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

Abstract

Lakes and ponds are considered as a major natural source of CH4 emissions, particularly during the ice-free period in boreal ecosystems. Aerobic methane-oxidizing bacteria (MOB), which utilize CH4 using oxygen as an electron acceptor, are one of the dominant microorganisms in the CH4-rich water columns. Metagenome-assembled genomes (MAGs) have revealed the genetic potential of MOB from boreal aquatic ecosystems for various microaerobic/anaerobic metabolic functions. However, experimental proof of these functions, i.e., organic acid production via fermentation, by lake MOB is lacking. In addition, psychrophilic (i.e., cold-loving) MOB and their CH4-oxidizing process have rarely been investigated. In this study, we isolated, provided a taxonomic description, and analyzed the genome of Methylobacter sp. S3L5C, a psychrophilic MOB, from a boreal lake in Finland. Based on phylogenomic comparisons to MAGs, Methylobacter sp. S3L5C represented a ubiquitous cluster of Methylobacter spp. in boreal aquatic ecosystems. At optimal temperatures (3–12 °C) and pH (6.8–8.3), the specific growth rates (µ) and CH4 utilization rate were in the range of 0.018–0.022 h−1 and 0.66–1.52 mmol l−1 d−1, respectively. In batch cultivation, the isolate could produce organic acids, and the concentrations were elevated after replenishing CH4 and air into the headspace. Up to 4.1 mM acetate, 0.02 mM malate, and 0.07 mM propionate were observed at the end of the test under optimal operational conditions. The results herein highlight the key role of Methylobacter spp. in regulating CH4 emissions and their potential to provide CH4-derived organic carbon compounds to surrounding heterotrophic microorganisms in cold ecosystems.

Versatile methanotrophs form an active methane biofilter in the oxycline of a seasonally stratified coastal basin

“…The methanotrophic community in the water column of Lake Grevelingen mainly consisted of Methylomonadaceae belonging to the aerobic gamma‐MOB. Although gamma‐MOB were also the dominant MOB in the water column of other marine and freshwater ecosystems during water column stratification (Blees et al, 2014; Khanongnuch et al, 2022; Padilla et al, 2017; Rissanen et al, 2018), the small reservoir of alpha‐MOB (<0.05% relative abundance), indicates that alpha‐MOB might still be active at different stages of water column stratification as observed in freshwater lakes (Mayr, Zimmermann, Dey, et al, 2020).…”

Versatile methanotrophs form an active methane biofilter in the oxycline of a seasonally stratified coastal basin

“…Gamma-MOB were also the dominant MOB group in the water column of other marine and freshwater ecosystems during water column stratification (Blees et al ., 2014; Padilla et al ., 2017; Rissanen et al ., 2018; Khanongnuch et al ., 2022). The sole gamma-MOB family detected in the water column of Lake Grevelingen, Methylomonadaceae , showed clear niche-partitioning as different genera peaked at various depths.…”

Draft genome sequence data of a psychrophilic tundra soil methanotroph, Methylobacter psychrophilus Z-0021 (DSM 9914)

“…In comparison to Methylobacter spp., the resequenced Z-0021 16S rRNA gene demonstrated high sequence similarities with the 16S rRNA gene of a recently isolated psychrophilic methanotroph, Methylobacter sp. S3L5C (99.7% similarity) [3] , and M. tundripaludum SV96 (99.3%), while the 16S rRNA gene similarity with other Methylobacter strains was much lower (95.4-98.0%) ( Fig. 1 A).…”

“…Psychrophilic (i.e., cold-loving) methanotrophic bacteria are widely distributed and play an important role in methane removal in cold, boreal and arctic soil and aquatic ecosystems [1] , [2] , [3] . They could also be applied in the bioconversion of biogas- and natural gas methane into value-added products in cold environments [4] .…”

“…Therefore, genomic data of psychrophilic methanotrophs is needed to provide important insights into their functional capabilities. However, psychrophilic methanotroph isolates and consequently their genomes are currently rare [3] . A psychrophilic methanotroph, Methylobacter psychrophilus Z-0021, was isolated from tundra soil during the 1990s [5] .…”