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Abstract and Figures

Permeable (sandy) sediments cover half of the continental margin and are major regulators of oceanic carbon cycling. The microbial communities within these highly dynamic sediments frequently shift between oxic and anoxic states, and hence are less stratified than those in cohesive (muddy) sediments. A major question is, therefore, how these communities maintain metabolism during oxic–anoxic transitions. Here, we show that molecular hydrogen (H2) accumulates in silicate sand sediments due to decoupling of bacterial fermentation and respiration processes following anoxia. In situ measurements show that H2 is 250-fold supersaturated in the water column overlying these sediments and has an isotopic composition consistent with fermentative production. Genome-resolved shotgun metagenomic profiling suggests that the sands harbour diverse and specialized microbial communities with a high abundance of [NiFe]-hydrogenase genes. Hydrogenase profiles predict that H2 is primarily produced by facultatively fermentative bacteria, including the dominant gammaproteobacterial family Woeseiaceae, and can be consumed by aerobic respiratory bacteria. Flow-through reactor and slurry experiments consistently demonstrate that H2 is rapidly produced by fermentation following anoxia, immediately consumed by aerobic respiration following reaeration and consumed by sulfate reduction only during prolonged anoxia. Hydrogenotrophic sulfur, nitrate and nitrite reducers were also detected, although contrary to previous hypotheses there was limited capacity for microalgal fermentation. In combination, these experiments confirm that fermentation dominates anoxic carbon mineralization in these permeable sediments and, in contrast to the case in cohesive sediments, is largely uncoupled from anaerobic respiration. Frequent changes in oxygen availability in these sediments may have selected for metabolically flexible bacteria while excluding strict anaerobes.
Permeable sediments harbour diverse H2-metabolizing bacteria a, Community composition of permeable sediments based on 16S reads retrieved from the five metagenomes. Eukaryotes and unassigned reads are not shown. Full taxonomic information is provided in Supplementary Tables 1 and 2. b, Functional capacity of permeable sediments based on normalized short-read count of genes encoding the catalytic subunits of key metabolic enzymes. The dots show read counts for each of the five metagenomes, the centre values show means and the error bars show standard deviations. 16S, 16S rRNA gene; NiFe, [NiFe]-hydrogenases; FeFe, [FeFe]-hydrogenases; atpA, ATP synthase; HCO, haem–copper oxidase genes (coxA, cyoA and ccoN); cydA, cytochrome bd oxidase; acsB, acetyl-CoA synthase; mcrA, methyl-CoM reductase; dsrA and rdsrA, reductive and oxidative clades of dissimilatory sulfite reductase; asrA, anaerobic sulfite reductase; sqr, sulfide–quinone oxidoreductase; soxB, thiosulfate hydrolase; sor, sulfur oxygenase/reductase; narG, dissimilatory nitrate reductase; napA, periplasmic nitrate reductase; nirK, dissimilatory nitrite reductase; nrfA, ammonifying nitrite reductase; haoB, hydroxylamine oxidoreductase; nifH, nitrogenase; rbcL, ribulose 1,5-bisphosphate carboxylase; pfor, pyruvate–ferredoxin oxidoreductase. Full counts are shown in Supplementary Table 4. c, Hydrogenase composition in the five metagenomes. The reads are divided into subtype as per the HydDB classification scheme, namely the oxidative group 1 and 2 [NiFe]-hydrogenases (groups 1a, 1b, 1c, 1d, 1e, 1f, 1h and 2a), bidirectional group 3 [NiFe]-hydrogenases (groups 3b, 3c and 3d), other [NiFe]-hydrogenases and the evolving [FeFe]-hydrogenases. Full counts are shown in Supplementary Tables 4 and 5.
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Fermentative and respiratory processes are uncoupled in permeable sediments a, Measurement of fermentative and respiratory processes in FTRs during oxic–anoxic transitions. The FTRs were made anoxic immediately after sampling at 48 h by purging with argon. O2, H2 and H2S were monitored. The centre values show means and the error bars show standard deviations from three independent FTRs. b, Slurry experiments detecting changes in H2 concentrations in subtidal surface sediments (22 October 2018 samples) during an oxic–anoxic transition at 21 h. For a and b, the dotted line shows the time when the bioreactor and slurry were made anoxic. c, Slurry experiments detecting fermentative H2 production in subtidal surface sediments (20 June 2018 samples). H2 production rates were compared in anoxic slurries that were either untreated or supplemented with 1 mM glucose. The experiment used three independent slurries. d, Relative abundance of Deltaproteobacteria in sediments from c before and after incubation. Community structure was determined by 16S rRNA gene amplicon sequencing and full phylum-level composition is shown in Supplementary Fig. 14. e, Slurry experiments detecting respiratory H2 consumption in subtidal surface sediments (30 April 2018 samples). Anoxic slurries were amended to give starting concentrations of either 16 mM elemental sulfur or 1 mM sodium nitrate. The study used six independent slurries. The levels of sulfide production and N2 production in these slurries are shown in Supplementary Figs. 15 and 16. For b, c and e, the centre values show means and the error bars show standard deviations. For autoclaved controls, values show one control per treatment.
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Articles
https://doi.org/10.1038/s41564-019-0391-z
1Water Studies Centre, School of Chemistry, Monash University, Melbourne, Victoria, Australia. 2School of Earth, Atmosphere & Environment, Monash
University, Melbourne, Victoria, Australia. 3School of Biological Sciences, Monash University, Melbourne, Victoria, Australia. 4Australian Centre for
Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, Queensland, Australia. 5School of Biological Sciences,
University of Auckland, Auckland, New Zealand. 6Institute for Marine and Atmospheric Research Utrecht, Utrecht University, Utrecht, The Netherlands.
7These authors contributed equally: Adam J. Kessler, Ya-Jou Chen, David W. Waite. *e-mail: perran.cook@monash.edu; chris.greening@monash.edu
At least half of the continental margin is covered by permeable
sediments1. Defined as sands and gravels with permeabilities
exceeding 1 × 1012 m2, these sediments are highly dynamic
across space and time, especially in contrast to cohesive sediments
(that is, muds and silts)2. Pore-water advection and physical disrup-
tors (for example, tidal flows and groundwater discharge) drive con-
tinual exchange of dissolved particles, solutes and microorganisms
between these sediments and the water column35. These sediments
therefore shift between being oxic and anoxic over short distances
and timescales, and rarely become as stratified in their redox chem-
istry as cohesive sediments2,68. It was long assumed that sands
are less biogeochemically active than muds, given they harbour
low levels of organic carbon. However, more recent studies have
revealed that sands are highly active: most organic carbon produced
by photoautotrophic and chemolithoautotrophic microorgan-
isms is immediately mineralized by heterotrophs2,9. Cultivation-
independent surveys have consistently shown that sands harbour
phylogenetically and functionally diverse communities of prokary-
otes and microbial eukaryotes1015. Permeable sediments are now
recognized as key systems for regulating global biogeochemical
cycling and supporting oceanic primary production2,16.
The biogeochemical processes and microbial communities that
mediate carbon cycling are likely to differ between coastal perme-
able and cohesive sediments. In coastal muds, carbon mineraliza-
tion pathways are highly stratified, with oxygen availability and
redox potential decreasing with sediment depth. Within anoxic
zones, organic carbon is primarily mineralized by obligately fer-
mentative bacteria (for example, Clostridiales). The dominant end
products, namely organic acids and molecular hydrogen (H2), are
oxidized by respiratory bacteria through redox cascades controlled
by the concentration and energy yield of available oxidants17,18. H2
is generally maintained at low steady-state concentrations (<2 nM)
through tight coupling of fermentative H2 producers (hydrogeno-
gens) and respiratory H2 consumers (hydrogenotrophs), notably
sulfate reducers (for example, Desulfobacterales)17,19,20. Anoxic
sands also maintain high mineralization rates, but the processes and
communities responsible are unresolved7,21. Denitrification and sul-
fate reduction occur in such sediments, but measured rates for these
processes vary and are often too low to account for carbon min-
eralization rates2130. Other processes, namely iron reduction and
methanogenesis, occur at low rates despite the availability of elec-
tron acceptors21. Hence, unlike cohesive sediments, anoxic miner-
alization processes in permeable sediments may not be principally
governed by the availability of electron acceptors.
We have recently produced evidence that hydrogenogenic fer-
mentation may be the dominant carbon mineralization pathway
in anoxic permeable sediments. We used flow-through reactor
(FTR) experiments to simulate shifts from oxic to anoxic condi-
tions. Following the transition to anoxia, carbon mineralization
rates were sustained and H2 concomitantly accumulated to high
levels (>1 µM). In contrast, low rates of respiration of sulfate,
nitrate, nitrite and ferrous iron were observed21. Other recent
Bacterial fermentation and respiration processes
are uncoupled in anoxic permeable sediments
AdamJ.Kessler 1,2,7, Ya-JouChen3,7, DavidW.Waite4,5,7, TessHutchinson1, SharlynnKoh1,
M.ElenaPopa 6, JohnBeardall 3, PhilipHugenholtz 4, PerranL.M.Cook 1* and ChrisGreening 3*
Permeable (sandy) sediments cover half of the continental margin and are major regulators of oceanic carbon cycling. The
microbial communities within these highly dynamic sediments frequently shift between oxic and anoxic states, and hence are
less stratified than those in cohesive (muddy) sediments. A major question is, therefore, how these communities maintain
metabolism during oxic–anoxic transitions. Here, we show that molecular hydrogen (H2) accumulates in silicate sand sedi-
ments due to decoupling of bacterial fermentation and respiration processes following anoxia. In situ measurements show
that H2 is 250-fold supersaturated in the water column overlying these sediments and has an isotopic composition consistent
with fermentative production. Genome-resolved shotgun metagenomic profiling suggests that the sands harbour diverse and
specialized microbial communities with a high abundance of [NiFe]-hydrogenase genes. Hydrogenase profiles predict that H2 is
primarily produced by facultatively fermentative bacteria, including the dominant gammaproteobacterial family Woeseiaceae,
and can be consumed by aerobic respiratory bacteria. Flow-through reactor and slurry experiments consistently demonstrate
that H2 is rapidly produced by fermentation following anoxia, immediately consumed by aerobic respiration following reaera-
tion and consumed by sulfate reduction only during prolonged anoxia. Hydrogenotrophic sulfur, nitrate and nitrite reducers
were also detected, although contrary to previous hypotheses there was limited capacity for microalgal fermentation. In com-
bination, these experiments confirm that fermentation dominates anoxic carbon mineralization in these permeable sediments
and, in contrast to the case in cohesive sediments, is largely uncoupled from anaerobic respiration. Frequent changes in oxygen
availability in these sediments may have selected for metabolically flexible bacteria while excluding strict anaerobes.
NATURE MICROBIOLOGY | VOL 4 | JUNE 2019 | 1014–1023 | www.nature.com/naturemicrobiology
1014
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... Hydrogen metabolism is crucial in energy cycling in marine environments [53]. Gemmatimonadota, except for Group 1, have different types of [NiFe] hydrogenases ( Supplementary Fig. 15) and few [FeFe] hydrogenases (mainly in Group 2) (Supplementary Fig. 16), suggesting hydrogen is coupled to metabolic pathways in these bacteria [54,55]. ...
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Background Gemmatimonadota bacteria are widely distributed in nature, but their metabolic potential and ecological roles in marine environments are poorly understood. Results Here, we obtained 495 metagenome-assembled genomes (MAGs), and associated viruses, from coastal to deep-sea sediments around the world. We used this expanded genomic catalog to compare the protein composition and update the phylogeny of these bacteria. The marine Gemmatimonadota are phylogenetically different from those previously reported from terrestrial environments. Functional analyses of these genomes revealed these marine genotypes are capable of degradation of complex organic carbon, denitrification, sulfate reduction, and oxidizing sulfide and sulfite. Interestingly, there is widespread genetic potential for secondary metabolite biosynthesis across Gemmatimonadota, which may represent an unexplored source of novel natural products. Furthermore, viruses associated with Gemmatimonadota have the potential to “hijack” and manipulate host metabolism, including the assembly of the lipopolysaccharide in their hosts. Conclusions This expanded genomic diversity advances our understanding of these globally distributed bacteria across a variety of ecosystems and reveals genetic distinctions between those in terrestrial and marine communities. -srP_8yBftBuaKffV-GvkTVideo Abstract
... H2 is primarily produced by cyanobacterial nitrogen fixation [18]. High concentrations of H2 are also produced during fermentation in hypoxic sediments, and these high concentrations can diffuse into the overlying water column, especially in coastal waters [19]. As a result, oceans contribute to net atmospheric emissions of these gases [11,12,20]. ...
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