Arid ecosystem: Future option for carbon sinks using microbial community intelligence

Abstract

Desert, comprising one-third of the Earth's surface, was a synonym for 'no life' as it supports very less or no life due to nutritional stress and extreme weather. Microbial autotrophic biochemistry is the principal source of carbon in arid environment, but understanding of these processes in arid ecosystem is limited. Emerging molecular tools have identified associations of phototrophic and chemolithoautotrophic communities often termed as 'biological soil crust' or 'microbiotic crust'. They are the sole sources of carbon and nitrogen, collectively providing soil stability to support vegetation. Here the curiosity arises, whether this phenomenon could be exploited in deserts for carbon sink using microbial community intelligence. By following the precipitation event under regulated nutrient supply that promotes the soil microbial intelligence for autotrophy would enrich soil carbon and nitrogen which in turn support plant growth in desert. Additionally, bioaugmentation of rhizobacteria could enhance the process. This will enable us to refine and formulate our strategies to exploit CO2-fixing microorganisms in such niches vis-à-vis supporting the carbon sink using microbial community intelligence.

Full text

GENERAL ARTICLES
CURRENT SCIENCE, VOL. 106 , NO . 10 , 25 MAY 2014 1357
Leena Agarwa l, Asifa Q ureshi, Atya Kapley a nd Hema nt J. Puro
hit are
in the Environmental Genomics Division, CSIR -Nationa l Environ-
mental Engineeri ng Research In
stitu te, Nehru Ma rg, Nagpur 440 020 ,
India ; Vipin Chandra Kalia is in Microbial Biotechnology and Geno-
mics Division, CSIR-
Institute of Ge nomi cs and Integrative Biology,
Delhi Uni versi ty Campus, Ma ll Road, Delhi 110
007, India; R. N.
Singh is in the CSIR -Nationa l Geoph ysical Research In stitute, Hydera -
bad 5 00 007, India.
*For corre spondence. (e -mail: hj_purohit@neeri.res.in)
Arid ecosystem: future option for carbon sinks
using microbial community intelligence
Leena Agarwal, Asifa Qureshi, Vipin Chandra Kalia, Atya Kapley, Hemant J. Purohit* and
R. N. Singh
Desert, comprising one-third of the Earth’s surface, was a synonym for ‘no life’ as it supports very
less or no life due to nutritional stress and extreme weather. Microbial autotrophic biochemistry is
the principal source of carbon in arid environment, but understanding of these processes in arid
ecosystem is limited. Emerging molecular tools have identified associations of phototrophic and
chemolithoautotrophic communities often termed as ‘biological soil crust’ or ‘microbiotic crust’.
They are the sole sources of carbon and nitrogen, collectively providing soil stability to support
vegetation. Here the curiosity arises, whether this phenomenon could be exploited in deserts for
carbon sink using microbial community intelligence. By following the precipitation event under
regulated nutrient supply that promotes the soil microbial intelligence for autotrophy would enrich
soil carbon and nitrogen which in turn support plant growth in desert. Additionally, bioaugmenta-
tion of rhizobacteria could enhance the process. This will enable us to refine and formulate our
strategies to exploit CO2-fixing microorganisms in such niches vis-à-vis supporting the carbon sink
using microbial community intelligence.
Keywords: Arid ecosystem, biological soil crust, carbon sequestration, metagenome, microbial intelligence,
CLIMAT E change is a global phenomenon shown to be
related with the increase of CO2 levels, which have been
reported up to 399 ppm in May 2013 (Mauna Loa Obser-
vatoy, Hawaii). It is attracting the attention of the scien-
tific community and correlations have shown that the
increasing levels of CO2 ar e directly associated with cli-
mate change effects1. There is a need to identify CO2 sink
options that could address the issue of ever increasing
atmosphere CO2 at global level. Is there an answer for
this issue by increasing carbon sequestration capacity
through degraded land or deserts? Deserts are a major
portion of the terrestrial ecosystem, mostly considered as
barren or without life due to extreme environment with
unbalanced or compromised nutritional status2. Soils after
a precipitation event, show subsurface soil heterotrophic
activity. Deserts are oligotrophic in nature, here microbial
autotrophy drives CO2 fixation and significantly contri-
butes to associated biomass at comparatively low levels
than plants. Microbial CO2 assimilation involves photo-
trophs and chemolith oautotrophs, viz. iron oxidizing,
sulfur oxidizing, ammonia oxidizing and nitrifying
bacteria. They are the key source of soil carbon in case of
arid soil, principally sequestering CO2 by Calvin–
Benson–Bassham (CBB) cycle. Beyond the CBB cycle,
there are five other options, viz. reductive acetyl CoA
pathway (rACoA), reductive tricarboxylic acid (rTCA)
cycle, 3-hydroxypropionate bicycle (3-HP), hydroxy-
propionate/hydroxybutyrate cycle and dicarboxylate-
hydroxybutyrate cycle3 available for the microbial com-
munity to assimilate CO2.
Arid ecosystem: a future option for carbon sinks
Increasing the capacity of desert and degraded land could
be the next option to sequester carbon. Long-term storage
of carbon in basic resources of an ecosystem is called
carbon sequestration. The two major natural C sink
options are ocean and terrestrial ecosystem, of which
oceans can bring maximum carbon sinks since they make
71% of the Earth’s surface. Terrestrial storage includes
abstraction of CO2 in both forest area as well as non-
forest area like desert.
Forest
Forest ecosystem is a reservoir for more than 70% of th e
terrestrial and soil organic carbon4,5. Although forest

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CURRENT SCIENCE, VOL. 106 , NO . 10 , 25 MAY 2014 1358
floors accumulate C quickly, but being labile and
available for a limited period, they are not considered as
long-term solutions6. The potential of enhancing C
sequestration rates of existing forests is not encouraging
and provides a rather conflicting set of evidences5.
Forest soils act as potential C sinks, but only a small pro-
portion of plant-derived C becomes stabilized on the
mineral soil7. Afforestation cannot help achieve large
amounts of C sequestration than is possible by fertiliza-
tion of forest, particularly on nutrient-limited sites like
deserts8.
Desert
Desert covers substantial part of terrestrial ecosystem and
have been shown to absorb around 100 g C/m2/yr (ref. 9).
The net CO2 exchange data using eddy covariance
method in Mojave and Gurbantunggut desert (China)
suggests that deserts act as ‘large carbon sink’9–11 . How-
ever, the absolute size of desert makes it significantly
more important for CO2 sinks. Th e carbon flux between
the desert soil and the atmosph ere is smaller in compari-
son to that which takes place between organically rich
soils. The carbon storage capacities of ecosystems with
low organic content, viz. arid and semiarid regions are
not well studied10.
Microbial community knowledge in deserts
Microbial autotrophs are closely associated with life on
Earth and are distributed amongst all the three domains of
life3. Microbial activity in desert soils is principally gov-
erned by soil carbon comparable to nitrogen1 2. The total
organic carbon of desert ecosystem has been r eported
between 560 and 765 g/g soil in Atacama Desert,
whereas it is 7000 and 1700 g/g soil in Mojave and Sa-
hara deserts respectively13. The same argument strongly
proposes to make the desert a better sink for CO2, since a
lot of autotrophic and oligotrophic bacteria are found to
exist in low organics1 4,15. Th ough deprived of green
cover, desert provides shelter to photoautotrophic and
chemolithoautotrophic microbial communities that access
carbon from the atmosphere16 ,17. The unvegetated soil of
Atacama Desert supports many chemolithotrophic genera
which were phylogenetically affiliated to previously
reported non-phototrophic genera, viz. Nitrospira, and
gamma-proteobacteria1 8 that obtain energy for CO2 fixa-
tion by the oxidation of nitrite, car bon monoxide, iron or
sulfur. Microbial community in arid soil was also found
to be rich in archaeal members affiliated to Crenar-
chaea19 ,20, an indicator group for the operation of 3-
hydroxypropionate pathway21 and primordial life-forms.
Freeman et al.22 report the abundance of photoautotrophic
microbial community in barren soil due to light-driven
CO2 influx. This CO2 influx resulted in the abundance of
photoautotrophic microbial communities on surface soil
compared to deeper soil. Yuan et al.16 determined the
diversity and abundan ce of CO2-fixing bacteria and algae
by clone library, T-RFLP and qPCR of rubisco gene. The
14C–CO2 incubation studies revealed the incorporation of
14C into the soil microbial biomass accounting up to 4%
of the total CO2 fixed by terrestrial ecosystems per year.
Yousuf et al.32 studied the diversity and abundance of
chemolithotrophic bacteria in coastal saline soil of Guja-
rat, targeting both phylogenetic and functional gene (cbb)
marker.
Biological soil crust (BSC) is a vital C sink in the
desert due to the photosynthetic community which is
decisive for carbon cycling either by oxygenic or anoxy-
genic phototrophy23. The association of cyanobacteria,
lichens and mosses forms the principal component of
BSC11. It sequesters 6% of total carbon sequestered by
terrestrial vegetation and fixes about 40% of biological
nitrogen24. The crust significantly contributes soil carbon,
nitrogen, nutrients and reduces soil erosion, thereby im-
proving soil fertility25 –27. The carbon fixation capacities
of BSC increase from 0.4 to 3.3 g C m–2 yr–1 with its
maturity as a result of increase in crust cover, its thick-
ness, chlorophyll content, organic carbon and nitrogen
content28. During the process of BSC succession, the
cyanobacteria–algae-dominated crust shifts toward
lichen–moss dominance. This shift causes increase in the
amount of carbon sequestered from 11.36 to
26.75 g C m−2 yr−1, possibly due to more surface area and
water-holding capacity of the later successions2 9. The
average rate of nitrogen fixed by BSC in different deserts
accounts for 70 mol m–2 h–1 of nitrogen26. Establishment
of BSC in desert supports plantation better compared
to bare soil, but principally depends on the succession
stage of BSC30 . The promising route for restoration
of degraded land is the establishment of BSC on dry land
that results in an increase in soil organic carbon and
nitrogen28.
In desert, microbial community intelligence for
autotrophy is possessed by members of cyanobacteria,
chloroflexi, bacteroidetes/chlorobi and some pr oteobacte-
ria16 ,31,3 2 along with group chemolithotroph affiliated with
purple sulfur, purple n on-sulfur, green sulfur and
green non-sulfur bacteria. Besides the knowledge of aut o-
trophy, understanding of nitrogen fixation by Azospiril-
lum sp., Rhizobium sp. and Pseudomonas sp. is also
present in arid ecosystem33 . It is proposed that if the in-
telligence for carbon, nitrogen and nutrient cycle
possessed by microbial components of BSC could be
harnessed for increasing the soil nutritional status, then
a system with enhanced efficiency of carbon sequestra-
tion could be designed (Figure 1). So the key to account
desert as a carbon sink should be to consider together
the effect of precipitation event, temperatur e, soil
process and microbial activity to support plant producti-
vity3 4.

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CURRENT SCIENCE, VOL. 106 , NO . 10 , 25 MAY 2014 1359
Figure 1 . Conceptual strategy for ca rbon sequestrati on i n a rid ecosystem using micr obial
commu nity intellige nce: The ide ntifi cat ion of critical time-fra me for precipita tion event and its
exploitation in favou r of development of eff ective biological crust (BSC) has been hypot hesized.
It inclu des defining the stra tegy for development of micr obial communi ty intelligence for carbon
seque stra tion by identification of co mmunity structu re or by appl ying required micr obia l me m-
bers to co mplet e the desired community structure. This could be fu rther assisted by supplementa-
tion of nut rients responsible for synthesis and sta bilization of BSC under the selected climatic
conditions o f temperatu re and humidity. E stablish ment of such microbia l knowledge woul d u lti-
mately su pport in an increase of soil carbon, nitrogen and its fert ilit y. The progr ammed scena rio
would su pport the pool of nutrients t o heterotrophs and plant to fu rther participate in sequestra-
tion process. Conversel y, under non -opti mal climatic conditions of increa sed temperature and
humidity, deep subsurface het erotrophic microbia l activity enhances, which further r educes soil
carbon resulti ng in land degradation.
Molecular tools aiding mining the microbial
community intelligence
Microbial community intelligence is the overall knowl-
edge that a community has in order to adapt to the present
state of stress or environmental conditions by altruistic or
cooperative behaviour. Such example of microbial com-
munity intelligence is found in soil ecosystems. Soil is a
complex dynamic biological system that harbours almost
4000 different bacterial species/g soil, but almost 99%
could not be isolated due to unavailability of th e knowl-
edge about their culturing conditions. This 99% could be
accessed by metagenomics, which provides the knowl-
edge of total community fr om any environmental sample.
It is an efficient technique to address the functional capa-
city of uncultivable microorganisms from any niche3 5.
The advancement of soil metagenomics provides a new
perspective for understanding the role of soil microorgan-
isms and to unearth the hidden functional knowledge
associated with the microbial community, even with the
extreme environment like Atacama Desert2, 36,3 7. Earlier
studies on the microbiology of desert soil have proved
that life in the desert was not explored due to limitations
of culturing techniques. The emerging molecular tools
could be applied for the analysis of microbial wealth
while considering the possible limitations16,3 8–40. Im-
provement in DNA extraction efficiency and high sam-
pling frequency is required to explore th e huge microbial
world, inhabiting the soil39; and this could be further
improved using high throughput approaches such as
microarray41 ,42.
Next-generation sequencing techniques ha ve opened a
wide spectrum of taxonomic and fun ctional aspects of
microbial community43. Identification of many uncultur-
able microbes and archaeal members of group Thermo-
protei in Sonaron Desert soil highlights the magnitude of

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CURRENT SCIENCE, VOL. 106 , NO . 10 , 25 MAY 2014 1360
pyrosequencing12. Of late, metatranscriptomics and
metaproteomics have been evolved to access the fun c-
tional knowledge from such a vast metagenome data43.
The functional annotation of such datasets is based on
homology search against the publicly available database
and requir es knowledge of bioinformatics tools and com-
putational storage space4 4. Recent advances in the field of
microbiology, biotechn ology, molecular biology and bio-
informatics opened up the way to identify novel genes
and for impr oving the quality of target output45. There are
many microbes reported for CO2 fixation through un-
known pathways, pointing towards the scope of finding
new genes, enzymes and path ways underlying CO2 fixa-
tion4 6. Developing such resource and database enlightens
the area of research and the understanding of new genes
and pathways.
The biochemistry of CO2 fixation by microbial com-
munities in extreme environments could be understood by
exploring the genetic information carried by the metage-
nomes. Metagenome analysis suggests colonization of
various phototrophs and lithotrophs in Arctic, Antarctic
and Atacama Desert2,25, 37,47 . This was evidenced by the
identification of rubisco gene in the metagenome3 2,48.
Marker genes for CO2 fixation were observed in metage-
nome isolated from various niches, but little is known
about the CO2 fixing gene other than rubisco. Hence
there is still scope for finding n ew genes that can fix CO2
in arid ecosystems. In addition to the phylogenetic analy-
sis, knowledge of functional gene diversity is more
important to study climate change impact in desert and
provide insight into the role of desert as a CO2 sink.
Community response to climatic drivers
The Southeast Asian region is observing the shift in the
geographical distribution of rainfall pattern. The tr end
shows that it is moving towards the western plains and
feeding the precipitation to deserts and also moving to-
wards the Middle East49. Desert is highly responsive to
climatic variability since bacteria-inhabiting deserts are
under various stresses, viz. temperature, salinity, precipi-
tation, carbon, etc. The bacteria that survive in desert
cope with these str esses. The presence of carbon dioxide-
fixing bacteria in deserts counteracts the carbon stress by
fixing the inorganic carbon and hence increases soil
organics and supports other lifeforms. The member of
genus Azospirillum, a known plant gr owth promoting
bacteria (PGPB), exerts its growth-promoting effect on
plants under various desert stresses of salinity50,
drought51 and extreme pH52. The soil microbial commu-
nity alters with change in precipitation, atmospheric CO2
concentration and temperature53,5 4. In arid ecosystems,
precipitation is the key dr iver controlling carbon, nitro-
gen and nutrients due to change in microbial response55.
The nature of episodic precipitation events in arid ecosys-
tem increases carbon influx due to increased surface
microbial autotrophic activity. The soil of Kalahari (Bot-
swana) Desert harbours cyanobacteria, which fix atmo-
spheric CO2 to add significant quantity of organic
matter56. The gains and losses of CO2 through the sands
of Kalahari Desert after light rainfall are the same as
grassland soil, but after the heavy rainfall, large amount
of CO2 is released due to increased degradation of
organic matter by heterotrophic bacteria, which masks the
activity of cyanobacteria. The heterotrophic microbial
respiration operates at a very low level in the desert eco-
system and for short durations, particularly after rains,
when the availability of nutrients enables CO2 efflux55. In
response to the increased precipitation in desert soil, the
rate of carbon efflux is observed in the range 65.6–
339.2 mg C m2 h–1 compared to 2.8–14.8 mg C m2 h–1 in dry
soil56. CO2 efflux increases with an increase in soil tem-
perature due to more heterotrophic microbial activity57. As
increase in soil temperature limits moisture and results in
reduced CO2 fixation capacity of desert due to declined
phototrophic activity. Here the microbial intelligence and
natural selection favours the temperature-tolerating photo-
trophic members in order to provide soil stability58.
Another climatic driver is atmospheric CO2 concentra-
tion, which is ever-increasing since 1988. Elevated CO2
concentration causes an increase in soil carbon sequestra-
tion due to increased plant productivity59. The soil en-
zyme activity alters in response to elevated CO2 that
affects the quantity and quality of soil organic matter and
microbial processes60 . Microbial response to such an ele-
vated CO2 was studied in different ecosystems, but the
observation suggests the need for more extensive analysis
to reveal the microbial r esponse to these changes6 1. An
integrated approach of pyrosequencing and GeoChip has
suggested that the functional structure of soil community
alters under elevated CO2 (ref. 42). There was an in-
creased abundance of genes responsible for carbon fixa-
tion, nitrogen fixation and phosphorus release under
elevated CO2 (ref. 42). A variety of carbon sources and
their metabolites support the n etwork of different
genomes, which collectively decide the way a biological
process evolves under the stress conditions prevailing in
such a system62.
Instances of microbial community intelligence
exploitation
Increasing the capacity of desert and degraded lands
could be the option to sequester car bon vis-à-vis CO2
mitigation. Integrating various approaches of car bon
sequestration and energy generation, exploiting microbial
intelligence could serve as a better option in the near
future. One such paradigm is a Sahara forest project,
which aims at integrating differ ent technologies where
processes feed each other and provide environmental as

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CURRENT SCIENCE, VOL. 106 , NO . 10 , 25 MAY 2014 1361
well as commercial benefits. This serves turning an arid
land into green oasis63. Another project ‘Biodesert pro-
gram’ enables unearthing of microbial resources in deserts,
which serve as a kn owledge pool to develop approaches
to mitigate climate change. Carbon cycling is one of the
thrust research areas of th e Genomic Science Program
funded by US Department of Energy (DOE) (http://geno-
micscience.energy.gov/). It is aimed at developing biose-
questration strategies for ocean and terrestrial ecosystem.
The DOE Joint Genome Institute has generated genome
sequences of many microbes and plants, which provide
knowledge of microbial/microbial community intelli-
gence. Genomic science researchers are developing
advanced methods to translate microbial intelligence into
an understanding of function to provide insights into
plant–microbe and microbe–microbe interactions that
increase carbon fixation in soils. Synthetic biology has
come up to explore microbial intelligence of stress sur-
vival for smart assembly of genome ‘parts’ to find key
solutions to carbon sequestration and climate change64 .
Such resources fulfil the DOE mission of synthesizing a
microbial system that was otherwise unculturable, to im-
prove carbon fixation capacities in soil and sediments.
Application of bioaugmentation strategy could also en-
hance the process of car bon fixation in arid systems.
Rhizospheric plant–microbe interaction serves as one of
the options to enhance carbon sequestration65. It enhances
nutrient uptake capacity of the plant due to increase in
surface area of roots, nitrogen and phosphorus availabil-
ity. Researches targeting the development of microbial
consortia in volving microbial members responsible for
nitrogen fixation, phosphorus solubilization, siderophore
production, phytohormone synthesis, biological crust
formation that would finally support plant growth in
symbiotic or non-symbiotic manner could help develop
microbe-based strategies for carbon sequestration. Resto-
ration of Sonoran Desert has been demonstrated by bio-
augmentation of PGPB formulation consisting of
Azospirillum brasilense and Bacillus pumilus, along with
arbuscular mycorrhizal fungi and compost66 ,67. However,
the plant growth response depends on the varying degrees
of bio-formulation application. A bio-formulation of
immobilized A. brasilense and microalgae Chlorella
sorokiniana was also used to increase the organic content
of desert soil to support sorghum plantation68 . By inte-
grating the knowledge-based research of application of
PGPB with the development of application-based techno-
logy would promote desert farming. This basically relies
on the detailed knowledge in terms of soil characteristics,
climatic factors and micr obial intelligence present in that
niche that has to be reclaimed. This enables us to under-
stand the missing knowledge that could be offered exter-
nally favouring the natural entropy. The microbial
community reserves of an arid ecosystem may offer insight
into finding new solutions to global environmental issues
and adding up to the existing natural capacities.
Conclusion
Deserts can be equated as dry ‘oceans’, but the vision of
converting deserts into green oasis could address the
problem of climate change. A biological appr oach for
carbon captur e through the microbial pr ocess in deserts is
the establishment of BSC. Researches targeting to iden-
tify the factors promoting BSC formation and their effect
on plant establishment offer a way to develop desert as a
carbon sink. Additionally, bioaugmentation of PGPB
could also address soil fertility. The genetic potential to
fix CO2 is widespread in soils; their capacity to fix CO2
has yet to be fully investigated. The knowledge of key
functions related to climatic drivers, their effect and
microbial responses within the desert ecosystem would be
useful for developing better solutions for carbon seques-
tration in the desert.
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ACKNOWLED GEMENT S. L.A. tha nks the Council of Scienti fic and
Industria l Research (CSI R), New Delhi for the award of Senior Re-
search Fellowship. R.N.S. is grateful to INSA for the award of S enior
Scientist Scheme. We thank the Director s of CSI R-Na tional Environ-
mental Engine ering Resear ch Institute, Nagpur and CSIR-Inst itute of
Genomi cs and Integrative Biology, Delhi, CSIR-WU M (ESC010 8) for
providing the necessary funds and fa cilities.
Receiv ed 2 Ja nuar y 2014; revised acce pted 21 Mar ch 20 14