Critical Reviews in Biotechnology, 25:199204, 2005

c Taylor & Francis Inc.

Copyright

ISSN: 0738-8551 print / 1549-7801 online
DOI: 10.1080/07388550500361994

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Nanotechnology and Potential

of Microorganisms
Debaditya Bhattacharya and
Rajinder K. Gupta
School of Biotechnology, Guru
Gobind Singh Indraprastha
University, Delhi, India

ABSTRACT There is a growing need to develop clean, nontoxic and environmentally friendly (green chemistry) procedures for synthesis and assembly of
nanoparticles. The use of biological organisms in this area is rapidly gaining
importance due to its growing success and ease of formation of nanoparticles.
Presently, the potential of bio-organisms ranges from simple prokaryotic bacterial cells to eukaryotic fungus and even live plants. In this article we have
reviewed some of these biological systems, which have revolutionized the art
of nano-material synthesis.
KEYWORDS nanomaterials, ecofriendly, prokaryotes, eukaryotes, s-layer, nanoparticles

INTRODUCTION

Address correspondence to Rajinder K.

Gupta, School of Biotechnology, Guru
Gobind Singh Indraprastha University,
K. Gate, Delhi 110006, India. E-mail:
rkg67ap@yahoo.com

Nanotechnology is the term used to describe the creation and exploitation of materials with structural features in between those of atoms and bulk
materials,34 with at least one dimension in the nanometer range (1nm =
109 m). The field of nanotechnology has gained tremendous impetus during the last decade and is expected to grow enormously in the years to come.
The National Science Foundation in the United States believes industrial production for this sector could exceed $ 1 trillion or more between 2010 and
2015.
Such a tremendous growth in the science of nanotechnology is primarily due to the availability of new methods for the synthesis of nanomaterials in addition to the improved tools for characterization and manipulation. Several methods for the synthesis of nanomaterials and nanotubes,
and their assemblies, are now available. These include various inorganic, organic and biological systems, all with control of size, shape, and structure.
To fulfill the ever-growing need to develop environmentally benign nanoparticle synthesis, researchers are now turning to biological systems as a new approach. This approach of evolving novel materials with unexpected properties
is termed biomimetics, defined as material science and engineering through
biology.39
This review examines some of the biological microorganisms predominantly
used in the biosynthesis of nanomaterials.
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BACTERIA AS WORKERS FOR

NANOMATERIAL BIOSYNTHESIS
The development of reliable, eco-friendly processes
for the synthesis of nanomaterials is an important aspect of nanotechnology. Nanotechnology also requires
the synthesis of nanomaterials of different chemical
compositions, sizes and controlled disparity. Many organisms, both unicellular and multicellular, are known
to produce inorganic materials either intracellularly or
extracellularly.23,44 One approach that shows immense
potential is based on the biosynthesis of nanomaterials
using bacteria.
Microorganisms, particularly bacteria, are often exposed to extreme environmental conditions and an
ability to resist those stresses is essential for their survival. The specific defense mechanisms help the bacteria to quell such stresses, including the toxicity due
to high concentration of foreign metal ions or metals. Such mechanisms include efflux systems, alterations of solubility and toxicity by changes in the
redox state of the metal ions, extracellular complexation or precipitation of the metals intracellularly (often
via formation of metal sulfides), and the lack of specific metal transport systems.7,36,43 This forms the basis of many important applications of microorganisms
such as bioleaching, bioremediation, microbial corrosion, as well as biomineralization and the synthesis of
nanoparticles.10,19 Bacteria intervene in mineral precipitation reactions directly as catalysts of aqueous chemical reactions and indirectly as geochemically reactive
solids.49
Biological systems provide many examples of specifically modified nanostructured molecules with highly
optimized properties and characteristics. The biological
material can thus be seen as a nanophase system in its
own right and as the starting point for producing other
novel nanophase systems.20 Some of the well-known
examples of bio-organisms synthesizing inorganic materials include diatoms (which synthesize siliceous
materials),22,31 bacteria carrying a paracrystalline cell
surface layer (S-layer)33 and magnetotatic bacteria
(which synthesize magnetite nanoparticles).11,48 Magnetotatic bacteria represent a heterogeneous group of
prokaryotes with a variety of morphological types. They
all intracellularly synthesize magnetic nanocrystals in
magnetosomes. The particles consist of Fe3 O4 and
Fe3 S4 , have a specific size range (35120 nm) and are
surrounded by a membrane. The morphologies of the
D. Bhattacharya and R. K. Gupta

magnetic iron particles include cubo-octahedral, elongated hexagonal prismatic and bullet-shaped.20,40
According to Pum and Sleytr,33 monomolecular twodimensional crystalline arrays of S-layer proteins provide quite a different approach for the functionalization of inorganic surfaces. In general terms, S-layers are
composed of single protein or glycoprotein species with
a molecular mass ranging from 40 to 200 kDa, they
form the outermost cell envelope of many bacteria and
are a common feature of archaea.33 Due to the high
density of functional groups on the outermost surface
and the ability of S-layer proteins to recrystallize into
monomolecular protein lattices on artificial supports,
Langmuir lipid films and liposomes, they have been
exploited as matrix for the immobilization of foreign
macromolecules and as templates for binding of preformed nanoparticles or for their in situ synthesis.15,33,38
It has been recently found that the S-layer protein SbpA
of Bacillus sphaericus CCM 2177 recognizes a pyruvylated secondary cell wall polymer (SCWP) as anchoring
structure to the peptidoglycan-containing layer.9,17,37
It is relatively recently that the material scientists
have been viewing the microorganisms as potential ecofriendly nanofactories.6,18,19,47 Metal accumulation by
microbes may occur in two steps: a rapid reversible and
metabolically independent surface binding followed
by metabolically dependent, irreversible, intracellular
accumulation.5,46
Beveridge and co-workers have demonstrated that
gold particles of nanoscale dimensions may be readily precipitated within bacterial cells by incubation of
the cells with Au3+ ions.6,47
Klaus-Joerger et al.18,19 have shown that the bacterium Pseudomonas stutzeri AG259 isolated from a silver
mine when placed in concentrated aqueous solution of
AgNO3 resulted in the reduction of the Ag+ ions and
formation of silver nanoparticles of well-defined size
and distinct morphology within the periplasmic space
of this bacterium. The particle size and morphology are
dependent on several physical and chemical growth parameters, e.g. pH, incubation time, growth in light or
dark, and/or composition of the culture medium.19 The
silver nanoparticles produced using P. stutzeri AG259
sized up to 200 nm and were often located at the
cell poles. In addition to the triangular nanoparticles,
a small number of silver sulfide crystals were also observed along with a few large crystals embedded in the
middle of the whole cells. Using EDX spectrum (energydispersive X-ray analysis) it was determined that the
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silver sulfide crystals had a molecular formula of Ag2 S,

termed acanthite. The large crystal had undetermined
structures.19 Such a response of reduction of Ag+ to Ag0
may be due to the fact that Ag0 is a less toxic form.20
The formation of acanthite crystal may be caused by a
facile reaction of the silver particles with H2 S gas, which
was reportedly produced by P. stutzeri.45
P. stutzeri AG259 was further employed by KlausJoerger et al.18 for the production of ceramic-metal composites, commonly known as cermets. These cermets exhibit interesting optical and electrical properties, such
as spectrally selective light absorption and tunable electrical resistivity. Cermet material consisted of an organic carbon matrix with embedded, crystalline metallic silver particles deposited as thin films on aluminium
substrates.18 Subsequent heat treatment at temperatures
between 300 C to 400 C was used to stabilize the films
and adjust the optical properties.18 This carbonaceous
coating containing silver and backed by aluminium substrate has a potential application as a solar absorbing
coating.
Nair and Pradeep have synthesized nanoparticles of
gold, silver and their alloys using the bacterial strain
Lactobacillus sp. common in buttermilk.29 Gold-based
nanoparticles were formed using HAuCl4 . UV/VIS
spectrum of the Au sample after 12 h of exposure
showed a well-defined surface plasmon band centered
around 540 nm characteristic of colloidal gold. After
heating to 200 C, the precipitated material formed elemental gold. Two kinds of size ranges were seen for
gold crystals, one in the range of 2050 nm, called clusters, and the other one above 100 nm, called crystals.29
Clusters were present within and outside the bacterial
contour, whereas the crystals were only detected within
the bacterial contour. The crystals were of fairly uniform
size, and were mostly hexagonal, in addition to some
triangularly shaped ones.29
Silver based clusters were formed with AgNO3
(AgNO3 was mixed with whey).29 UV/VIS spectrum after 12 h of exposure showed a well-defined surface plasmon band at 439 nm. The smallest particles observed
were in the range of 15 nm and the largest particles were
around 500 nm formed along the axis.29
Accumulation and reduction of Au3+ inside Bacillus
subtilis have also been reported before.47 The reduction
process is mainly caused by the acids and sugars present
in the medium. The initial nucleation of the clusters
mostly occurs extraneous to the bacterial cells followed
by the transfer of ions into the bacterial cell. Subse201

quently, the formed nanoclusters grow within the cells,

which appear to involve coalescence.29
The actinomycete Thermomonospora sp. has recently
been identified as an exciting candidate for the synthesis of gold nanoparticles by chemical reaction of the
biomass with aqueous chloroaurate ions.3 The identification of Thermomonospora sp. was significant since
the actinomycete was involved in the extracellular synthesis of metal nanoparticles, unlike other prokaryotes,
and offered greater scope for development via genetic
modification through modern methods of recombinant
DNA technology and protein engineering. Moreover,
this actinomycete produced high concentration gold
nanoparticles with good monodisperity as compared
to other microbial species, with average size of 8 nm
particles.3

POTENTIAL OF EUKARYOTES IN
NANOPARTICLE SYNTHESIS
Until now, we have witnessed a wide range of
prokaryotes as prospective nanoparticle synthesizers.
One major advantage of having prokaryotes as nanoparticle synthesizers is that they can be easily modified using genetic engineering techniques for overexpression
of specific enzymes, apart from the ease of handling.
However, the use of eukaryotes, especially fungi, is
potentially exciting since they secrete large amounts of
proteins, thus increasing productivity, and are simple to
deal with in the laboratory. Moreover the process can
be easily scaled up, economically viable with the possibility of easily covering large surface areas by suitable
growth of mycelia.26 Furthermore, downstream processing would be much simpler using fungi.26
One of the novel works defining the use of fungus
for nanoparticle synthesis was carried out by Mukherjee
et al.26 for the intracellular production of silver nanoparticle using Verticillium, (AAT-TS-4). Verticillium, when
exposed to aqueous AgNO3 , caused the reduction of
the metal ions and formation of silver nanoparticles of
about 25 nm diameters. It was also determined that the
mechanism for the formation of the silver nanoparticle was different from those earlier stated regarding the
role of peptides like glutathione, which implicated the
formation of metal sulfide nanoparticles like CdS10 and
Ag2 S8 by reacting yeast cells with appropriate metal
ions. From the UV-VIS spectra recorded the most probable mechanism was the intracellular or surface reduction of Ag+ ions for the synthesis of silver nanoparticles
Nanotechnology and Potential of Microorganisms

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by the fungus.26 Since the nanoparticles are formed

on the surface of the mycelia, it was believed that the
first step involved the trapping of the Ag+ ions on the
surface of fungal cells, maybe by electrostatic interaction between the Ag+ and negatively charged carboxylate groups in the enzymes present in the cell wall of
mycelia. Thereafter, the silver ions were reduced by enzymes present in the cell wall leading to the formation
of the silver nuclei, which subsequently grew by further reduction of Ag+ ions and accumulation on these
nuclei.26
Similar results were obtained for the fungus Verticillium on aqueous solution of AuCl4 ions, resulting
in the in situ reduction and consequent formation of
gold nanoparticles of good monodisperity.25 However,
the above studies using Verticillium showed intracellular
formation of silver and gold nanoparticles.
In 2002, Mukherjee et al.27 carried out extracellular
synthesis of gold nanoparticles using fungus Fusarium
oxysporum with aqueous AuCl4 ions. The most plausible reason for the reduction of AuCl4 ions might be
the release of reductases by the fungus into the solution,
specifically the release of NADH-dependent reductases.
Longterm stability of the nanoparticles was also observed, which might be due to the presence of specific
fungal proteins in the solution.27 The gold nanoparticles produced by F. oxysporum were in the range
of 840 nm sizes and were more monodisperse than
those synthesized intracellularly with bacteria.20,47 This
was the first report on extracellular synthesis of gold
nanoparticles by a eukaryotic system such as fungi.27
Developing reliable protocols for the synthesis of
nanometer scale semiconductor particles is a problem
of great importance,4,42 and recently microorganisms
have been sought after for the process. While enzymatic processes in sulfate reducing bacteria are relatively
well understood32 and identified in the formation of
biofilms of sphalerite (ZnS)21 and CdS,16 the intracellular synthesis of CdS in yeast10,32 occurs by a process
involving sequestering of the Cd2+ ions glutathionerelated peptides and a consequent production of CdS
within the yeast cells.35
Ahmad-Mukherjee et al.1 reported regarding the
synthesis of CdS and other metal sulfide nanoparticles extracellularly by a purely enzymatic process.
F. oxysporum, when exposed to aqueous Cd2+ and SO2
4
in solution, led to the formation of extremely stable
CdS nanoparticles in the solution.1 The longterm stability of the nanoparticles is due to the presence of
D. Bhattacharya and R. K. Gupta

the proteins in the nanoparticle solution that bind to

the surface of the nanoparticle and prevent aggregation.
It was also determined from various experiments that
F. oxysporum released reductases enzyme into the solution that was responsible for the formation of CdS
nanoparticles from Cd2+ and SO4 2 ions.1 This was
the first report on the secretion of sulfate reducing enzymes by a fungus.1
The formation of extracellular CdS nanoparticles by
enzymatic reduction of sulfate ions by F. oxysporum
was extended to the formation of PbS, ZnS, and
MoS2 nanoparticles starting with appropriate sulfatecontaining salts.1
F. oxysporum was later utilized for the extracellular
production of silver nanoparticles2 by adding the fungal biomass to aqueous solution of AgNO3 . The reduction of the Ag+ ions occurred through the release
of reductases into the solution by the fungus. The solution was extremely stable with no flocculation even
a month after reaction due to the presence of specific
fungal proteins in the solution. This was the first report
on the extracellular synthesis of silver nanoparticles by
a eukaryotic system such as fungi.2
Production of nanoparticle using inactivated alfalfa biomass has been reported in which the biomass
reduced gold (III) ions in solution to gold (0)
nanoparticles.13
Yacaman et al.12 reported about the formation of
gold nanoparticles inside live alfalfa plants. The alfalfa
plants were grown in an AuCl4 rich environment. The
absorption of Au metal by the plants was confirmed by
X-ray absorption studies and transmission electron microscopy. Nucleation and growth of Au nanoparticles
in a crystalline state inside the plant was confirmed with
icosahedral geometry. This was the first report on the
formation of gold nanoparticles by living plants.12

WHY NANOTECHNOLOGY
In this review, we have witnessed how the material
science is connected to biotechnology, leading to a new
emerging field of nanobiotechnology. With increasing
success of bio-organisms in the formation of nanomaterials, the potential of nanotechnology is also ever increasing in spectrum of science. Newer methods for the
production of nanomaterials and support membranes
are imminent.41 The applications of nanotechnology
now range from nanophase ceramic materials in textiles and plastics to non-linear optics and optoelectronic
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applications.30 The most important and far-reaching applications of nanomaterials will be in nanodevices and
nanoelectronics.
In addition to electronics, nanotechnology will be
extremely useful to biology. Carbon nanotubes are being used as tips in scanning microscopes and as efficient
field emitters for possible use in display devices. Colloidal gold particles attached to DNA strands can be
employed to assay specific cDNA.24,30 Nanotechnology is further bound to improve DNA microchip arrays, involving lithographic patterning.14 Recently, a
new PCR driven method for identification of a unique
set of sequences that bind to silver and cobalt nanoparticles from a phage peptide display library has been
developed.28 Similarly, drug and gene delivery will
be more effective with the use of nanoparticles and
nanocapsules.30,34 Other applications include the use
of nanosensors in monitoring the environment and living systems, as well as in the improvement of prosthetics
used to repair or replace parts of the human body.
Thus, it is truly an interdisciplinary area, encompassing physics, chemistry, biology, material science and
engineering.

ACKNOWLEDGEMENT
We are grateful to Prof. Margit Sara, Center for
Nanobiotechnology, Department of Biotechnology,
University of Natural Resources and Applied Life Sciences, Vienna, for her thorough revision of this review
and providing us with her invaluable suggestions.

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