Selvakumar
Selvakumar
Selvakumar
Biotemplates from microbial origin have been a new source of inspiration for designing and fabricating
intricate, high surface area structures that possess potent applications in nanotechnology. Microbial
biotemplates are useful for synthesizing nano/micro structural materials based on a bottom up
approach. Being from nature, microbial biotemplates with their extraordinarily molecular machinery have
been reported to be considerably superior and cost effective for fabricating complex and heterogeneous
structures when compared to the conventional and advanced lithographic techniques. The advantage of
speedy growth and multiplication along with controlled shape, structure and size, make microorganisms
a viable template for preparing nanomaterials of defined size and shape. In this review, we have
Received 31st July 2014
Accepted 29th September 2014
consolidated the recent advances in the synthesis of nano/micro structures using biotemplates obtained
from various types of microorganisms like bacteria, fungi, algae and virus, and have highlighted its
DOI: 10.1039/c4ra07903e
possible applications. This review excludes biomolecules like DNA, protein and lipid based biotemplates
www.rsc.org/advances extracted from various microorganisms.
52156 | RSC Adv., 2014, 4, 52156–52169 This journal is © The Royal Society of Chemistry 2014
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have many advantages. These biotemplates are natural, eco- fungal and algae including diatoms based biotemplates have
friendly, inexpensive, having metal ion binding capacity, been taken into consideration. We have also highlighted the
stability and high production yield. They can be used to application of nanostructures derived through these microor-
synthesize nanomaterials at room temperature using so ganism based biotemplates.
chemical processes, which are mostly ecofriendly in nature.
Biological systems have been reported to exhibit multiple levels
of hierarchical structures from microscopic to macroscopic
2. Microorganism based biotemplate
length scale.5 Despite the presence of micro and macroscale 2.1 Bacteria based biotemplates
structures in biological systems, their building blocks are 2.1.1 Whole cell template. Various living microorganisms
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mostly in nanoscale. The examples of such naturally available and their features are closely related to the recent nano-
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nanostructures include nanostructure in bone formation,6 structures developed using chemical and physical methods.
nanostructures in lotus leaf,7 nanostructures reported in Hence these living microbes and their special structures can be
buttery wings and nanostructures in various living used as biotemplate. Bacterial surface structures and
organism.8–10 Microorganisms and their nano and microstruc- morphology is one such feature looked into as a biotemplate.
tures are always the most preferable biotemplate because of their Different strains of bacteria such as B. subtilis, E. coli, S. ther-
low generation time, easy growth conditions, possibility of mass mophilus, S. typhimurium have been used as templates for the
multiplication and scalability and its inherent resistant proper- micro/nanostructure formation. Some of the bacteria possess
ties towards various environmental conditions. The microbial self-assembled nanostructures on its cell wall which is made up
cell wall functional groups like carboxyl, phosphate and amide of surface layer proteins (S layer).13 These S-layer proteins have
groups favor an atmosphere for metal binding and nucleation, multiple functions like maintenance of cell shape and struc-
which in turn leads to the formation of nanoparticles/structures ture, template for ne grain mineralization, pathogenicity and
on its surface.11 The exopolysaccharides produced by these cell adhesion, surface recognisation, as a protective coat and for
microbes especially bacteria impart negative charge through attachment to surface which makes them survive in adverse
carboxyl and phosphate groups, which also allow the nucleation environmental conditions.14,15 These protein nanostructures are
of positive charged metals like silver and leads to the formation either found embedded into the cell wall surface or attached to
of nanostructures in solution.12 the cell wall supercially through secondary cell wall poly-
Considering these facts and advantages of biotemplating, mers.16 The assembly of S-layer protein can be of different
several researchers have focused onto microbes with unique symmetries like P1, P2, P3, P4 and P6 and differs from one
structural and functional properties as a possible biotemplate organism to the other. Such symmetries give different structural
for the synthesis of nanostructures of different size, shape and arrangement and shape to cell wall surface which can inturn be
morphology. In this review, we have consolidated the recent used as biotemplate. The P1 and P2 symmetry give oblique
updates on the use of microorganism as biotemplate for the template structure where as P3 and P6 give hexagonal structure
nanostructure formation. We have excluded extracellular and to the cell wall surface. P4 gives square shaped structure (Fig. 1).
intracellular synthesis of nanoparticles by microorganisms These S-layers can be reassembled into dened symmetries
because several reviews are available on it. Bacterial, viral, even onto various matrices like mica, silicon, lipid interfaces,
Fig. 1 Bacterial cell wall with different types of S-layer symmetries and structures. Adopted from ref. 16 with permission.
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liposomes, nanocapsules, polyelectrolyte layers and even on nanoclusters coated bacterial structure. Followed by formation
solution there by acting as a suitable biotemplate for further of ZnS nanoclusters the cellular materials were removed by high
synthesis of different nanostructure having precise shape and intensity ultrasound process leaving the hollow ZnS nano-
size.17 Mark et al.18,19 used 2D microbial S-layer protein bio- structure behind (Fig. 3, method 2).26 Yang et al.27 prepared
template for preparing dentrimer-encapsulated nanoparticle hollow porous silver microspheres using Streptococcus thermo-
arrays and metallic and semiconductor nanoparticle arrays. philus as a bacterial template using same approach of sonica-
Mark et al.20 tried using S-layer protein based biotemplated tion. They found that these silver microspheres were Raman
assembly of colloidal gold etch mask for the fabrication of active when tagged with Raman probe like 2-mercaptopyridine
silicon nanopillar arrays. These nanopillars were of 60–90 nm using surface enhanced Raman spectroscopy (SERS) study. The
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tall, 8–13 nm wide at the tip, 15–20 nm wide at half height and silver microspheres were also porous in nature there by exhib-
Open Access Article. Published on 29 September 2014. Downloaded on 18/06/2016 17:15:35.
20–30 nm at base (Fig. 2). Silica enhanced S-layer protein cages iting higher surface area for interaction. Zhou et al.28 prepared
were prepared by Schuster et al.21 using liposomal assembly. TiO2 micro/nanostructures using these bacterial templates
S-layers were reassembled onto liposomes and subjected to through a surface sol–gel process. The hollow sphere and tube
silicication. Aer silicication, the lipid components were structures of TiO2 nanostructures were formed through a series
dissolved using suitable detergent. The organism without of hydrolysis processes and calcinations (at 700 C) and tested
S-layer and with S-layer can as such be used as biotemplate to for photocatalytic activity. These structures were found to show
synthesis dened nano/microstructures. Bacteria use their high photocatalytic activity under UV-visible radiation (Fig. 3,
efflux system/oxidation/reduction mechanisms/cell wall func- method 3). Recently, Zhang et al.29 have prepared Co3O4 deco-
tional groups to detoxify the metal contaminants that they rated ZnO hollow spheres with a porous shell at a low temper-
encounter in the surrounding media and escapes from the ature using Microzyme cells as a biotemplate and have tested it
environmental stress. Bacteria like Shewanella sp. strain HN-41 for sensing gases like CO, H2, H2S, and vapors of ethanol and
have been reported to produce arsenic–sulphide nanotubes of acetone. These Co3O4-decorated ZnO hollow spheres were
20–100 nm in diameter by 30 mm in length via reduction of As(V) effective in sensing acetone followed by ethanol; whereas, the
and S2O32 using dissimilatory metal reducing process. These same structures were ineffective in sensing CO, H2 and H2S at
nanotubes behaved as metal and semiconductor nanomaterial 50 ppm of initial concentration. Bacteria/ZnO core–shell
with electrical and photocatalytic property, which can nd spheres have been prepared by a hydrothermal method. The
applications in nano and optoelectronics.22 This potential of formation of such structures mainly depends on the pH of the
bacteria to accumulate metals/minerals intra- or extracellularly medium. At acidic pH, metal ions bind to the carboxyl and
has made them an ideal candidate for biotemplate leading to a phosphate groups of the biotemplate. The metal ions form a
nanostructure formation.4,23 Nickel nanostructure was synthe- complex with the amine group at pH higher than 8 and leads to
sized using Bacillus subtilis as a biotemplate by exploiting the core–shell like structure.26 Hollow zirconia particles were
redox reactions of their surface amino acids. Microscopic synthesized using E.coli cells as a biotemplate. It has been
studies revealed the formation of nanostructures according to observed that the presence of water in templates results in the
the morphology of the bacteria used.24 ZnO, ZnS and TiO2 hydrolysis of zirconium butoxide leading to the formation of
nanostructures were prepared using Streptococcus thermophilus zirconia hollow particles.30 Yang et al.31 developed hierarchically
and Lactobacillus bulgaricus as biotemplate (Fig. 3). ZnO hollow branched Au-nanowire/E.coli nanocomposites using CTAB
spheres were prepared using Streptococcus thermophilus as bio- directed bacterial template (E.coli). These Au-nanowires showed
template through a simple hydrothermal process followed by increased adsorption at near IR region (1900 nm). Kaehr and
calcinations at 600 C (Fig. 3, method 1).25 ZnS nanostructures Brinker32 reported that the segregation of a catalytic region on a
were formed using these biotemplate through sonochemical biotemplate is possible by exploiting the polar segregation
and ultrasound process. ZnS nanoparticles were subjected to process of dividing E.coli cells. They also suggested that the
sonication in the presence of bacterial template to form ZnS formation of more complex materials and architectures are
Fig. 2 Bionanofabrication of vertically aligned silicon based nanostructures using bacterial S-layers. Modified from ref. 20 with permission.
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Fig. 3 Synthesis of various forms of ZnO, ZnS and TiO2 nano/microstructure using bacterial morphology.25,26,28
Fig. 4 Various nanostructures derived using entire cell of bacteria. FESEM images of E. coli templated hollow silica microparticles (a) (insert:
cross sectional view of calcined particle),84 B. sthermophilus/ZnO core–shell spheres (b),25 SEM images of crushed calcined zirconia particles
using E.coli template (c),30 Co3O4-decorated ZnO hollow spheres (d),29 Au nanostructures synthesized by the reduction of aqueous HAuCl4 (e),31
SEM image of H2O2 etched Ag microspheres at a higher magnification using S. thermophilus template (f),27 FE-SEM image of uniform, bacteria-
supported, hierarchical Co3O4 superstructures produced without changing the spherical shape of the original micrococcus template (g)85 [all
images were obtained with permission].
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possible by chemical, genetical and connement induced nanoparticle arrays using engineered bacterial agellar FliC
modication in bacterial morphology and bacterial surface proteins obtained from mesophilic bacteria. The FliC protein
properties. Various nanostructures obtained using whole was further modied at peptide loops, such as histidine and
bacterial cell as a biotemplate has been consolidated in Fig. 4. cysteine loops, and various nanoparticles like Au, Ag, and Cd
2.1.2 Bacterial agella. Other than the entire cell, bacterial were allowed to bind to the histidine loops. Such binding
structures like agella and pili have been used as a biotemplate resulted in an ordered array of nanoparticles on agella nano-
for the synthesis of nanostructures. These agella and pili are tubes. They also prepared other organic and inorganic nano-
used for mobilization and communication between one bacte- particle arrays and nanotubes made of hydroxyapatite, silica
rium to the other. Natural and genetically engineered agella and titania using a similar approach.38 Ovalbumin coated
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have been studied as templates/scaffolds for the formation of agellin nanoparticle were prepared from Salmonella enteritidis
Open Access Article. Published on 29 September 2014. Downloaded on 18/06/2016 17:15:35.
metal nanostructures.33,34 Hesse et al.34 used a mineralization derived agellin and studied for its immune adjuvant capacity
process for the formation of nanotubes from bacterial agella. for the development of an oral vaccine.39 They reported that the
They depolymerised the agella into agellin monomers and vaccine conjugated with agellin in the form of a nanoparticle
repolymerized it using Na2SO4 to form agellin seeds. These along with ovalbumin were found to exhibit strong, long lasting
seeds were further used to develop lengthy agella. The systemic and mucosal immune responses than the respective
repolymerised lengthy agella were deposited with titanium by non-conjugated vectors. Wang et al.40 synthesized periodic
a ceramic thin lm deposition technique and further mineral- nanohole arrays along with silica bers using high temperature
ization at 50 C to obtain agella coated with TiO2 nanoparticles calcinations of silica nanotubes synthesized using agella
of anatase phase having a particle size of 5–10 nm. On obtained from Salmonella sp. They also demonstrated the
annealing these agella coated with TiO2 nanoparticles at application of these double-layered silica-agella nanotubes for
200 C, they achieved nanotubes sized from 200–300 nm in selective CdTe quantum dot uptake into the innerchannels or
diameter. Our group used similar approach to develop one selective Au nanoparticle coating on the outer wall of the
dimensional silver nanoparticle coated nano/micro structure nanotubes by the difference in chemistry between inner
using Salmonella typhimurium agella.35 In this work, we have agellum core protein and outer silica wall of the nanotubes. Jo
demonstrated two different approaches to prepare agella et al.41 prepared silica nanotubes using bacterial agella as
based silver nanoparticle coated bionanomaterial (Fig. 5) template and coated them with various types of nanoparticles
having increased conductivity. We have also proved that the made up of gold, palladium and iron oxide using reductive
deposition of such bionanomaterials onto a graphite electrode metallization or oxidative hydrolysis. Similar to Jo et al.,41 Li
can enhance the conductivity of the electrode surface that can et al.42 prepared morphologically controlled silica nanotubes
be used in microbial fuel cells.36 Similar nanoparticle impreg- using bacterial agella as a biotemplate. They manipulated the
nated agella was prepared by Deplanche et al.33 They immo- morphology by changing the pH and using a peptide display to
bilized stable gold and palladium nanoparticles onto normal prepare silica nanotubes. They were also successful in
and genetically engineered agella isolated from Desulfovibrio preparing sol–gel mediated hollow double layered core–shell
desulfuricans to form nano-microstructures, which can be useful titania/silica nanotubes under ambient conditions using
for catalyst formulations. Mudalige et al.37 synthesized various
Fig. 5 Possible mechanism for silver nanoparticle impregnation onto bacterial flagella35 (reproduced with permission).
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Fig. 7 Synthesis of porous carbon containing ordered hierarchical zirconium phosphate nanoparticles using yeast as a biotemplate. Adopted
from ref. 57 with permission.
structures showed a better electrocatalytic property when Similar to bacteria, the different morphological forms of algae,
compared to a commercially available manganese dioxide air such as unicellular, lamentous and as colonies, can be used as
electrode, and hence, it can be widely used in fuel cell tech- a biotemplate for the synthesis of nanostructures. Various
nology. Wang et al.58 exploited Pastoris (PPCs) cells as a bio- structured and patterned skeletal morphologies of algae that
template to prepare closely packed, size controllable gold can be used for the biomimetic fabrication of nanostructures
nanohorns (AuNHs) and AuNHs/PPCs nanocomposite by a are presented in Fig. 8.
chemical method. These AuNHs/PPCs nanocomposite exhibi- Some algae, like diatoms, take part in the process of
ted high Raman enhancement effect when tested with Rhoda- mineralization, which is more fascinating to form different
mine 6G. nanostructures. Diatoms are unicellular, eukaryotic microalgae
that can be seen in fresh and saltwater ecosystems. Diatoms
2.3 Algal biotemplates have a very interesting model system with high potential in the
nano-structured production as there are almost 100 000
Algae are aquatic organisms with photosynthetic ability. They
different species with unique frustule morphologies.59 Diatoms
appear as either single cellular or multicellular organisms.
Fig. 8 Various structural and patterned skeletal morphology of algae that can be used for the biomimetic fabrication of nano/microstructures.
Euglena spirogyra (a) Batrachospermum sp. (b) Desmodes musopoliensis (c) Pithophora sp. (d) (with multiseriate morphology), Oscillatoria sp. (e)
Asterionella sp. (f) Triceratium favus (g) Volvox sp. (h) Micrasterias crux-melitensis (i) Desmidium swartzii (j) Vaucheria sp. (k) Biddulphia ante-
diluvian (l) Closterium costatum (m) Anabaena sp. (n) Pediastrum sp. (o) (courtesy: Google images on algae and diatoms, http://
microscopy.uk.org) (ref. 86).
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have rigid cell wall structure called frustules, which are made of stress. The brittle nature of these frustules can be changed into
silica. These structures are created naturally in a controlled ductile through structural arrangements at the nanoscale
manner which provides them a unique morphology. These level.66 Al/Tp ordered macroporous–mesoporous carbonaceous
frustules have two halves called thecae. The top and bottom part materials were prepared using Thalassiosira pseudonana as a
of these thecae are called valves which are made of nano- biotemplate.67 Zhou et al.68 synthesized ordered porous ZnS
structures granular silica.60,61 The new theca are created in a nanostructures using Coscinodiscus lineatus as a biotemplate via
vesicle called a silica deposition vesicle, which have silaffins a sonochemical method (Fig. 9). Using such a biotemplate and
and long-chain polyamines that are involved in the precipita- biomineralisation process, various materials have been devel-
tion of silicic acid into silica. These silica shells are synthesized oped for multiple applications. A few of the recently reported
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by the polymerization of silicic acid. This individual silica diatom based materials are shown Table 1. The nano and
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frustule consists of two valves, which are held together by bands microstructures produced using diatoms as biotemplates are
like structures called girdle bands. There are three types frus- presented in Fig. 10.
tules based on its structure viz., rod, ake and three dimen-
sional (3D) shaped frustules. Rod shaped frustules show a 2.4 Viral templates
higher assembling property with larger area coverage when
Viruses are infectious agents composed of a proteinaceous shell
compared to other shapes, which can be used in monolayer
surrounding their genetic material that can live only in living
formation. Flake shaped frustules act as possible biocarriers
cells. They lack their innate metabolic activity and remains as
and are used for biodetection. 3D frustules have very good
virions (for more introductions on viruses, its classication and
porosity that can be used in drug delivery applications.62,63 The
structure, the readers are advised to refer to basic microbiology
frustule valves are separated by plates, which appear like
books). This property makes viruses as suitable and safe
chambers. These plates contain pores varying in diameter either
building blocks for preparing composite materials.69 The
increasing or decreasing from outside to inside. The size and
protein shell of virions facilitates mineralization/metallization
positioning of these pores are genetically determined. The
process via amino acids present on their surface. For example,
smallest pore (40 nm) has been observed in Coscinodiscus sp.
aspartic acid, glutamic acid, lysine, arginine and cysteine amino
and Thalassiosira eccentrica.64,65 These unique structure and its
acids present in a viral cell wall have more affinity towards metal
skeletons have been considered as a potential biotemplate for
ions because of the presence of carboxylate, amino and thiol
the synthesis of various nanostructures that cannot be easily
groups. Such affinity of viruses and virus like particles towards
prepared by conventional and advanced techniques that are
metals and ions has found immense application as scaffolds
available. Although the silica structures in diatoms are brittle in
and templates for nanostructure formation. The molecules of
nature, its nanoporous structure provides good toughness to
interest are liganded via a bioconjugation process. The possi-
the frustules, which can withstand considerable environmental
bilities of viral manipulation and engineering through
Fig. 9 Synthesis of diatom-templated ordered porous ZnS meso/nanostructures68 (reproduced with permission).
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Table 1 Nano and micro structure prepared using various microorganisms as a biotemplate
Bacteria
RSC Advances
110
111
112
113
114
116
115
117
118
nanomaterials through mineralization/metallization
91
92
76
97
96
95
78
processes.69 The viral surfaces can also be chemically engi-
neered to attain desirable properties. A few of the chemical and
molecular biology approaches used to modify viral surfaces are
bioconjugation and covalent modication, introduction of
specic surface display genes through genetic engineering and
membrane anchoring. These virus based materials can be two
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Solar cell
the viruses used by scientists are plant viruses and are selected
on the basis of their nonpathogenecity to human beings and
—
—
—
—
—
—
—
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—
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animals. The frequently studied viruses for biotemplating are
non enveloped plant viruses like tobacco mosaic virus (TMV),
cowpea mosaic virus (CPMV), or cowpea chlorotic mottle virus
(CCMV). They are also selected on the basis of the shape and
size requirement. For example, viruses such as M13 phage and
TMV are rod shaped and CCMV and CPMV are spherical shaped
viruses. The length, inner and outer diameter of TMV are 300, 4
and 18 nm, respectively.73 This inner diameter has a great
signicance in forming nanostructures. Various metal nano-
silica to silicon diatom frustules
Magnesiothermic conversion of
templates and metal binding sites (Fig. 11). Apart from these
nanotube composites
Co3O4 nanowire
Au nanoshell
Cu nanowire
Frustules
Phage
Virus
fd phage
of the phage rather than the ends (p3). M13 phage was used to
Table 1
Virus
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Fig. 10 Microscopic images of materials prepared using various diatom as biotemplate, Palladium frustule replica synthesized via electroless
deposition (a),87 diatomite with faujastic crystals (b),88 polymer-silica composite made using T. weissflogii frustules (c),89 Navicula frustules after
annealing at 1000 C for 2 h (d),123 macroporous carbon/aluminium composite obtained from Thalassiosira pseudonana (e),67 diatom-TiO2/SiO2
composite of Cocconeis placentula frustules (inset: high resolution image of TiO2/SiO2) (f),90 SEM images of an Aulacoseira sp. frustule after the
magnesiothermic conversion process (g),91 Carbon nitride coated onto single frustules of Celatom FW-14 diatomite (h),82 carbon/Al-Thalassiosira
psesudonana (C/Al-Tp) composites (i),67 gold-coated Coscinodiscus asteromphalus frustule valve (j),93 free standing silica free cavities after ion
milling gold coated Coscinodiscus asteromphalus (k),93 gold structures replicated from the frustules of Coscinodiscus species (l)94 (all images
reproduced with permission).
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12 R. Selvakumar, S. Aravind, M. A. Anuradha and
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