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Pulses of labile carbon cause transient decoupling of fermentation and respiration in permeable sediments.

ABSTRACT: Dihydrogen (H₂) is an important intermediate in anaerobic microbial processes, and concentrations are tightly controlled by thermodynamic limits of consumption and production. However, recent studies reported unusual H₂ accumulation in permeable marine sediments under anoxic conditions, suggesting decoupling of fermentation and sulfate reduction, the dominant respiratory process in anoxic permeable marine sediments. Yet, the extent, prevalence and potential triggers for such H₂ accumulation and decoupling remain unknown. We surveyed H₂ concentrations in situ at different settings of permeable sand and found that H₂ accumulation was only observed during a coral spawning event on the Great Barrier Reef. A flume experiment with organic matter addition to the water column showed a rapid accumulation of hydrogen within the sediment. Laboratory experiments were used to explore the effect of oxygen exposure, physical disturbance and organic matter inputs on H₂ accumulation. Oxygen exposure had little effect on H₂ accumulation in permeable sediments suggesting both fermenters and sulfate reducers survive and rapidly resume activity after exposure to oxygen. Mild physical disturbance mimicking sediment resuspension had little effect on H₂ accumulation; however, vigorous shaking led to a transient accumulation of H₂ and release of dissolved organic carbon suggesting mechanical disturbance and cell destruction led to organic matter release and transient decoupling of fermenters and sulfate reducers. In summary, the highly dynamic nature of permeable sediments and its microbial community allows for rapid but transient decoupling of fermentation and respiration after a C pulse, leading to high H₂ levels in the sediment.

SUBMITTER: Nauer PA

PROVIDER: S-EPMC10952694 | biostudies-literature | 2023 Sep

REPOSITORIES: biostudies-literature

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Pulses of labile carbon cause transient decoupling of fermentation and respiration in permeable sediments.

Nauer Philipp A PA Kessler Adam J AJ Hall Puspitaningsih P Popa Maria Elena ME Ten Hietbrink Sophie S Hutchinson Tess T Wong Wei Wen WW Attard Karl K Glud Ronnie N RN Greening Chris C Cook Perran L M PLM

Limnology and oceanography 20230731 9

Dihydrogen (H<sub>2</sub>) is an important intermediate in anaerobic microbial processes, and concentrations are tightly controlled by thermodynamic limits of consumption and production. However, recent studies reported unusual H<sub>2</sub> accumulation in permeable marine sediments under anoxic conditions, suggesting decoupling of fermentation and sulfate reduction, the dominant respiratory process in anoxic permeable marine sediments. Yet, the extent, prevalence and potential triggers for suc ...[more]

PMID: 38516532

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Project description:Coastal zones act as a sink for riverine and atmospheric nitrogen inputs and thereby buffer the open ocean from the effects of anthropogenic activity. Recently, microbial activity in sandy permeable sediments has been identified as a dominant source of N-loss in coastal zones, namely through denitrification. Some of the highest coastal denitrification rates measured so far occur within the intertidal permeable sediments of the eutrophied Wadden Sea. Still, denitrification alone can often account for only half of the substantial nitrate (NO3-) consumption. Therefore, to investigate alternative NO3- sinks such as dissimilatory nitrate reduction to ammonium (DNRA), intracellular nitrate storage by eukaryotes and isotope equilibration effects we carried out 15NO3- amendment experiments. By considering all of these sinks in combination, we could quantify the fate of the 15NO3- added to the sediment. Denitrification was the dominant nitrate sink (50-75%), while DNRA, which recycles N to the environment accounted for 10-20% of NO3- consumption. Intriguingly, we also observed that between 20 and 40% of 15NO3- added to the incubations entered an intracellular pool of NO3- and was subsequently respired when nitrate became limiting. Eukaryotes were responsible for a large proportion of intracellular nitrate storage, and it could be shown through inhibition experiments that at least a third of the stored nitrate was subsequently also respired by eukaryotes. The environmental significance of the intracellular nitrate pool was confirmed by in situ measurements which revealed that intracellular storage can accumulate nitrate at concentrations six fold higher than the surrounding porewater. This intracellular pool is so far not considered when modeling N-loss from intertidal permeable sediments; however it can act as a reservoir for nitrate during low tide. Consequently, nitrate respiration supported by intracellular nitrate storage can add an additional 20% to previous nitrate reduction estimates in intertidal sediments, further increasing their contribution to N-loss.

Dataset Information

Pulses of labile carbon cause transient decoupling of fermentation and respiration in permeable sediments.

Publications

Pulses of labile carbon cause transient decoupling of fermentation and respiration in permeable sediments.

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