Bacterial fermentation and respiration processes are uncoupled in anoxic permeable sediments

Adam John Kessler, Ya-Jou Chen, David W. Waite, Tess Frances Hutchinson, Sharlynn Koh, M. Elena Popa, John Beardall, Philip Hugenholtz, Perran Cook, Christopher Andrew Greening

Research output: Contribution to journalArticleResearchpeer-review

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 (H 2 ) accumulates in silicate sand sediments due to decoupling of bacterial fermentation and respiration processes following anoxia. In situ measurements show that H 2 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 H 2 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 H 2 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.

Original languageEnglish
Pages (from-to)1014–1023
Number of pages10
JournalNature Microbiology
Volume4
Issue number6
DOIs
Publication statusPublished - 11 Mar 2019

Cite this

Kessler, Adam John ; Chen, Ya-Jou ; Waite, David W. ; Hutchinson, Tess Frances ; Koh, Sharlynn ; Popa, M. Elena ; Beardall, John ; Hugenholtz, Philip ; Cook, Perran ; Greening, Christopher Andrew. / Bacterial fermentation and respiration processes are uncoupled in anoxic permeable sediments. In: Nature Microbiology. 2019 ; Vol. 4, No. 6. pp. 1014–1023.
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Bacterial fermentation and respiration processes are uncoupled in anoxic permeable sediments. / Kessler, Adam John; Chen, Ya-Jou; Waite, David W.; Hutchinson, Tess Frances; Koh, Sharlynn; Popa, M. Elena; Beardall, John; Hugenholtz, Philip; Cook, Perran; Greening, Christopher Andrew.

In: Nature Microbiology, Vol. 4, No. 6, 11.03.2019, p. 1014–1023.

Research output: Contribution to journalArticleResearchpeer-review

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