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Candidatus Methylumidiphilus Drives Peaks in Methanotrophic Relative Abundance in Stratified Lakes and Ponds Across Northern Landscapes

Martin, Gaëtan and Rissanen, Antti J. and Garcia, Sarahi L. and Mehrshad, Maliheh and Buck, Moritz and Peura, Sari (2021). Candidatus Methylumidiphilus Drives Peaks in Methanotrophic Relative Abundance in Stratified Lakes and Ponds Across Northern Landscapes. Frontiers in Microbiology. 12 , 669937
[Research article]

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Abstract

Boreal lakes and ponds produce two-thirds of the total natural methane emissions above the latitude of 50 degrees North. These lake emissions are regulated by methanotrophs which can oxidize up to 99% of the methane produced in the sediments and the water column. Despite their importance, the diversity and distribution of the methanotrophs in lakes are still poorly understood. Here, we used shotgun metagenomic data to explore the diversity and distribution of methanotrophs in 40 oxygen-stratified water bodies in boreal and subarctic areas in Europe and North America. In our data, gammaproteobacterial methanotrophs (order Methylococcales) generally dominated the methanotrophic communities throughout the water columns. A recently discovered lineage of Methylococcales, Candidatus Methylumidiphilus, was present in all the studied water bodies and dominated the methanotrophic community in lakes with a high relative abundance of methanotrophs. Alphaproteobacterial methanotrophs were the second most abundant group of methanotrophs. In the top layer of the lakes, characterized by low CH4 concentration, their abundance could surpass that of the gammaproteobacterial methanotrophs. These results support the theory that the alphaproteobacterial methanotrophs have a high affinity for CH4 and can be considered stress-tolerant strategists. In contrast, the gammaproteobacterial methanotrophs are competitive strategists. In addition, relative abundances of anaerobic methanotrophs, Candidatus Methanoperedenaceae and Candidatus Methylomirabilis, were strongly correlated, suggesting possible co-metabolism. Our data also suggest that these anaerobic methanotrophs could be active even in the oxic layers. In non-metric multidimensional scaling, alpha- and gammaproteobacterial methanotrophs formed separate clusters based on their abundances in the samples, except for the gammaproteobacterial Candidatus Methylumidiphilus, which was separated from these two clusters. This may reflect similarities in the niche and environmental requirements of the different genera within alpha- and gammaproteobacterial methanotrophs. Our study confirms the importance of O-2 and CH4 in shaping the methanotrophic communities and suggests that one variable cannot explain the diversity and distribution of the methanotrophs across lakes. Instead, we suggest that the diversity and distribution of freshwater methanotrophs are regulated by lake-specific factors.

Authors/Creators:Martin, Gaëtan and Rissanen, Antti J. and Garcia, Sarahi L. and Mehrshad, Maliheh and Buck, Moritz and Peura, Sari
Title:Candidatus Methylumidiphilus Drives Peaks in Methanotrophic Relative Abundance in Stratified Lakes and Ponds Across Northern Landscapes
Series Name/Journal:Frontiers in Microbiology
Year of publishing :2021
Volume:12
Article number:669937
Number of Pages:16
Publisher:FRONTIERS MEDIA SA
ISSN:1664-302X
Language:English
Publication Type:Research article
Article category:Scientific peer reviewed
Version:Published version
Copyright:Creative Commons: Attribution 4.0
Full Text Status:Public
Subjects:(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Microbiology (Microbiology in the medical area to be 30109)
Keywords:methanotroph, greenhouse gas, metagenomics, thaw ponds, microbial diversity, lakes
URN:NBN:urn:nbn:se:slu:epsilon-p-113516
Permanent URL:
http://urn.kb.se/resolve?urn=urn:nbn:se:slu:epsilon-p-113516
Additional ID:
Type of IDID
DOI10.3389/fmicb.2021.669937
Web of Science (WoS)000690892500001
ID Code:25305
Faculty:S - Faculty of Forest Sciences
NJ - Fakulteten för naturresurser och jordbruksvetenskap
Department:(NL, NJ) > Dept. of Forest Mycology and Plant Pathology
(S) > Dept. of Forest Mycology and Plant Pathology

(NL, NJ) > Dept. of Aquatic Sciences and Assessment
Deposited By: SLUpub Connector
Deposited On:10 Sep 2021 13:25
Metadata Last Modified:10 Sep 2021 13:31

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