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Gammaproteobacterial methanotrophs dominate methanotrophy in aerobic and anaerobic layers of boreal lake waters

Rissanen, Antti J.; Saarenheimo, Jatta; Tiirola, Marja; Peura, Sari; Aalto, Sanni L.; Karvinen, Anu; Nykanen, Hannu

Sammanfattning

Small oxygen-stratified humic lakes of the boreal zone are important sources of methane to the atmosphere. Although stable isotope profiling has indicated that a substantial part of methane is already oxidized in the anaerobic water layers in these lakes, the contributions of aerobic and anaerobic methanotrophs in the process are unknown. We used next-generation sequencing of mcrA and 16S rRNA genes to characterize the microbial communities in the water columns of 2 boreal lakes in Finland, Lake Alinen-Mustajarvi and Lake Mekkojarvi, and complemented this with a shotgun metagenomic analysis from Alinen-Mustajarvi and an analysis of pmoA genes and 16S rRNA, mcrA, and pmoA transcripts from Mekkojarvi. Furthermore, we tested the effect of various electron acceptors and light on methane oxidation (C-13-CH4 labeling) in incubations of water samples collected from the lakes. Aerobic gammaproteobacterial methanotrophs (order Methylococcales) exclusively dominated the methanotrophic community both above and below the oxycline in the lakes. A novel lineage within Methylococcales, Candidatus Methyloumidiphilus alinensis, defined here for the first time, dominated in Alinen-Mustajarvi, while methanotrophs belonging to Methylobacter were more abundant in Mekkojarvi. Light enhanced methane oxidation in the anoxic water layer, while alternative electron acceptors (SO42-, Fe3+, Mn4+, and anthraquinone-2, 6-disulfonate), except for NO3-, suppressed the process. Our results suggest that oxygenic photosynthesis potentially fuels methanotrophy below the aerobic water layers in methane-rich boreal lakes. Furthermore, incubation results, together with the detection of denitrification genes from metagenome-assembled genomes of gammaproteo-bacterial methanotrophs, imply that boreal lake methanotrophs may couple methane oxidation with NOx- reduction in hypoxic conditions.

Nyckelord

Methanotroph; Methane oxidation; Boreal lake; Water column; Shotgun metagenomics; 16S rRNA; mcrA; pmoA

Publicerad i

Aquatic Microbial Ecology
2018, Volym: 81, nummer: 3, sidor: 257-276 Utgivare: INTER-RESEARCH

    UKÄ forskningsämne

    Mikrobiologi

    Publikationens identifierare

    DOI: https://doi.org/10.3354/ame01874

    Permanent länk till denna sida (URI)

    https://res.slu.se/id/publ/95817