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Aquatic Microbial Ecology


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AME 81:257-276 (2018)  -  DOI: https://doi.org/10.3354/ame01874

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

Antti J. Rissanen1,2,*, Jatta Saarenheimo2, Marja Tiirola2, Sari Peura3, Sanni L. Aalto2, Anu Karvinen4, Hannu Nykänen2,5

1Tampere University of Technology, Laboratory of Chemistry and Bioengineering, PO Box 527, 33101 Tampere, Finland
2University of Jyväskylä, Department of Biological and Environmental Science, PO Box 35, 40014 Jyväskylä, Finland
3Swedish University of Agricultural Sciences, Department of Forest Mycology and Plant Pathology, Science for Life Laboratory, PO Box 7026, 75007 Uppsala, Sweden
4University of Eastern Finland, Department of Environmental and Biological Sciences, PO Box 111, 80101 Joensuu, Finland
5University of Eastern Finland, Department of Environmental and Biological Sciences, PO Box 1627, 70211 Kuopio, Finland
*Corresponding author:

ABSTRACT: 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-Mustajärvi and Lake Mekkojärvi, and complemented this with a shotgun metagenomic analysis from Alinen-Mustajärvi and an analysis of pmoA genes and 16S rRNA, mcrA, and pmoA transcripts from Mekkojärvi. Furthermore, we tested the effect of various electron acceptors and light on methane oxidation (13C-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-Mustajärvi, while methanotrophs belonging to Methylobacter were more abundant in Mekkojärvi. 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 gammaproteobacterial methanotrophs, imply that boreal lake methanotrophs may couple methane oxidation with NOx- reduction in hypoxic conditions.


KEY WORDS: Methanotroph · Methane oxidation · Boreal lake · Water column · Shotgun metagenomics · 16S rRNA · mcrA


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Cite this article as: Rissanen AJ, Saarenheimo J, Tiirola M, Peura S, Aalto SL, Karvinen A, Nykänen H (2018) Gammaproteobacterial methanotrophs dominate methanotrophy in aerobic and anaerobic layers of boreal lake waters. Aquat Microb Ecol 81:257-276. https://doi.org/10.3354/ame01874

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