nucleolus and Role in Respiration; Oxidative Phosphorylation
Euglena mitochondrial deoxyribonucleic acid (DNA)
Mitochondrion has a molecular mass of 40  106 Da and a low (25%) G+C
content and appears to exist as a complex mixture of
The mitochondrial system of E. gracilis and apparently circular and heterogeneous linear molecules similar to the
of other Euglena species is usually a single reticulum that situation encountered with higher plant mitochondrial
ramies throughout the cell (Figure 1). The degree of genomes (Buetow, 1989).
branching and the thickness of the branches, however, may
vary under dierent nutritional conditions and during Chloroplast
dierent phases of the cell cycle. The outer mitochondrial
membrane is strongly undulated and the cristae, unlike Chloroplasts in Euglena species range from small pyrenoid-
those in most eukaryotes but like those in trypanosomes, less discs to large plates or complexes with pyrenoids,
are discoid (previously called at) and constricted at their photosynthetic lamellae typically with three thylakoids
bases. Also, the mitochondrial succinate dehydrogenase and a matrix (or stroma) containing 70S ribosomes. In
enzyme is encoded by a unique split and rearranged nuclear contrast to green algal and higher plant chloroplasts, which
gene in E. gracilis as it is in trypanosomes (Gawryluk and are surrounded by two membranes, Euglena chloroplasts
Gray, 2009). are surrounded by three membranes. Thus, the latter
The mitochondrion of E. gracilis shares with all mito- organelles evolved from a secondary endosymbiosis with a
chondria a common basic pattern of oxidative phos- eukaryotic symbiont rather than a primary endosymbiosis
phorylation and participation in intermediary metabolism with a prokaryotic symbiont (Gibbs, 1978; Archibald and
(Buetow, 1989; Kitaoka et al., 1989). It also shows some Keeling, 2002). In green algae and higher plant chloro-
apparently unique characteristics. For example, its tri- plasts, protein import is posttranslational. In Euglena,
carboxylic acid (TCA) cycle in overall function is similar to the presence of an extra chloroplast membrane leads to
that in other mitochondria but contains novel NADP+- an unusual import pathway with many nuclear-encoded
dependent 2-oxoglutarate decarboxylase (OGD) and chloroplast proteins being transported rst to the endo-
pyruvate dehydrogenase (PD) enzymes. Both function as plasmic reticulum then to the Golgi and then to the chloro-
single enzymes rather than as part of a complex of enzymes plast (Sulli and Schwartzbach, 1996; Slavikova et al., 2005).
and are dependent on NADP+ rather than NAD. The Light is indispensable for plastid development in
Euglena PD is oxygen-sensitive and functions as a regu- E. gracilis (Schi and Schwartzbach, 1982). During hetero-
latory enzyme depending on the concentration of oxygen. trophic growth in darkness, plastid development is stopped

ENCYCLOPEDIA OF LIFE SCIENCES & 2011, John Wiley & Sons, Ltd. www.els.net 3
Euglena

at the stage of a small proplastid. On exposure to light, the is cost eective for degrading swine manure in polluted
proplastid is induced to develop into a chloroplast. Thus, agro-wastewater (de Godos et al., 2010). E. sanguinea
chloroplast development is easily studied in E. gracilis by contains a toxin, euglenophycin, which has herbicidal
rst growing the cells in the dark and then simply exposing and anticancer activities (Zimba et al., 2010). See also:
them to white light. Therefore, more research has been Bioremediation
devoted to the chloroplasts of E. gracilis than to any other
component of a Euglena cell. These chloroplasts are rela-
tively streamlined to function mainly as photosynthetic
units. Unlike those in higher plants, Euglena chloroplasts,
References
for example, do not store starch, do not activate or reduce Ahmadinejad N, Dagan T and Martin W (2007) Genome history
sulfate, and do not contain an NADP+-dependent malate in the hybrid Euglena gracilis. Gene 402: 3539.
dehydrogenase. Sulfur metabolism and the dehydrogenase Archibald JM and Keeling PJ (2002) Recycled plastids; a green
are located in mitochondria in Euglena (Saidha et al., 1988; movement in eukaryotic evolution. Trends in Genetics 18:
Patton et al., 2008). See also: Photosynthesis 577584.
Chloroplast DNA in E. gracilis is A+T-rich (about Buetow DE (ed.) (19681989) The Biology of Euglena, vols. IIV.
75%) and has a molecular mass of 92  106 Da. There New York: Academic Press.
are about 2002800 DNA molecules in the 610 chloro- Buetow DE (1989) The mitochondrion. In: Buetow DE (ed.) The
plasts in a Euglena cell with the exact number depending Biology of Euglema, vol. IV, pp. 247314. San Diego: Academic
on the condition of growth and the phase of the growth Press.
cycle. The chloroplast DNA has been completely seque- Chae SR, Hwang ET and Shin HS (2006) Single cell protein
nced (Hallick et al., 1993), this circular DNA is 143 170 bp production of Euglena gracilis and carbon dioxide xation in
in size, counting only one copy of a 54-bp tandem an innovative photo-bioreactor. Bioresource Technology 97:
repeat that is present in variable copy number. In contrast 322329.
to the 120130 genes in land-plant chloroplast genomes, Cook JR (1968) The Cultivation and Growth of Euglena. In:
Buetow DE (ed.) The Biology of Euglena, vol. I, pp. 243314.
there are only 103 in Euglena. Introns account for
New York: Academic Press.
38.3% of the total DNA content and are the most
Devars S, Hernandez R, Covian R et al. (1998) The content of
numerous of any organelle genome known. Included are
alternative oxidase of Euglena mitochondria is increased by
twintrons (introns-within-introns). growth in the presence of cyanide and is not cytochrome
O. Journal of Eukaryotic Microbiology 45: 122130.
Ehrenberg CG (1830) Neue Beobachtungen uber blutartige
Impact on Human Welfare Erscheinungen in Agypten, Arabien und Sibirien, nebst einer
Ubersicht und Kritik der fruher bekannten. Poggendors
E. gracilis requires low levels of vitamin B12 for growth. Annalen der Physik und Chemie 94: 477514.
Therefore, the rst use of this organism for medical pur- Frantz C, Ebel C, Paulus F and Imbault P (2000) Characterization
poses was in assays to determine B12 levels in biological of trans-splicing in Euglenoids. Current Genetics 37: 47384746.
uids. E. gracilis shows promise as a single-cell source of Gawryluk RMR and Gray MW (2009) A split and rearranged
protein (Hosoya and Kitaoka, 1977; Chae et al., 2006) and nuclear gene encoding the iron-sulfur subunit of mitochondrial
as an antihypertensive agent (Murakami, 1985), provides succinate dehydrogenese in Euglenozoa. BMC Research Notes
an ecient and inexpensive system for purication and 2: 1622.
reclamation of farm and urban wastes (Waygood et al., Gibbs SP (1978) The chloroplast of Euglena may have evolved
1980), can serve as a bioreactor for the production of wax from symbiotic green algae. Canadian Journal of Botany 56:
esters (Tani et al., 1987), is highly resistant to heavy metals 28832889.
and can be used to indicate the health of the environment de Godos I, Vargas VA, Blanco S et al. (2010) A comparative
(Rodriguez-Zavala et al., 2007), is suitable for remediating evaluation of microalgae for the degradation of piggery was-
water contaminated by radioactive technium (Ishii and tewater under photosynthetic oxygenation. Biosource Tech-
nology 101: 51505158.
Uchida, 2006) and is promising for commercial production
Green AG (2004) From alpha to omega producing essential
of g-tocopherol which is used as a dietary supplement for
fatty acids in plants. Nature Biotechnology 22: 680682.
humans, as a food preservative, and in the manufacture
Gupta S and Agrawal SC (2005) Motility and survival of Euglena
of cosmetics and for the fortication of animal feed (Tani ignobilis as aected by dierent factors. Folia Microbiologica
and Tsumura, 1989; Ogbonna, 2009). Paramyton, a major 50: 315322.
glucan in E. gracilis, protects mammalian liver from injury Hallick RB, Hong L, Drager RG et al. (1993) Complete sequence
by carbon tetrachloride and inhibits dermatitis-like skin of Euglena gracilis chloroplast DNA. Nucleic Acids Research
lesions (Sugiyama et al., 2009, 2010). 21: 35373544.
Plants, transformed with an unusual desaturase gene Hayashi H, Wada S, Funayama T et al. (2004) Evaluation of the
from Euglena, produce essential fatty acids normally resistance of Euglena gracilis to ion beam radiation. Journal of
obtained only from sh (Green, 2004). E. ignobilis, based Eukaryotic Microbiology 51: 321324.
on mobility and morphological changes, can be used to Homeister M, van der Klei A, Rotte C et al. (2004) Euglena
access water quality (Gupta and Agrawal, 2005). E. viridis gracilis rhodoquinone: ubiquinone ratio and mitochondrial

4 ENCYCLOPEDIA OF LIFE SCIENCES & 2011, John Wiley & Sons, Ltd. www.els.net
Euglena

proteome dier under aerobic and anaerobic conditions. Sogin ML, Elwood HJ and Gunderson JH (1986) Evolutionary
Journal of Biological Chemistry 279: 2242222429. diversity of eukaryotic small-subunit rRNA genes. Proceedings
Hosoya K and Kitaoka S (1977) Determination of the nutritive of the National Academy of Sciences of the USA 83: 13831387.
value of Euglena gracilis protein by in vitro digestion experi- Sugiyama A, Hata S, Suzuki K et al. (2010) Oral administration of
ments and rat feeding tests. Journal of the Agricultural Chem- paramylon, a b-1,3-D-glucan isolated from Euglena gracilis Z
istry Society of Japan 51: 483488. inhibits development of atopic dermatitis-like skin lesions
Ishii N and Uchida S (2006) Removal of technium from solution from NC/Nga micE. Journal of Veterinary Medical Science 72:
by the algal agellate Euglena gracilis. Journal of Environmental 755763.
Quality 35: 20172020. Sugiyama A, Suzuki K, Mitra S et al. (2009) Hepatoprotective
Kitaoka S, Nakano Y, Miyatake K and Yokota A (1989) eects of paramylon, a b-1,3-D-glucan isolated from Euglena
Enzymes and their functional location. In: Buetow DE (ed.) The gracilis Z, on acute liver injury induced by carbon tetrachloride
Biology of Euglena, vol. IV, pp. 1135. San Diego: Academic in rats. Journal of Veterinary Medical Science 71: 885890.
Press. Sulli C and Schwartzbach SD (1996) A soluble protein is imported
Lacky JB (1968) Ecology of Euglena. In: Buetow DE (ed.) The into Euglena chloroplasts as a membrane-bound precursor.
Biology of Euglena, vol. I, pp. 2744. New York: Academic Plant Cell 8: 4353.
Press. Tani Y, Okumura M and Li S (1987) Liquid wax ester production
Leedale GF (1967) Euglenoid Flagellates. Englewood Clis, NJ: by Euglena gracilis. Agricultural and Biological Chemistry 51:
Prentice-Hall. 225230.
Leedale GF (1982) Ultrastructure. In: Buetow DE (ed.) The Tani Y and Tsumura H (1989) Screening for tocopherol-
Biology of Euglena, vol. III, pp. 127. New York: Academic producing microorganisms and a-tocopherol production by
Press. Euglena gracilis Z. Agricultural and Biological Chemistry 53:
Linton EW, Karnkowska-Ishikawa A, Kim JI et al. (2010) 305312.
Reconstructing Euglenoid evolutionary relationships using Tessier L-H, Keller M, Chan RL et al. (1991) Short leader
three genes: nuclear SSU and LSU, and chloroplast SSU sequences may be transferred from small RNAs to premature
rDNA sequences and the description of Eugleneria gen. nov. mRNAs by trans-splicing in Euglena. EMBO Journal 10:
(Euglenophyta). Protist 161: 603619. 26212625.
Murakami T (1985) Eects of three kinds of single cell proteins Von der Heyden S, Chao EE, Vickerman K and Cavalier-Smith T
on blood pressure, cerebral stroke lesions and hypertensive (2004) Ribsomal RNA phylogeny of bodonid and diplonemid
vascular changes in SHRSP. Acta Medica Kinki University 10: agellates and the evolution of Euglenozoa. Journal of
5171. Eukaryotic Microbiology 51: 402416.
Ogbonna JC (2009) Microbiological production of tocopherols: Waygood ER, Hussain A, Godavari HR, Tai YC and Badour SS
current state and prospects. Applied Microbiology and Bio- (1980) Purication and reclamation of farm and urban wastes
technology 84: 217225. by Euglena gracilis: photosynthetic capacity, eect of pH,
Ono K, Kondo M, Osafune T et al. (2003) Presence of glyoxylate temperature, acetate and whey. Environmental Pollution
cycle enzymes in the mitochondria of Euglena gracilis. Journal 23(Series A): 179215.
of Eukaryotic Microbiology 50: 9296. Zimba PV, Moeller PD, Beauchesne K et al. (2010) Identication
Patton NJ, Durnford DG and Kopriva S (2008) Sulfate assimi- of euglenophycin a toxin found in certain euglenoids. Toxicon
lation in eukaryotes: fusions, relocations and lateral transfers. 55: 100104.
BMC Evolutionary Biology 8: 3952.
Rodriguez-Zavala JS, Garcia-Garcia JD, Ortiz-Cruz MA and
Moreno-Sanchez R (2007) Molecular mechanisms of resistance
to heavy metals in the protist Euglena gracilis. Journal of
Environmental Science and Health Part A 42: 13651378. Further Reading
Saidha T, Na SQ, Li JY and Schi JA (1988) A sulfate metabol-
izing centre in Euglena mitochondria. Biochemical Journal 253: Ciugulea I and Triemer RE (2010) A Color Atlas of Photosynthetic
533539. Euglenoids. East Lansing: Michigan State University Press.
Schi JA and Schwartzbach SD (1982) Photocontrol of chloro- Gojdics M (1953) The Genus Euglena. Madison: The University of
plast development. In: Buetow DE (ed.) The Biology of Euglena, Wisconson Press.
vol. III, pp. 314352. New York: Academic Press. Kitaoka S (1989) Euglena-Physiology and Biochemistry. Tokyo:
Sittenfeld A, Marielos M, Ortega JM et al. (2002) Character- Gakkai Shuppan Center. [In Japanese].
ization of a photosynthetic Euglena strain isolated from an Leedale GF (1971) The Euglenoids. Oxford Biology Readers.
acidic hot mud pool of a volcanic area of Costa Rica. FEMS London: Oxford University Press.
Microbiology Ecology 42: 151160. Leedale GF (2000) Euglenozoa. In: Lee JJ, Leedale GF and
Slavikova S, Vacula R, Fang Z et al. (2005) Homologous and Bradbury P (eds) An Illustrated Guide to the Protozoa, 2nd edn,
heterologous reconstitution of Golgi to chloroplast transport vol. II, pp. 11351185. Lawrence, KS: Allen Press, Inc.
and protein import into the complex chloroplasts of Euglena. Sleigh M (1989) Protozoa and Other Protists. London: Edward
Journal of Cell Science 118: 16511661. Arnold.

ENCYCLOPEDIA OF LIFE SCIENCES & 2011, John Wiley & Sons, Ltd. www.els.net 5