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Australia: The Land Where Time Began |
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A Single-Species Ecosystem Deep Within
the Earth Revealed by Environmental Genomics A single complete genome has been sequenced and
assembled from DNA recovered from low-biodiversity fracture water that
was collected at a depth of 2.8 km in a gold mine in South Africa. A
bacterium,
Candidatus Desulforudis
audaxviator, comprises more than 99.9 % of organisms that
inhabit the fluid phase of this particular fracture. It is indicated by
its genome to be a motile, sporulating, sulphate-reducing
chemoautotrophic thermophile that has the ability to fix its own
nitrogen and carbon by using mechanisms shared with archaea.
Candidatus Desulforudis
audaxviator has an independent lifestyle deep within the crust
of the Earth that is well adapted to long-term isolation from the
photosphere and offers an example of a natural ecosystem that apparently
has its biological component encoded entirely with a single genome. Recently a more complete picture of life within, as
well as on the Earth, has been made possible by the extraction and
sequencing of DNA from an environmental sample, the process being called
environmental genomics or metagenomics (Deutchbauer, Chivian & Arkin,
2006; Beja et al., 2000;
Rondon et al., 2000; Venter, 2004; Tyson et al., 2004; Tringe, 2004;
Strous et al., 2006; Rusch et al., 2007). The identification of members of
microbial communities has been made possible by this approach, as well
as characterisation of abilities of the dominant members of the
community, even when isolation of those members has proven to be
intractable. The complexity of natural microbial communities has,
however, hampered the assembly of complete or even near-complete genomes
for a substantial portion of the member species. As well as elevated temperatures and anoxic
conditions within the crust of the Earth at depths of more than 1 km are
fundamentally different from those of the surface and deep ocean
environments. Cell-doubling times of from 100s to 1,000s of years
(Phelps et al., 1994; Jørgensen & D’Hondt, 2006; Lin et
al., 2006), are believed to
result from severe nutrient limitation, and therefore the subsurface
microorganisms might be expected to reduce their reproductive burden and
exhibit genomes that are streamlined as is found in specialists or spend
more time in semi-senescence as they wait for a return of favourable
conditions. As such organisms permit insight into a mode of life that is
independent of the photosphere they are of particular interest. A bacterium, named by Chivian et
al.
Candidatus Desulforudis audaxviator, phylum
Firmicutes, is prominent
in small subunit (SSU of 16S) ribosomal RNA (rRNA) gene clone libraries
(Lin et al., 2006; 11-14) from
almost all fracture fluids sampled to date from deposits greater than
1.5 km in depth throughout the Witwatersrand Basin, which covers 150 km
by 300 km near Johannesburg, South Africa. It has been shown in a
previous geochemical and 16S rRNA study (Lin et
al., 2006) that this bacterium
dominates the indigenous microorganisms found in a fracture zone at 2.8
km below the surface of the land at level 104 in the Mponeng mine
(MP104). Chivian et al. were
surprised with the results of the environmental study reported in this
paper that showed that a single species was present within the fracture
fluid, though it had been discovered (Lin et
al., 2006) that the least
diverse natural free-living microbial community that had been reported
at that time, which exceeded the approximate 80 % dominance by the
methanogenic archaeon IUA5/6 of a shallow subsurface community in Idaho
(Chapelle et al., 2002). Also,
it was found by Chivian et al.
that this organism apparently possessed all the metabolic abilities that
were necessary to live independently. This gene component was consistent
with geochemical and thermodynamic analyses that had been carried out
previously at the ambient temperature of about 60oC and 9.3
pH, which indicated that the energy and nutrients to the system (Lin et
al., 2006) was provided by
radiolytically generated chemical species, with formate and H2
possessing the greatest potential among candidate electron donors, and
the dominant electron-accepting process (Lin et
al., 2006) being sulphate (SO42-).
Discussion According to Chivian et
al. if
D. audaxviator proves to
be the only inhabitant of this habitat, then the complete genetic
complement for the maintenance of the biological component of the
ecosystem must be present, and this would prohibit the extreme reduction
of its genome. At 2.35 Mbp the genome was smaller than the 3 Mbp of its
nearest relative to be sequenced,
Pelotomaculum thermopropionicum.
The genome of
D. audaxviator contained 2,157 predicted coding genes; which is
more than are present in streamlined free-living microorganisms, which
typically have fewer than 2,000 genes (Giovannoni et al., 2005). It was
found in this study that all the genes coding for necessary processes
for life were present in the genome, and this included energy
metabolism, carbon fixation, and nitrogen fixation. The genome has the capability for dissimilarity
sulphate reduction (DSR),
having a gene repertoire like that of other microorganisms (Mussmann et
al., 2005) that can reduce sulphate (SO42-),
which is consistent with the thermodynamic evaluation
(Lin et al., 2006) that
SO42- offers the most energetically favourable
electron acceptor. These genes are present in a set of operons,
including an extra copy of an archaeal-type sulphate adenylyltransferase
(Sat), both appearing to be consequent upon horizontal gene transfer
(HGT). Chivian et al. suggest
it is probable that high potential electrons enter primarily by the
activity of a variety of hydrogenases which act upon H2. Assimilation of carbon may be from a number of
sources depending on local conditions. Transporters of sugar and amino
acid are present in the genome, which suggests that at locations where
there is high biodiversity, heterotrophic sources could be used, which
includes recycling of dead cells. Where biodiversity is low, as occurs
at MP104, carbon from inorganic sources is fixed.
D. audaxviator doesn’t
appear to use the reverse TCA cycle, though it did have all the
machinery of the acetyl-coenzyme A (CoA) synthesis (Wood-Ljungdahl)
pathway (Drake, 2005; Wu et al., 2005), which uses carbon monoxide
dehydrogenase (CODH) to assimilate inorganic carbon. Its anionic species
may accomplish the entry into the cell of CO2 substrate
through its putative carbonate adenosine triphosphate (ATP)-binding
cassette transporter or a putative bicarbonate/Na+ symporter.
Formate and carbon monoxide may serve as alternate carbon sources that
are more direct in other fractures when sufficiently abundant. In the
fracture water the ambient concentration of ammonia ([NH3] +
NH4+] = ~100 μM) (Lin et
al., 2006) appears to be
sufficient for
D. audaxviator (which has
an ammonium transporter as well as a glutamine synthetase) to obtain its
nitrogen from ammonia without needing to resort to a nitrogenase
conversion of N2 to ammonia which is more costly. A
nitrogenase is nonetheless present in the genome with a nifH subunit
that is more similar to archaeal types, which includes high temperature
variants (Mehta & Baross, 2006), than to the nitrogenase of
Desulfotomaculum reducens. Chivian et
al. suggests
D. audaxviator is not
always present with sufficient amounts of ammonia; therefore the
versatility that is provided by nitrogenase that is horizontally
acquired may have contributed substantially to the success of
D. audaxviator in colonising such habitats. There are other
genes that are shared between
D. audaxviator and archaea
that are suggested to possibly confer benefits in extreme environments.
As well as the unusual nitrogenase and sulphate adenylyltransferase,
acquisitions by ancestors of
D. audaxviator include a
second CODH system, cobalamin biosynthesis protein CobN, and genes that
code for gas vesicles. Also, it has 2 clustered regularly interspaced
shot palindromic repeat (CRISPR) regions that are used for viral defence
(Barrangou et al., 2007) and
which occur in the genome with genes that are CRISPR-associated (CAS,
some of which are horizontally shared between
D. audaxviator and
archaea. The possession by
D. audaxviator of all the
amino acid synthesis pathways assists its ability to colonise
independently. The ability to form endospores and the potential for it
to grow in deeper, hotter conditions than provided by MP104 are other
factors that may confer fitness in this environment. It appears that
D. audaxviator is capable
of sensing nutrients in its environment and has flagellar genes to
permit motility along chemical gradients, such as those occurring at the
mineral surfaces of the fracture (Wanger, Onstott & Southam, 2006). A
complete system for oxygen resistance is an ability that
D. audaxviator lacks, which suggests long term isolation from
oxygen. Contained within the MP104 fracture is the simplest
environmental microbial community that has been described to date and
has yielded a single complete genome of a microorganism that wasn’t
cultured with the use of environmental genomics. The ability of
D. audaxviator to reduce
SO42- allows access to the electron acceptor that
is energetically favourable in the fracture zone of the Witwatersrand
basin (Onstott et al., 2006). Also, characteristics inherited by
D. audaxviator, such as
motility, sporulation and carbon fixation, have been complemented by
systems that are frequently present in archaea that have been acquired
horizontally. D. audaxviator has been
enabled by these abilities to colonise the deep subsurface, a process
which differs from surface habitats, permitting more immediate access,
has required fitness throughout the history of colonisation. This
audaxviator (‘bold
traveller’) has revealed a mode of life that is isolated from the
photosphere, which captures all the roles that are necessary for a
life-style that is independent and shows the possibility of encoding the
entire biological component of a simple ecosystem within a single
genome. Chivian, D., E. L. Brodie, E. J. Alm, D. E. Culley,
P. S. Dehal, T. Z. DeSantis, T. M. Gihring, A. Lapidus, L.-H. Lin, S. R.
Lowry, D. P. Moser, P. M. Richardson, G. Southam, G. Wanger, L. M.
Pratt, G. L. Andersen, T. C. Hazen, F. J. Brockman, A. P. Arkin and T.
C. Onstott (2008). "Environmental
Genomics Reveals a Single-Species Ecosystem Deep Within Earth."
Science 322(5899): 275-278. |
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Author: M.H.Monroe Email: admin@austhrutime.com Sources & Further reading |