Sulfide Toxicity as Key Control on Anaerobic Oxidation of Methane in Eutrophic Coastal Sediments

Paula Dalcin Martins*, João P.R.C. de Monlevad, Maider J. Echeveste Medrano, Wytze Klaas Lenstra, Anna Julia Wallenius, Martijn Hermans, Caroline P. Slomp, Cornelia Ulrike Welte, Mike S.M. Jetten, Niels A.G.M. van Helmond

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Coastal zones account for 75% of marine methane emissions, despite covering only 15% of the ocean surface area. In these ecosystems, the tight balance between methane production and oxidation in sediments prevents most methane from escaping into seawater. However, anthropogenic activities could disrupt this balance, leading to an increased methane escape from coastal sediments. To quantify and unravel potential mechanisms underlying this disruption, we used a suite of biogeochemical and microbiological analyses to investigate the impact of anthropogenically induced redox shifts on methane cycling in sediments from three sites with contrasting bottom water redox conditions (oxic-hypoxic-euxinic) in the eutrophic Stockholm Archipelago. Our results indicate that the methane production potential increased under hypoxia and euxinia, while anaerobic oxidation of methane was disrupted under euxinia. Experimental, genomic, and biogeochemical data suggest that the virtual disappearance of methane-oxidizing archaea at the euxinic site occurred due to sulfide toxicity. This could explain a near 7-fold increase in the extent of escape of benthic methane at the euxinic site relative to the hypoxic one. In conclusion, these insights reveal how the development of euxinia could disrupt the coastal methane biofilter, potentially leading to increased methane emissions from coastal zones.

Original languageEnglish
Pages (from-to)11421-11435
Number of pages15
JournalEnvironmental Science and Technology
Volume58
Issue number26
DOIs
Publication statusPublished - 2 Jul 2024

Bibliographical note

Publisher Copyright:
© 2024 The Authors. Published by American Chemical Society.

Funding

We thank the captain, the crew of RV Electra, and Christoph Humborg for their assistance with the fieldwork. Arnold van Dijk, Coen Mulder, Helen de Waard, Tom Bastiaan, and Liam Kirwan (Utrecht University) are thanked for analytical assistance. This study was funded by ERC Synergy MARIX 854088 (M.S.M.J., C.P.S., and N.A.G.M.v.H.), NESCC 02001001 (W.K.L., A.J.W., M.S.M.J., and C.P.S.), SIAM 024002002 (M.J.E.M., C.U.W., M.S.M.J.), Havsochvattenmyndigheten DNR 1960-2018 (M.H. and C.P.S.), VI.Veni.222.332 (W.K.L.), and VI.Veni.212.040 (P.D.M.). We are also grateful to Rasmus Rodineliussen for assistance with sampling, Linnea Kop for ideas and code for data visualization, and Mike Lee for creating the DADA2 tutorial (https://astrobiomike.github.io/amplicon/dada2_workflow_ex) from which we derived code for the 16S rRNA gene analyses in this study.

FundersFunder number
European Research Council854088
NESCCSIAM 024002002, 02001001
Havsochvattenmyndigheten DNRVI.Veni.212.040

    Keywords

    • anaerobic oxidation of methane
    • coastal sediments
    • eutrophication
    • euxinia

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