Photonic Potential of Haloarchaeal

Pigment Bacteriorhodopsin for Future

Electronics: A Review

Ravi Ashwini, S. Vijayanand &

J. Hemapriya

Current Microbiology

ISSN 0343-8651

Curr Microbiol
DOI 10.1007/s00284-017-1271-5

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 Author's personal copy
Curr Microbiol
DOI 10.1007/s00284-017-1271-5
REVIEW ARTICLE
Photonic Potential of Haloarchaeal Pigment Bacteriorhodopsin
for Future Electronics: A Review
Ravi Ashwini1 • S. Vijayanand2 • J. Hemapriya3
Received: 9 November 2016 / Accepted: 23 May 2017
Ó Springer Science+Business Media New York 2017
Abstract Haloarchaea are known for its adaptation in
extreme saline environment. Halophilic archaea produces
carotenoid pigments and proton pumps to protect them
from extremes of salinity. Bacteriorhodopsin (bR) is a
light-driven proton pump that resides in the membrane of
haloarchaea Halobacterium salinarum. The photocycle of
Bacteriorhodopsin passes through several states from K to
O, finally liberating ATP for host’s survival. Extensive
studies on Bacteriorhodopsin photocycle has provided in
depth knowledge on their sequential mechanism of con-
verting solar energy into chemical energy inside the cell.
This ability of Bacteriorhodopsin to harvest sunlight has
now been experimented to exploit the unexplored and
extensively available solar energy in various biotechno-
logical applications. Currently, bacteriorhodopsin finds its
importance in dye-sensitized solar cell (DSSC), logic gates
(integrated circuits, IC’s), optical switching, optical mem-
ories, storage devices (random access memory, RAM),
biosensors, electronic sensors and optical microcavities.
This review deals with the optical and electrical applica-
tions of the purple pigment Bacteriorhodopsin.
& Ravi Ashwini
ashwiniphd18@gmail.com
S. Vijayanand
vipni76@gmail.com
J. Hemapriya
micropriya80@gmail.com
1
Bioresource Technology Lab, Department of Biotechnology,
Thiruvalluvar University, Vellore, Tamilnadu 632115, India
2
Bioresource Technology Lab, Department of Biotechnology,
Thiruvalluvar University, Vellore, Tamilnadu 632115, India
3
Department of Microbiology, DKM College for Women,
Vellore, Tamilnadu 632001, India
Introduction
Halophile (‘halo’ means ‘salt’ and ‘philos’ means ‘loving’)
are salt loving organisms that thrive well in various ranges
of salinities [78]. Haloarchaea lives in conditions of extreme
salinity like saline lakes, solar salterns and salt-fermented
foods [100]. They were found to be evolved from the
anaerobic methanogen acquiring 1047 genes which is found
responsible for catabolic metabolism, membrane trans-
porters and components required for oxygen respiration
[55, 56]. Bacteriorhodopsin is a 26 kDa protein that is first
recognized in halophilic archaea Halobacterium salinarum
formerly called as Halobacterium halobium [8, 49, 63, 86].
The photochromic protein acquired the name Bacteri-
orhodopsin based on its similarities in absorption of light,
chromophore, schiff’s base, composition of amino acids and
sequence of reactions with the visual rhodopsin found in
mammals. The cell membrane that holds bacteriorhodopsin
is called as ‘‘purple membrane’’ due to the presence of
pigment as patches [62, 64, 84] and constitutes a retinal
based photosynthetic system in the presence of sunlight
under anxious circumstances [8].
The protein contains 248 amino acids which are bound
to retinal chromophore at Lys 216 by a schiff’s base
linkage [37, 49, 66, 86]. Two dimensional crystal lattice
view through electron microscope of bacteriorhodopsin
revealed that the protein exists as trimers in purple mem-
brane and each monomer consists of seven alpha helices
running nearly perpendicular to the surface of membrane at
an angle from 08 to *208 [8, 31, 63]. The pigment acts as a
green light-driven proton pump of wavelength 500–650 nm
that converts light energy into chemical energy. This
converted light-driven energy is utilized by halobacterium
for the production of ATP, amino acid uptake and loco-
motion [61, 64, 85].
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Simulation of bacteriorhodopsin by green light initiates
photonic cascade during which protons of 10,000 times
higher folds is produced within the cell. [26, 27, 89]. This
reversible cascade lasts for 1 ps to 3 ms when light hits
bacteriorhodopsin at a range of 250 mv. The proton ava-
lanche created during the cascade makes cell more alkaline
than the outside environment and generates ATP for cell’s
survival even in deprived environmental conditions
[26, 39, 83].
Research on Bacteriorhodopsin initiated with a quest of
understanding its nature and proton pumping cycle. But in
later years, it was considered as a model system for G
protein coupled receptor (GPCR) and membrane protein
folding studies [30, 90]. In addition to these, the photo-
tactic ability of bacteriorhodopsin has also enhanced its
applications in several fields such as optical memories,
real-time holographic media, photovoltaic cells and artifi-
cial retinas [7, 14, 24, 44, 88, 99]. The necessity of bac-
teriorhodopsin for its photo tactic ability is increasing
every day and this review deals with applications of bac-
teriorhodopsin in various optical and electronic devices.
Bacteriorhodopsin Photocycle
Bacteriorhodopsin photocycle is triggered by light leading
to a series of reactions finally resulting in liberation of
proton. These sequential reactions go through the inter-
mediates K, L, M, N and O which revert the original
bacteriorhodopsin form (Fig. 1) [57] i.e. bR gets excited
from the ground state by absorbing the green light at
wavelength 568 nm and passes through the reaction K, L,
M, N and O. The final product O decays again to retain the
bacteriorhodopsin ready for next cycle [18, 36, 41, 42]. In
Fig. 1 Bacteriorhodopsin photocycle [30]
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R. Ashwini et al.
this way, proton is transferred across the transmembrane.
The photocycle initiates with the photoisomerization of
retinal that is bound covalently with protein at Lys 216 via
Schiff’s base linkage. The photoisomerization causes the
retinal all trans to 13 cis 15 anti-transformation, resulting
in H? proton gradient across the transmembrane and acti-
vating the ATP production by the cells [9].
Application of Bacteriorhodopsin
The bacteriorhodopsin photocycle has globally attracted
the attention of several researchers since it is optically
active and sensitive. It also has a simple mechanism and
liberates fastest intermediate, transferring the proton across
the membrane rather than the complex chemical method
and also its efficiency to be controlled at any intermediate.
Dye-Sensitized Solar Cells (DSSC)
Dye-sensitized solar cell (DSSC) developed by Graetzel
and his co-workers in 1991 have emerged as a promising
third generation photovoltaic concept in producing energy
against solid state junction devices [20, 22, 34, 59]. The
general working of DSSC is shown in Fig. 2 [58]. DSSC
consists of two electrodes in which one electrode is
transparent for visible light range. Usually nanostructured
TiO2 is used for the purpose of absorbing light range. The
sensitizer i.e. the dye of choice is coated on to the
nanocrystalline surface. Upon photo excitation, dye injects
an electron into the conducting band of oxide to transfer
current to the other electrode. The dye is subsequently
restored by the electrolyte which is usually an organic
Fig. 2 DSSC working model [40]
 Author's personal copy
Photonic Potential of Haloarchaeal Pigment Bacteriorhodopsin for Future...
solvent such as iodide/triiodide couple. With this setup, the
device generates electric power from sunlight without any
permanent chemical transformation [21, 54].
Natural dyes such as fluorescent dyes [60], phthalo-
cyanines [28, 53], porphyrins [71], chlorophylls [96], car-
otenoids [25] and anthocyanins [40] have been used as
sensitizers in DSSC’s rather than the highly efficient
chemically synthesized Ruthenium-based dye-sensitized
cells due to low cost and simple synthetic routes [101].
Bacteriorhodopsin is found to be a notable exception in
respect with the usual biological molecules due to its
functional stability even at high concentration of salt (up to
5 M), temperature (*140 °C) and broad range of pH
(5–11) [16, 38, 77].
Exploration of bacteriorhodopsin as a sensitizer for Dye-
sensitized solar cells has developed modifications in elec-
trodes, metal oxides and processes involved in sensitizing
them on solar cell. The metal oxide anode such as TiO2
nanocrystals [50–52, 72, 91] TiO2 nanotubes [47], bio-
functionalized Au surface [3, 72], quantum dots [72], CdTe
[45], WO3 [43] and UC NP’s [46] has been used either
alone or in combinations with Fluorine-doped Tin Oxide
(FTO) for the cells. Similarly, platinum cathode is used
universally but it also has been replaced by carbon to make
the system cheaper [32]. The photovoltaic efficiency of
bacteriorhodopsin was found to increase on treating bac-
teriorhodopsin with biotin followed by streptavidin medi-
ated adherence using surfactants (such as SDS and Triton
X) and also by TiO2 with TiCl4 [3, 50].
Another study showed the use of QD/Au coated surface
as anode on to which bR was coated as sensitizer. This
transfers electrons to the semiconductors such as TiO2 or
ZnO2 without the use of an electrolyte [72]. Similarly Al-
Aribe et al. [3] reported that biotinylated bacteriorhodopsin
adhered to Au surface through streptavidin can function
even in the absence of electrolyte. The energy conversion
efficiency of bacteriorhodopsin-mediated Dye-sensitized
solar cell has been increased from 0.09% to 0.35% with
under AM 1.5 irradiation, with open circuit of voltages of
0.5 V [32, 51].
Holographic Memory Storage
Holographic memory is an inorganic photorefractive
crystal doped with transition metals which can act as data
storage material by passing coherent optical beams. Such
storage of data by two beams is called as interferometric
recording. The approaching fundamental limits of con-
ventional memory technologies such as magnetic hard
discs, optical discs and semiconductor discs have led to the
development of new generation memories called as holo-
graphic 3D memories which can be used in future com-
puter generations and electronic devices that uses memory
data storage [70]. Several photoconvertible and photo-
switchable fluorescent proteins such as EosFP (in which
Eos stands for God of dawn in Greek mythology and FP
stands for Fluorescent Protein. EosFP is a fluorescent
protein gene taken from Lobophyllia hemprichii and cloned
in Escherichia coli [97]) and IrisFP (in which Iris stands
for God of Rainbow in Greek mythology and FP stands for
Fluorescent protein. IrisFP is a mutant of EosFP [1]) are
used as holographic memories [2]. However, bacteri-
orhodopsin has been studied extensively for its holographic
property due to its controllable intermediates, long-term
stability, resistance to thermal and photochemical degra-
dation, real-time writing in microseconds, allowing mil-
lions of write and erase cycles without degradation, high
spatial resolution and high sensitivity [5, 35].
Bacteriorhodopsin was used naturally, embedded in
gelatin or polyvinyl alcohol films and also experimented as
cubes to be used as holographic memory [15, 33, 87]. The
two photon excitation of bacteriorhodopsin has found to be
optimal for writing and reading data. Data are managed in
any system using as binary codes. When bacteriorhodopsin
is excited by green light it follows core photocycle which
initiates with K state and ends in O state. The second
excitation by red light initiates branched photocycle that
passes from O which is considered binary 0 to P and Q
which is considered as binary 1. During this P state tran-
sition, data are written, while the data are stored and read in
Q state (Fig. 3). By using these binaries, data are stored and
read from bacteriorhodopsin-based holographic memory.
On the other hand, P and Q state are the highly state that
can absorb light in the blue spectrum. Excitation by blue
light erases the stored data from bacteriorhodopsin. In this
way, it acts as perfect holographic material for memory
storage [35, 67, 87].
Fig. 3 Working of bacteriorhodopsin-based memory [68]
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Bacteriorhodopsin used in CDMA, CNN-UM and
POACs was found to be a successful holographic material
for future memory storage [92]. It has also been found that
site directed mutagenesis of bacteriorhodopsin increases its
ability 700 folds when compared to wild type [98]. Initially
data were written in 514 nm and read out in 633 nm [5].
But latter studies showed that it was P state in which data
are written at 450 nm and it is read by passing a laser beam
of 594 nm [11]. Further studies showed that bacteri-
orhodopsin not only allows writing and reading data but
also aids in erasing, refreshing and resetting data.
Refreshing is done at every 1024 bits and resetting is done
by continuous illumination through red light [67].
Optical Switches and Logic Gates
Optical switches will be a next breakthrough in telecom-
munication, transferring several signals at a time through
same channel. Optical switches can effectively replace
electronic switched networks since it avoids optical–elec-
trical–optical conversions and allows switching directly in
optic domain [10]. Several non-linear optical materials
(NLO) have been used for data processing and also as
optical switches. In addition to these organic and inorganic
materials, biological materials are gaining importance in
optical switching [6, 23] and bacteriorhodopsin was found
be an effective biological non-linear optical material for
use in optical switches [19, 65].
Bacteriorhodopsin’s optically active intermediates are
considered as a convenient optical switch in mere future.
When bacteriorhodopsin is excited by green light of 532
[12, 75], 533 [13] or 570 nm [75, 76], it follows the pho-
tocycle with intermediates from K to O. The final inter-
mediate O is an unstable intermediate and reaches back to
the ground state immediately whereas the M state remains
stable for several seconds until it gets saturated. After
saturation, when it absorbs blue light of 640 [81], 635 [75]
or 632.8 nm [13] it gets excited to the higher energy state
and goes back to the original bacteriorhodopsin ground
state. The initial state of excitation from bR is considered
as Switch On state at which signals are transmitted and the
M state is considered as Switch Off state at which signal
transmission is stopped [75].
Several studies on bacteriorhodopsin as optical switch
showed that it can act as reverse image converter and can
transfer images via optical signals. During image trans-
ferring, the pumping beam which excites bR from its
ground state has to be interfered with the pumping beam
that excites M back to bR ground state and the image is
visualized. The pumping beam acts as image background
without which the image cannot be visualized properly
[12, 13]. Another study revealed that, along with the green
and blue light excitation, addition of laser beam at 410 nm
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R. Ashwini et al.
was found to increase efficiency of optical switch in bac-
teriorhodopsin [76, 81]. The refractive index, intensity and
the time required for writing and transferring data have also
been optimized for using bacteriorhodopsin as a perfect
tool for optical switching. In addition to M state, K state
was also considered as notable intermediate to use bacte-
riorhodopsin as optical switch [17, 94].
This phenomenon of exciting bacteriorhodopsin inter-
mediates by pumping laser beam and probe laser beam has
made them to be explored as a promising alternative for
electrical logic gates. Bacteriorhodopsin has been found to
be working significantly as an inverter (NOT gate) and
universal NOR and NAND gates [82]. Another study also
revealed that the fastest intermediates of bacteriorhodopsin
can efficiently perform fastest logic operations. Apart from
its use as NOR and NAND gates, bacteriorhodopsin can
also be used as XOR gate and as ternary logic gates [48].
Biosensors
Fibre optic sensors and biosensors are devices that are used
to detect gases, vapours and temperature in atmosphere and
biological analytes, respectively. Since bacteriorhodopsin
is highly prone to external stimulations, they are considered
as skilful material for its use in fibre optic sensors and
biological sensors [68, 69]. Bacteriorhodopsin can be made
more efficient as biosensor by identifying and genetically
engineering the regions for effective binding of bR, to
target species and also by selecting chemical additives
[29, 80].
A study on bacteriorhodopsin by an interaction with
artificially made streptavidin-coated beads showed that bR
can be used as efficient molecule for biosensing and also
chemical sensing [79]. Another study on using carbon
nanotubes as scaffold along with bacteriorhodopsin as
optical biosensor was found to be used as optical sensor
and also for data storage [69]. Bacteriorhodopsin was also
found to detect ammonia and humidity in nature efficiently
[79]. Combining bacteriorhodopsin with Single electron
transistor showed bR’s use as sensor. These show that
bacteriorhodopsin can act as a perfect material for sensing
[95].
Fig. 4 Microresonator [99]
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Photonic Potential of Haloarchaeal Pigment Bacteriorhodopsin for Future...
Optical Microcavities
Optical microcavities (Fig. 4) also called as optical res-
onators are newly emerged as the most sensitive micro or
nanosystem that can be used as sensors in fibre-optic and
integrated optic formats, used with any other coated pho-
tosensitive material and an externally controlled
microresonator switch [4, 73]. It can be used also in 2D or
3D structures. These optical microresonators will be a
futuristic all in one device which can be used in all fields
with minimal time and also requires only a short laser for
its functioning. Bacteriorhodopsin-coated microcavity can
be implemented with any other photosensitive material-
coated on a microresonator and in any condition in which
the resonance and the coupling can be controlled exter-
nally. This bacteriorhodopsin-mediated high Q microres-
onator offer single molecule detection [73]. They can also
be used in integrated optic photonic crystal micro or
nanocavities and also for reversible computing applications
[74, 93].
Conclusion
Bacteriorhodopsin can be noted as a perfect example for
biotechnology where the biology of the protein is well
explored by technology and now used for the human
welfare. Several genetic engineering approaches such as
genetic modification, recombinant technology and directed
evolution have paved way for the successful modification
and expression of bR protein and its use in several appli-
cations. The review has demonstrated optical and electrical
applications of bacteriorhodopsin in various fields. The
unique ability of bacteriorhodopsin in using solar energy
for proton production will be a significant breakthrough in
development and utilization of bacteriorhodopsin-derived
biological sensitized solar cell (BSSC). Bacteriorhodopsin-
derived BSSC can be considered as an effective alternative
to save the exploitation of fossil fuel and the utilization of
the underutilized renewable and more available solar
energy in many tropical developing countries. As optical
sensors bR can be used in diagnostics of both human dis-
eases and environmental hazards, the exploration of bac-
teriorhodopsin will pursue innovative identifications and
human welfare.
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