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

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 ( 13 C-CH 4 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 (SO 4 2− , Fe 3+ , Mn 4+ , and anthraquinone-2, 6-disulfonate), except for NO 3 − , 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 gamma proteobacterial methanotrophs, imply that boreal lake methanotrophs may couple methane oxidation with NO x − reduction in hypoxic conditions.

Thriving in Wetlands: Ecophysiology of the Spiral-Shaped Methanotroph Methylospira mobilis as Revealed by the Complete Genome Sequence

“…Similar preferences for reduced O 2 concentrations were earlier reported for several gammaproteobacterial methanotrophs isolated from lake sediments, such as Methylosoma difficile and Methyloglobulus morosus [65,66]. Candidatus Methyloumidiphilus alinensis, one of the closest phylogenetic relatives of strain Shm1, was also detected at the oxycline of a humic lake in Finland, at a depth of 3 to 4.5 m [43].…”

“…Their comparative analysis confirmed an earlier report that strain Shm1 is affiliated with the clade of Methylococcus-related, type Ib methanotrophs [11]. Methyloterricola oryzae 73a T [21] and Candidatus Methyloumidiphilus alinensis [43] were identified as the two closest phylogenetic relatives of strain Shm1. The most closely related methanotroph with a complete genome sequence, however, was Methylococcus capsulatus Bath ( Figure 2), which displayed 94.3% 16S rRNA gene sequence similarity to strain Shm1.…”

Novel autotrophic organisms contribute significantly to the internal carbon cycling potential of a boreal lake

“…In accordance with the redox potentials in the water column, and literature (30, 31), the reduction of nitrate to N2 was dispersed among multiple organisms. Candidatus Methyloumidiphilus alinensis (bin 10) (32) and a MAG closely affiliated with Chrenotrix (bin 149) both had a complete narGHIJ operon for nitrate reduction, and also genes for methane oxidation, as has been previously described for a member of Methylobacter family (33). Gene NosZ, coding for N 2 O reductase, was present in two high quality MAGs, which were taxonomically assigned to Myxococcales (bin 233) and Bacteroidetes (bin 64).…”

CH4 oxidation in a boreal lake during the development of hypolimnetic hypoxia

“…downwelling of oxygenated water) in otherwise hypoxic layers potentially fueled methanotrophy below the oxycline, thus stimulating microaerobic CH 4 oxidation (Kalyuzhnaya et al 2013;Blees et al 2014;Kits et al 2015). Recently, aerobic gamma-proteobacterial methanotrophs have been reported to almost exclusively dominate the methanotrophic community in both oxic and anoxic layers of boreal and temperate lakes (Milucka et al 2015;Oswald et al 2016;Rissanen et al 2018). Further research identifying the microbial communities involved in these processes is required to confirm whether the metabolism of methane-oxidizing microbes in Lake Kuivajärvi was aerobic or anaerobic.…”