GEOLOGY, March 2011 219
INTRODUCTION
The large estimates of prokaryotic biomass in
the subseafloor biosphere (Whitman et al., 1998)
have been questioned on the basis of insufficient
energy supply (D’Hondt et al., 2002). However,
increases in temperatures during burial may pro-
vide energy by making recalcitrant organic mat-
ter more degradable for prokaryotes (Wellsbury
et al., 1997). In addition, products of thermo-
genic organic matter alteration (>100 °C) can
diffuse upward to feed the base of the deep bio-
sphere (Roussel et al., 2008; Parkes et al., 1994).
However, the suggestion that H
2
from oxidation
of ferrous iron minerals by water at low temper-
atures might be an additional significant energy
source for the deep biosphere (Stevens and
McKinley, 1995) has been challenged (Ander-
son et al., 1998), as mineral:sterile groundwater
incubations produce limited and only transitory
amounts of H
2
. Nevertheless, in deep sediments
the combined effects of prokaryotic activity,
presence of organic matter, and increasing tem-
peratures on mineral:water H
2
generation from a
range of minerals would occur, but this has not
yet been investigated. Here we report the results
of such studies and the direct impact of prokary-
otic activity on thermogenic processes at even
higher temperatures.
METHODS
Natural rock minerals (X-ray diffraction and
inductively coupled plasma-optical emission
spectrometry were used to confirm mineral type
and chemical composition; see Table DR2 in
the GSA Data Repository
1
) were ground (agate
centrifugal ball mill) and added (100 g/L) to
25% Tamar Estuary sediment (St. John’s Lake,
UK) anoxic slurries (Parkes et al., 2007) plus
~1% Guaymas Basin (Jorgensen et al., 1992)
sediment inoculum. These were incubated
(unshaken and in the dark) in 7 mL crimp vials
for thermal gradient experiments (Wellsbury
et al., 1997) or in a high-pressure vessel (Parr
Instrument Company). Headspace gases were
analyzed by a natural gas analyzer (PerkinElmer
Clarus 500) or gas chromatography combustion
isotope ratio mass spectrometer (Varian 3400GC
with ThermoElectron XP mass spectrometer)
for stable carbon isotopes and pore water by ion
chromatography (Dionex ICS-2000). Gas con-
centrations are presented as experiment head-
space (in μmol/L). Sterile control slurries were
triple autoclaved to ensure long-term sterility.
RockEval analysis was conducted as described
by Parkes et al. (2007).
DNA was extracted from slurries using the
FastDNA Spin Kit For Soil (MP Biomedicals)
and stored at -80 °C. Polymerase chain reac-
tion (PCR) was conducted with 16S rRNA
gene primers for Bacteria (27F-907R) and
Archaea (109F-958R or 109F-PARCH519R)
as described by Webster et al. (2006). Products
were reamplified by nested PCR (Bacteria,
357F-518R; Archaea, SAF-PARCH519R) and
analyzed by density gradient gel electrophore-
sis (DGGE) with a 30%–60% denaturant gra-
dient. Archaeal products were also analyzed
on a 30%–80% denaturant gradient due to the
higher guanine-cytosine content of thermophilic
archaeal sequences. Selected DGGE bands were
excised and sequenced using an Applied Bio-
systems 3130xl Genetic Analyzer.
In addition, for some samples (ilmenite and
pyrite slurries incubated at 63–90 °C) replicate
initial PCR products were pooled and cloned
using the pGEM-T Easy Vector System (Pro-
mega). We randomly chose 16S rRNA gene
clones from each library (25) and sequenced
them. Sequences were checked for chimeras
and assigned to phylogenetic groups by com-
parison with the National Center for Biotech-
nology Information database (http://www.ncbi.
nlm.nih.gov/); assignment was confirmed by
phylogenetic tree reconstruction with neighbor-
joining and Jukes and Cantor correction and
Minimum Evolution and LogDet in Molecular
Evolutionary Genetics Analysis Software Ver-
sion 4.0. All sequences have been submitted
to the European Molecular Biology Laboratory
nucleotide sequence database under accession
numbers FR692121–FR692180.
RESULTS AND DISCUSSION
Temperature gradient incubation experiments
were conducted (~0–100 °C, to 130 days) with
a range of minerals and rock, both iron and
non-iron (hematite, labradorite, pyrite, basalt,
ilmenite, hornblende, olivine, magnetite, quartz
sand), added to the sediment slurries, which pro-
vided both a prokaryotic inoculum and a natu-
ral mineral and organic matter matrix. Mineral
additions resulted in considerable H
2
(maximum
1626 μM) and acetate production (maximum
~10,000 μM), which increased with incubation
time and temperature (e.g., basalt, Fig. 1A; 83
days incubation). During incubation some H
2
and acetate were probably also consumed to fuel
the stimulated sulfate removal and CH
4
produc-
tion (maximum 536 μM), as both are important
substrates for sulfate reduction and methanogen-
esis (Parkes et al., 1989; Whiticar et al., 1986).
These reactions were mediated by prokaryotes,
as sterile controls had negligible H
2
and CH
4
for-
mation and sulfate removal, even at temperatures
Geology, March 2011; v. 39; no. 3; p. 219–222; doi: 10.1130/G31598.1; 2 figures; 1 table; Data Repository item 2011086.
© 2011 Geological Society of America. For permission to copy, contact Copyright Permissions, GSA, or editing@geosociety.org.
*E-mail: ParkesRJ@cf.ac.uk.
Prokaryotes stimulate mineral H
2
formation for the deep biosphere
and subsequent thermogenic activity
R. John Parkes
1
*, Cathal D. Linnane
1
, Gordon Webster
1
, Henrik Sass
1
, Andrew J. Weightman
2
, Ed R.C. Hornibrook
3
,
and Brian Horsfield
4
1
School of Earth and Ocean Sciences, Cardiff University, Main Building, Cardiff, Wales CF10 3AT, UK
2
Cardiff School of Biosciences, Cardiff University, Main Building, Cardiff, Wales, CF10 3AT, UK
3
Department of Earth Sciences, University of Bristol, Wills Memorial Building, Bristol, BS8 1RJ, UK
4
GeoForschungsZentrum (GFZ), Telegrafenberg, B425 D-14473 Potsdam, Germany
1
GSA Data Repository item 2011086, Tables
DR1-DR3, Figures DR1-DR8, and references, is
available online at www.geosociety.org/pubs/ft2011
.htm, or on request from editing@geosociety.org or
Documents Secretary, GSA, P.O. Box 9140, Boulder,
CO 80301, USA.
ABSTRACT
The deep subseafloor biosphere contains two-thirds of Earth’s prokaryotic biomass, which
may indicate the presence of novel mechanisms of energy generation as temperatures increase
in the subsurface. In sediment slurry experiments (0–100 °C) with a range of common min-
erals and rocks (including basalt and quartz), there is significant H
2
formation at elevated
temperatures, but only in the presence of prokaryotes. This stimulates further prokaryotic
activity, typical of deep sediments (sulfate reduction, acetogenesis, and CO
2
production, plus
continuing methanogenesis), and Bacteria and Archaea representative of many deep sediment
types develop. H
2
and acetate formation is particularly stimulated above 70 °C. This pro-
karyotic activity even enhances reactions when temperatures are raised to thermogenic levels
(~125–155 °C), including hydrocarbon generation. Mechanochemistry may be important for
mineral H
2
formation; this is enhanced by prokaryotes (biomechanochemistry), and subsur-
face stress and fracturing, which is widespread on Earth.
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