Bacterial fermentation and respiration processes are uncoupled in anoxic permeable sediments

Abstract

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.

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Fig. 1: Biogenic H2 accumulates in permeable sediments in situ.
Fig. 2: Permeable sediments harbour diverse H2-metabolizing bacteria.
Fig. 3: Phylogenetic analysis of hydrogenase genes.
Fig. 4: Fermentative and respiratory processes are uncoupled in permeable sediments.

Data availability

The data that support the findings of this study are available from the corresponding authors upon request. All sequencing data and MAGs have been uploaded to the Sequence Read Archive under BioProject accession number PRJNA515295.

References

  1. 1.

    Hall, S. J. The continental shelf benthic ecosystem: current status, agents for change and future prospects. Environ. Conserv. 29, 350–374 (2002).

    Article  Google Scholar 

  2. 2.

    Huettel, M., Berg, P. & Kostka, J. E. Benthic exchange and biogeochemical cycling in permeable sediments. Annu. Rev. Mar. Sci. 6, 23–51 (2014).

    Article  Google Scholar 

  3. 3.

    Reimers, C. E. et al. In situ measurements of advective solute transport in permeable shelf sands. Cont. Shelf Res. 24, 183–201 (2004).

    Article  Google Scholar 

  4. 4.

    Santos, I. R., Eyre, B. D. & Huettel, M. The driving forces of porewater and groundwater flow in permeable coastal sediments: a review. Estuar. Coast. Shelf Sci. 98, 1–15 (2012).

    Article  Google Scholar 

  5. 5.

    Huettel, M., Ziebis, W. & Forster, S. Flow‐induced uptake of particulate matter in permeable sediments. Limnol. Oceanogr. 41, 309–322 (1996).

    Article  Google Scholar 

  6. 6.

    Glud, R. N. Oxygen dynamics of marine sediments. Mar. Biol. Res. 4, 243–289 (2008).

    Article  Google Scholar 

  7. 7.

    Cook, P. L., Frank, W., Glud, R., Felix, J. & Markus, H. Benthic solute exchange and carbon mineralization in two shallow subtidal sandy sediments: effect of advective pore‐water exchange. Limnol. Oceanogr. 52, 1943–1963 (2007).

    Article  CAS  Google Scholar 

  8. 8.

    Ahmerkamp, S. et al. Regulation of benthic oxygen fluxes in permeable sediments of the coastal ocean. Limnol. Oceanogr. 62, 1935–1954 (2017).

    Article  CAS  Google Scholar 

  9. 9.

    Boudreau, B. P. et al. Permeable marine sediments: overturning an old paradigm. EOS Trans. Am. Geophys. Union 82, 133–136 (2001).

    Google Scholar 

  10. 10.

    Gobet, A. et al. Diversity and dynamics of rare and of resident bacterial populations in coastal sands. ISME J. 6, 542 (2012).

    Article  PubMed  Google Scholar 

  11. 11.

    Böer, S. I., Arnosti, C., Van Beusekom, J. E. E. & Boetius, A. Temporal variations in microbial activities and carbon turnover in subtidal sandy sediments. Biogeosciences 6, 1149–1165 (2009).

    Article  Google Scholar 

  12. 12.

    Dyksma, S. et al. Ubiquitous Gammaproteobacteria dominate dark carbon fixation in coastal sediments. ISME J. 10, 1939 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Hunter, E. M., Mills, H. J. & Kostka, J. E. Microbial community diversity associated with carbon and nitrogen cycling in permeable shelf sediments. Appl. Environ. Microbiol. 72, 5689–5701 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Probandt, D. et al. Permeability shapes bacterial communities in sublittoral surface sediments. Environ. Microbiol. 19, 1584–1599 (2017).

    Article  CAS  PubMed  Google Scholar 

  15. 15.

    Probandt, D., Eickhorst, T., Ellrott, A., Amann, R. & Knittel, K. Microbial life on a sand grain: from bulk sediment to single grains. ISME J. 12, 623–633 (2017).

  16. 16.

    Devol, A. H. Denitrification, anammox, and N2 production in marine sediments. Annu. Rev. Mar. Sci. 7, 403–423 (2015).

    Article  Google Scholar 

  17. 17.

    Hoehler, T. M., Alperin, M. J., Albert, D. B. & Martens, C. S. Thermodynamic control on hydrogen concentrations in anoxic sediments. Geochim. Cosmochim. Acta 62, 1745–1756 (1998).

    Article  CAS  Google Scholar 

  18. 18.

    Canfield, D. E., Thamdrup, B. & Hansen, J. W. The anaerobic degradation of organic matter in Danish coastal sediments: iron reduction, manganese reduction, and sulfate reduction. Geochim. Cosmochim. Acta 57, 3867–3883 (1993).

    Article  CAS  PubMed  Google Scholar 

  19. 19.

    Lovley, D. R. & Goodwin, S. Hydrogen concentrations as an indicator of the predominant terminal electron-accepting reactions in aquatic sediments. Geochim. Cosmochim. Acta 52, 2993–3003 (1988).

    Article  CAS  Google Scholar 

  20. 20.

    Lin, Y.-S. et al. Towards constraining H2 concentration in subseafloor sediment: a proposal for combined analysis by two distinct approaches. Geochim. Cosmochim. Acta 77, 186–201 (2012).

    Article  CAS  Google Scholar 

  21. 21.

    Bourke, M. F. M. F. et al. Metabolism in anoxic permeable sediments is dominated by eukaryotic dark fermentation. Nat. Geosci. 10, 30–35 (2017).

    Article  CAS  PubMed  Google Scholar 

  22. 22.

    Chen, J. et al. Impacts of chemical gradients on microbial community structure. ISME J. 11, 920 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Rao, A. M. F., McCarthy, M. J., Gardner, W. S. & Jahnke, R. A. Respiration and denitrification in permeable continental shelf deposits on the South Atlantic Bight: rates of carbon and nitrogen cycling from sediment column experiments. Cont. Shelf Res. 27, 1801–1819 (2007).

    Article  Google Scholar 

  24. 24.

    Evrard, V., Glud, R. N. & Cook, P. L. M. The kinetics of denitrification in permeable sediments. Biogeochemistry 113, 563–572 (2013).

    Article  CAS  Google Scholar 

  25. 25.

    Eyre, B. D., Santos, I. R. & Maher, D. T. Seasonal, daily and diel N2 effluxes in permeable carbonate sediments. Biogeosciences 10, 2601–2615 (2013).

    Article  CAS  Google Scholar 

  26. 26.

    Kessler, A. J. et al. Quantifying denitrification in rippled permeable sands through combined flume experiments and modeling. Limnol. Oceanogr. 57, 1217–1232 (2012).

    Article  CAS  Google Scholar 

  27. 27.

    Marchant, H. K. et al. Coupled nitrification–denitrification leads to extensive N loss in subtidal permeable sediments. Limnol. Oceanogr. 61, 1033–1048 (2016).

    Article  CAS  Google Scholar 

  28. 28.

    Marchant, H. K. et al. Denitrifying community in coastal sediments performs aerobic and anaerobic respiration simultaneously. ISME J. 11, 1799 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Marchant, H. K. et al. Metabolic specialization of denitrifiers in permeable sediments controls N2O emissions. Environ. Microbiol. 20, 4486–4502 (2018).

  30. 30.

    Dyksma, S., Pjevac, P., Ovanesov, K. & Mussmann, M. Evidence for H2 consumption by uncultured Desulfobacterales in coastal sediments. Environ. Microbiol. 20, 450–461 (2018).

    Article  CAS  PubMed  Google Scholar 

  31. 31.

    Saad, S. et al. Transient exposure to oxygen or nitrate reveals ecophysiology of fermentative and sulfate‐reducing benthic microbial populations. Environ. Microbiol. 19, 4866–4881 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Greening, C., Berney, M., Hards, K., Cook, G. M. & Conrad, R. A soil actinobacterium scavenges atmospheric H2 using two membrane-associated, oxygen-dependent [NiFe] hydrogenases. Proc. Natl Acad. Sci. USA 111, 4257–4261 (2014).

    Article  CAS  PubMed  Google Scholar 

  33. 33.

    Novelli, P. C. et al. Molecular hydrogen in the troposphere: global distribution and budget. J. Geophys. Res. Atmos. 104, 30427–30444 (1999).

    Article  CAS  Google Scholar 

  34. 34.

    Walter, S. et al. The stable isotopic signature of biologically produced molecular hydrogen (H2). Biogeosciences 9, 4115–4123 (2012).

    Article  CAS  Google Scholar 

  35. 35.

    Bottinga, Y. Calculated fractionation factors for carbon and hydrogen isotope exchange in the system calcite-carbon dioxide-graphite-methane-hydrogen-water vapor. Geochim. Cosmochim. Acta 33, 49–64 (1969).

    Article  CAS  Google Scholar 

  36. 36.

    Rahn, T. et al. Extreme deuterium enrichment in stratospheric hydrogen and the global atmospheric budget of H2. Nature 424, 918–921 (2003).

    Article  CAS  PubMed  Google Scholar 

  37. 37.

    Röckmann, T., Rhee, T. S. & Engel, A. Heavy hydrogen in the stratosphere. Atmos. Chem. Phys. 3, 2015–2023 (2003).

    Article  Google Scholar 

  38. 38.

    Röckmann, T. et al. Isotopic composition of H2 from wood burning: dependency on combustion efficiency, moisture content, and δD of local precipitation. J. Geophys. Res. Atmos. 115, D17308 (2010).

  39. 39.

    Gerst, S. & Quay, P. Deuterium component of the global molecular hydrogen cycle. J. Geophys. Res. Atmos. 106, 5021–5031 (2001).

    Article  CAS  Google Scholar 

  40. 40.

    Mußmann, M., Pjevac, P., Krüger, K. & Dyksma, S. Genomic repertoire of the Woeseiaceae/JTB255, cosmopolitan and abundant core members of microbial communities in marine sediments. ISME J. 11, 1276–1281 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Greening, C. et al. Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival. ISME J. 10, 761–777 (2016).

    Article  CAS  PubMed  Google Scholar 

  42. 42.

    Søndergaard, D., Pedersen, C. N. S. & Greening, C. HydDB: a web tool for hydrogenase classification and analysis. Sci. Rep. 6, 34212 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Berney, M., Greening, C., Conrad, R., Jacobs, W. R. & Cook, G. M. An obligately aerobic soil bacterium activates fermentative hydrogen production to survive reductive stress during hypoxia. Proc. Natl Acad. Sci. USA 111, 11479–11484 (2014).

    Article  CAS  PubMed  Google Scholar 

  44. 44.

    Greening, C. & Cook, G. M. Integration of hydrogenase expression and hydrogen sensing in bacterial cell physiology. Curr. Opin. Microbiol. 18, 30–38 (2014).

    Article  CAS  PubMed  Google Scholar 

  45. 45.

    Carere, C. R. et al. Mixotrophy drives niche expansion of verrucomicrobial methanotrophs. ISME J. 11, 2599–2610 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Tengölics, R. et al. Connection between the membrane electron transport system and Hyn hydrogenase in the purple sulfur bacterium, Thiocapsa roseopersicina BBS. BBA Bioenerg. 1837, 1691–1698 (2014).

    Article  CAS  Google Scholar 

  47. 47.

    Kreutzmann, A.-C. & Schulz-Vogt, H. N. Oxidation of molecular hydrogen by a chemolithoautotrophic Beggiatoa strain. Appl. Environ. Microbiol. 82, 2527–2536 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Schwartz, E., Fritsch, J. & Friedrich, B. H 2 -Metabolizing Prokaryotes (Springer, Berlin, 2013).

  49. 49.

    Peters, J. W. et al. [FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation. BBA Mol. Cell Res. 1853, 1350–1369 (2015).

    CAS  Google Scholar 

  50. 50.

    Banat, I. M., Lindström, E. B., Nedwell, D. B. & Balba, M. T. Evidence for coexistence of two distinct functional groups of sulfate-reducing bacteria in salt marsh sediment. Appl. Environ. Microbiol. 42, 985–992 (1981).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Dong, X. et al. Fermentative Spirochaetes mediate necromass recycling in anoxic hydrocarbon-contaminated habitats. ISME J. 12, 2039–2050 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Amin, S. A., Parker, M. S. & Armbrust, E. V. Interactions between diatoms and bacteria. Microbiol. Mol. Biol. Rev. 76, 667–684 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Bullister, J. L., Guinasso, N. L. Jr & Schink, D. R. Dissolved hydrogen, carbon monoxide, and methane at the CEPEX site. J. Geophys. Res. C 87, 2022–2034 (1982).

    Article  CAS  Google Scholar 

  54. 54.

    Lilley, M. D., Baross, J. A. & Gordon, L. I. Dissolved hydrogen and methane in Saanich Inlet, British Columbia. Deep. Sea Res. A 29, 1471–1484 (1982).

    Article  CAS  Google Scholar 

  55. 55.

    Precht, E., Franke, U., Polerecky, L. & Huettel, M. Oxygen dynamics in permeable sediments with wave‐driven pore water exchange. Limnol. Oceanogr. 49, 693–705 (2004).

    Article  CAS  Google Scholar 

  56. 56.

    Kessler, A. J., Glud, R. N., Cardenas, M. B. & Cook, P. L. M. Transport zonation limits coupled nitrification–denitrification in permeable sediments. Environ. Sci. Technol. 47, 13404–13411 (2013).

    Article  CAS  PubMed  Google Scholar 

  57. 57.

    Arnosti, C., Ziervogel, K., Ocampo, L. & Ghobrial, S. Enzyme activities in the water column and in shallow permeable sediments from the northeastern Gulf of Mexico. Estuar. Coast. Shelf Sci. 84, 202–208 (2009).

    Article  CAS  Google Scholar 

  58. 58.

    Grunwald, M. et al. Nutrient dynamics in a back barrier tidal basin of the Southern North Sea: Time-series, model simulations, and budget estimates. J. Sea Res. 64, 199–212 (2010).

    Article  Google Scholar 

  59. 59.

    Kappelmann, L. et al. Polysaccharide utilization loci of North Sea Flavobacteriia as basis for using SusC/D-protein expression for predicting major phytoplankton glycans. ISME J. 13, 76–91 (2019).

  60. 60.

    Du, Z.-J., Wang, Z.-J., Zhao, J.-X. & Chen, G.-J. Woeseia oceani gen. nov., sp. nov., a chemoheterotrophic member of the order Chromatiales, and proposal of Woeseiaceae fam. nov. Int. J. Syst. Evol. Microbiol. 66, 107–112 (2016).

    Article  CAS  PubMed  Google Scholar 

  61. 61.

    Constant, P., Chowdhury, S. P., Pratscher, J. & Conrad, R. Streptomycetes contributing to atmospheric molecular hydrogen soil uptake are widespread and encode a putative high-affinity [NiFe]-hydrogenase. Environ. Microbiol. 12, 821–829 (2010).

    Article  CAS  PubMed  Google Scholar 

  62. 62.

    Myers, M. R. & King, G. M. Isolation and characterization of Acidobacterium ailaaui sp. nov., a novel member of Acidobacteria subdivision 1, from a geothermally heated Hawaiian microbial mat. Int. J. Syst. Evol. Microbiol. 66, 5328–5335 (2016).

    Article  CAS  PubMed  Google Scholar 

  63. 63.

    Canfield, D. E. et al. A cryptic sulfur cycle in oxygen-minimum–zone waters off the Chilean coast. Science 330, 1375–1378 (2010).

    Article  CAS  PubMed  Google Scholar 

  64. 64.

    Novelli, P. C., Crotwell, A. M. & Hall, B. D. Application of gas chromatography with a pulsed discharge helium ionization detector for measurements of molecular hydrogen in the atmosphere. Environ. Sci. Technol. 43, 2431–2436 (2009).

    Article  CAS  PubMed  Google Scholar 

  65. 65.

    Rhee, T. S., Mak, J., Röckmann, T. & Brenninkmeijer, C. A. M. Continuous‐flow isotope analysis of the deuterium/hydrogen ratio in atmospheric hydrogen. Rapid Commun. Mass Spectrom. 18, 299–306 (2004).

    Article  CAS  PubMed  Google Scholar 

  66. 66.

    Chen, Q., Popa, M. E., Batenburg, A. M. & Röckmann, T. Isotopic signatures of production and uptake of H2 by soil. Atmos. Chem. Phys. 15, 13003–13021 (2015).

    Article  CAS  Google Scholar 

  67. 67.

    Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. 68.

    Kang, D. D., Froula, J., Egan, R. & Wang, Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ 3, e1165 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. 69.

    Wu, Y.-W., Tang, Y.-H., Tringe, S. G., Simmons, B. A. & Singer, S. W. MaxBin: an automated binning method to recover individual genomes from metagenomes using an expectation-maximization algorithm. Microbiome 2, 26 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. 70.

    Imelfort, M. et al. GroopM: an automated tool for the recovery of population genomes from related metagenomes. PeerJ 2, e603 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  71. 71.

    Sieber, C. M. K. et al. Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy. Nat. Microbiol. 3, 836–843 (2018).

  72. 72.

    Olm, M. R., Brown, C. T., Brooks, B. & Banfield, J. F. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 11, 2864 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. 73.

    Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. 74.

    Bowers, R. M. et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat. Biotechnol. 35, 725–731 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. 75.

    Lagesen, K. et al. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35, 3100–3108 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. 76.

    Pruesse, E., Peplies, J. & Glöckner, F. O. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823–1829 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. 77.

    Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. 78.

    Parks, D. H. et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 36, 996–1004 (2018).

    CAS  PubMed  Google Scholar 

  79. 79.

    Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. 80.

    Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 119 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. 81.

    Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. 7, e1002195 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. 82.

    Boyd, J. A., Woodcroft, B. J. & Tyson, G. W. GraftM: a tool for scalable, phylogenetically informed classification of genes within metagenomes. Nucleic Acids Res. 46, e59–e59 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. 83.

    Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. 84.

    Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl Acad. Sci. USA 108, 4516–4522 (2011).

    Article  PubMed  Google Scholar 

  85. 85.

    Amir, A. et al. Deblur rapidly resolves single-nucleotide community sequence patterns. mSystems 2, e00191–16 (2017).

    PubMed  PubMed Central  Google Scholar 

  86. 86.

    Callahan, B. J., McMurdie, P. J. & Holmes, S. P. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J. 11, 2639 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  87. 87.

    Anantharaman, K. et al. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat. Commun. 7, 13219 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. 88.

    Anantharaman, K. et al. Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle. ISME J. 1 2, 1715–1728 (2018).

  89. 89.

    Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. 90.

    Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).

  91. 91.

    Fonselius, S., Dyrssen, D. & Yhlen, B. in Methods of Seawater Analysis 3rd edn (eds Grasshoff, K., Kremling, K. & Ehrhardt, M.), 91–100 (Wiley, 2007).

  92. 92.

    Guillard, R. R. L. & Ryther, J. H. Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can. J. Microbiol. 8, 229–239 (1962).

    Article  CAS  PubMed  Google Scholar 

  93. 93.

    Paulin, M. M. et al. Improving Griffith’s protocol for co-extraction of microbial DNA and RNA in adsorptive soils. Soil Biol. Biochem. 63, 37–49 (2013).

    Article  CAS  Google Scholar 

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Acknowledgements

This study was funded by an ARC Discovery Project (DP180101762; awarded to P.L.M.C. and C.G.), an ARC DECRA Fellowship (DE170100310; awarded to C.G.) and an ARC Laureate Fellowship (FL150100038; awarded to P.H.). Y.-J.C. was supported by PhD scholarships from Monash University and the Taiwan Ministry of Education. We thank T. Röckmann for supporting the isotope fractionation work, R. Glud for helpful discussions that led to the conception of this project, and K. Handley and M. Mußmann for their helpful insights. We also acknowledge V. Eate, D. Brehm, L. Stoop, T. Jirapanjawat, S. Davy-Prefumo, S. Bay, R. Pierson and M. Raveggi for providing field and technical support.

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P.L.M.C., C.G. and A.J.K. conceived, designed and supervised this study. Different authors were responsible for in situ measurements (Y.-J.C., A.J.K., S.K., P.L.M.C., T.H. and C.G.), isotope mass spectrometry analysis (M.E.P., A.J.K. and P.L.M.C.), diatom experiments (Y.-J.C., J.B., C.G. and P.L.M.C.), FTR experiments (A.J.K., S.K. and P.L.M.C.), slurry experiments (T.H., Y.-J.C., A.J.K., P.L.M.C. and C.G.), community analysis (Y.-J.C., D.W.W., C.G. and P.H.) and functional gene analysis (D.W.W., C.G., P.H. and Y.-J.C.). C.G., A.J.K., Y.-J.C., P.L.M.C. and D.W.W. analysed the data and wrote the paper with input from all authors.

Corresponding authors

Correspondence to Perran L. M. Cook or Chris Greening.

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Supplementary Information

Legends for Supplementary Datasets and Supplementary Figures 1–19.

Reporting Summary

Supplementary Table 1

Community composition based on 16S rRNA gene reads from metagenome.

Supplementary Table 2

Community composition based on 16S rRNA gene amplicon sequencing.

Supplementary Table 3

Assembly statistics, taxonomic information and key metabolic genes of the 12 MAGs.

Supplementary Table 4

Absolute and normalized read counts of key metabolic genes retrieved from the metagenome.

Supplementary Table 5

Accession number, classification and closest matches of filtered hydrogenase hits.

Supplementary Table 6

Accession number, classification, and closest matches of filtered oxidative and reductive dsrA hits.

Supplementary Table 7

Distribution of [FeFe]-hydrogenase structural and maturation genes in the genomes of the eight sequenced diatom species.

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Kessler, A.J., Chen, Y., Waite, D.W. et al. Bacterial fermentation and respiration processes are uncoupled in anoxic permeable sediments. Nat Microbiol 4, 1014–1023 (2019). https://doi.org/10.1038/s41564-019-0391-z

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