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Reactive oxygen species affect the potential for mineralization processes in permeable intertidal flats.

ABSTRACT: Intertidal permeable sediments are crucial sites of organic matter remineralization. These sediments likely have a large capacity to produce reactive oxygen species (ROS) because of shifting oxic-anoxic interfaces and intense iron-sulfur cycling. Here, we show that high concentrations of the ROS hydrogen peroxide are present in intertidal sediments using microsensors, and chemiluminescent analysis on extracted porewater. We furthermore investigate the effect of ROS on potential rates of microbial degradation processes in intertidal surface sediments after transient oxygenation, using slurries that transitioned from oxic to anoxic conditions. Enzymatic removal of ROS strongly increases rates of aerobic respiration, sulfate reduction and hydrogen accumulation. We conclude that ROS are formed in sediments, and subsequently moderate microbial mineralization process rates. Although sulfate reduction is completely inhibited in the oxic period, it resumes immediately upon anoxia. This study demonstrates the strong effects of ROS and transient oxygenation on the biogeochemistry of intertidal sediments.

SUBMITTER: van Erk MR

PROVIDER: S-EPMC9941506 | biostudies-literature | 2023 Feb

REPOSITORIES: biostudies-literature

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Reactive oxygen species affect the potential for mineralization processes in permeable intertidal flats.

van Erk Marit R MR Bourceau Olivia M OM Moncada Chyrene C Basu Subhajit S Hansel Colleen M CM de Beer Dirk D

Nature communications 20230220 1

Intertidal permeable sediments are crucial sites of organic matter remineralization. These sediments likely have a large capacity to produce reactive oxygen species (ROS) because of shifting oxic-anoxic interfaces and intense iron-sulfur cycling. Here, we show that high concentrations of the ROS hydrogen peroxide are present in intertidal sediments using microsensors, and chemiluminescent analysis on extracted porewater. We furthermore investigate the effect of ROS on potential rates of microbia ...[more]

PMID: 36804536

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Project description:Wounded leaves of Arabidopsis thaliana show transient immunity to Botrytis cinerea, the causal agent of grey mould. Using a fluorescent probe, histological staining and a luminol assay, we now show that reactive oxygen species (ROS), including H(2)O(2) and O(2) (-), are produced within minutes after wounding. ROS are formed in the absence of the enzymes Atrboh D and F and can be prevented by diphenylene iodonium (DPI) or catalase. H(2)O(2) was shown to protect plants upon exogenous application. ROS accumulation and resistance to B. cinerea were abolished when wounded leaves were incubated under dry conditions, an effect that was found to depend on abscisic acid (ABA). Accordingly, ABA biosynthesis mutants (aba2 and aba3) were still fully resistant under dry conditions even without wounding. Under dry conditions, wounded plants contained higher ABA levels and displayed enhanced expression of ABA-dependent and ABA-reporter genes. Mutants impaired in cutin synthesis such as bdg and lacs2.3 are already known to display a high level of resistance to B. cinerea and were found to produce ROS even when leaves were not wounded. An increased permeability of the cuticle and enhanced ROS production were detected in aba2 and aba3 mutants as described for bdg and lacs2.3. Moreover, leaf surfaces treated with cutinase produced ROS and became more protected to B. cinerea. Thus, increased permeability of the cuticle is strongly linked with ROS formation and resistance to B. cinerea. The amount of oxalic acid, an inhibitor of ROS secreted by B. cinerea could be reduced using plants over expressing a fungal oxalate decarboxylase of Trametes versicolor. Infection of such plants resulted in a faster ROS accumulation and resistance to B. cinerea than that observed in untransformed controls, demonstrating the importance of fungal suppression of ROS formation by oxalic acid. Thus, changes in the diffusive properties of the cuticle are linked with the induction ROS and attending innate defenses.

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.

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Reactive oxygen species affect the potential for mineralization processes in permeable intertidal flats.

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Reactive oxygen species affect the potential for mineralization processes in permeable intertidal flats.

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