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Bacterial fermentation and respiration processes are uncoupled in anoxic permeable sediments

Nature Microbiology volume 4, pages 1014–1023 (2019)Cite this article

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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.

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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.

Author information

Author notes

  1. These authors contributed equally: Adam J. Kessler, Ya-Jou Chen, David W. Waite.

Authors and Affiliations

  1. Water Studies Centre, School of Chemistry, Monash University, Melbourne, Victoria, Australia

    Adam J. Kessler, Tess Hutchinson, Sharlynn Koh & Perran L. M. Cook

  2. School of Earth, Atmosphere & Environment, Monash University, Melbourne, Victoria, Australia

    Adam J. Kessler

  3. School of Biological Sciences, Monash University, Melbourne, Victoria, Australia

    Ya-Jou Chen, John Beardall & Chris Greening

  4. Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, Queensland, Australia

    David W. Waite & Philip Hugenholtz

  5. School of Biological Sciences, University of Auckland, Auckland, New Zealand

    David W. Waite

  6. Institute for Marine and Atmospheric Research Utrecht, Utrecht University, Utrecht, The Netherlands

    M. Elena Popa

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Contributions

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

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, YJ., 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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