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Research article - Peer-reviewed, 2023

Organic matter lability modifies the vertical structure of methane-related microbial communities in lake sediments

Rissanen, Antti J.; Jilbert, Tom; Simojoki, Asko; Mangayil, Rahul; Aalto, Sanni L.; Khanongnuch, Ramita; Peura, Sari; Jantti, Helena

Abstract

Eutrophication increases the input of labile, algae-derived, organic matter (OM) into lake sediments. This potentially increases methane (CH4) emissions from sediment to water through increased methane production rates and decreased methane oxidation efficiency in sediments. However, the effect of OM lability on the structure of methane oxidizing (methanotrophic) and methane producing (methanogenic) microbial communities in lake sediments is still understudied. We studied the vertical profiles of the sediment and porewater geochemistry and the microbial communities (16S rRNA gene amplicon sequencing) at five profundal stations of an oligo-mesotrophic, boreal lake (Lake Paajarvi, Finland), varying in surface sediment OM sources (assessed via sediment C:N ratio). Porewater profiles of methane, dissolved inorganic carbon (DIC), acetate, iron, and sulfur suggested that sites with more autochthonous OM showed higher overall OM lability, which increased remineralization rates, leading to increased electron acceptor (EA) consumption and methane emissions from sediment to water. When OM lability increased, the abundance of anaerobic nitrite-reducing methanotrophs (Candidatus Methylomirabilis) relative to aerobic methanotrophs (Methylococcales) in the methane oxidation layer of sediment surface decreased, suggesting that Methylococcales were more competitive than Ca. Methylomirabilis under decreasing redox conditions and increasing methane availability due to their more diverse metabolism (fermentation and anaerobic respiration) and lower affinity for methane. Furthermore, when OM lability increased, the abundance of methanotrophic community in the sediment surface layer, especially Ca. Methylomirabilis, relative to the methanogenic community decreased. We conclude that increasing input of labile OM, subsequently affecting the redox zonation of sediments, significantly modifies the methane producing and consuming microbial community of lake sediments.IMPORTANCE Lakes are important natural emitters of the greenhouse gas methane (CH4). It has been shown that eutrophication, via increasing the input of labile organic matter (OM) into lake sediments and subsequently affecting the redox conditions, increases methane emissions from lake sediments through increased sediment methane production rates and decreased methane oxidation efficiency. However, the effect of organic matter lability on the structure of the methane-related microbial communities of lake sediments is not known. In this study, we show that, besides the activity, also the structure of lake sediment methane producing and consuming microbial community is significantly affected by changes in the sediment organic matter lability.

Keywords

greenhouse gas; freshwater; methanotroph; methanogen; 16S rRNA gene; eutrophication

Published in

Microbiology Spectrum
2023, Volume: 11, number: 5, article number: e01955-23
Publisher: AMER SOC MICROBIOLOGY

    UKÄ Subject classification

    Geochemistry
    Microbiology

    Publication identifier

    DOI: https://doi.org/10.1128/spectrum.01955-23

    Permanent link to this page (URI)

    https://res.slu.se/id/publ/126599