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

Abstract

Boreal lakes and ponds produce two-thirds of the total natural methane emissions above the latitude of 50° 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 O2 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.

Exploring methane cycling in an arctic lake in Kangerlussuaq Greenland using stable isotopes and 16S rRNA gene sequencing

“…Frontiers in Environmental Science frontiersin.org lake were elevated throughout the water column (2 μM-27 μM), consistent with the ubiquitous presence of type I methanotrophs, which have been suggested to have lower methane affinity compared to type II methanotrophs (Martin et al, 2021).…”

“…Methylumidiphilus within the order Methylococcales, had high relative abundances throughout the lake, but Alphaproteobacteria known to be type II methanotrophs had high relative abundance in surface water where methane concentrations were comparatively low (0 μM-1 μM) (Martin et al, 2021). In comparison, methane concentrations in Teardrop (A-C).…”

Characterization and genome analysis of a psychrophilic methanotroph representing a ubiquitous Methylobacter spp. cluster in boreal lake ecosystems

“…Strain S3L5C, isolated and classified in this study as Methylobacter sp., has been previously reported to be a dominant genus in the oxic-anoxic transition zone in boreal and subarctic lakes, ponds, and wetlands [ 7 , 8 , 10 , 11 , 50 – 52 ]. Our phylogenetic and phylogenomic tree analyses showed that the isolate represents a ubiquitous cluster of Methylobacter spp.…”

Characterization and genome analysis of a psychrophilic methanotroph representing a ubiquitousMethylobacterspp. cluster in boreal lake ecosystems

“…Strain S3L5C, isolated and classified in this study as Methylobacter sp., has been previously reported to be a dominant genus at oxic-anoxic transition zone in boreal and subarctic lakes, ponds and wetlands (Cabrol et al, 2020; Cassarini et al, 2019; Martin et al, 2021; Rissanen et al, 2021b, 2018; Smith et al, 2018; van Grinsven et al, 2021a). Our phylogenetic and phylogenomic tree analyses showed that the isolate represents a ubiquitous cluster of Methylobacter spp.…”