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ABSTRACT While methane is typically produced under anoxic conditions, methane supersaturation in the presence of oxygen has been observed in both marine and fresh waters. The biological cleavage of methylphosphonate (MPn), which releases both phosphate and methane, is one pathway that may contribute to this paradox. Here, we explore the genomic and functional potential for oxic methane production (OMP) via MPn in Flathead Lake, a large oligotrophic freshwater lake in northwest Montana. Time series and depth profile measurements show that epilimnetic methane was persistently supersaturated despite high oxygen levels, suggesting a possiblein situoxic source. Metagenomic sequencing indicated that 10% of microorganisms in the lake, many of which are related to the Burkholderiales (Betaproteobacteria) and Actinomycetota, have the genomic capacity to cleave MPn. We experimentally demonstrated that these organisms produce methane stoichiometrically with MPn consumption across multiple years. However, methane was only produced at appreciable rates in the presence of MPn when a labile organic carbon source was added, suggesting that this process may be limited by both MPn and labile carbon supply. Members of the generaAcidovorax,Rhodoferax, andAllorhizobium, organisms which make up less than 1% of Flathead Lake communities, consistently responded to MPn addition. We demonstrate that the genomic and physiological potential for MPn use exists among diverse, resident members of Flathead Lake and could contribute to OMP in freshwater lakes when substrates are available. IMPORTANCEMethane is an important greenhouse gas that is typically produced under anoxic conditions. We show that methane is supersaturated in a large oligotrophic lake despite the presence of oxygen. Metagenomic sequencing indicates that diverse, widespread microorganisms may contribute to the oxic production of methane through the cleavage of methylphosphonate. We experimentally demonstrate that these organisms, especially members of the genusAcidovorax, can produce methane through this process. However, appreciable rates of methane production only occurred when both methylphosphonate and labile sources of carbon were added, indicating that this process may be limited to specific niches and may not be completely responsible for methane concentrations in Flathead Lake. This work adds to our understanding of methane dynamics by describing the organisms and the rates at which they can produce methane through an oxic pathway in a representative oligotrophic lake. 

ABSTRACT Five metagenome-assembled genomes were obtained from the bottom waters of Echo Lake, Montana. These genomes suggest that lineages involved in methane oxidation and sulfur cycling flourish near the steep oxygen and methane chemocline in Echo Lake. 

Abstract Nitrification is an important control on the form and distribution of nitrogen in freshwater ecosystems. However, the seasonality of nitrogen pools and the diversity of organisms catalyzing this process have not been well documented in oligotrophic lakes. Here, we show that nitrogen pools and nitrifying organisms in Flathead Lake are temporally and vertically dynamic, with nitrifiers displaying specific preferences depending on the season. While the ammonia‐oxidizing bacteria (AOB) Nitrosomonadaceae and nitrite‐oxidizing bacteria (NOB)Nitrotogadominate at depth in the summer, the ammonia‐oxidizing archaea (AOA) Nitrososphaerota and NOB Nitrospirota become abundant in the winter. Given clear seasonality in ammonium, with higher concentrations during the summer, we hypothesize that the succession between these two nitrifying groups may be due to nitrogen affinity, with AOB more competitive when ammonia concentrations are higher and AOA when they are lower. Nitrifiers in Flathead Lake share more than 99% average nucleotide identity with those reported in other North American lakes but are distinct from those in Europe and Asia, indicating a role for geographic isolation as a factor controlling speciation among nitrifiers. Our study shows there are seasonal shifts in nitrogen pools and nitrifying populations, highlighting the dynamic spatial and temporal nature of nitrogen cycling in freshwater ecosystems. 

Summary Hot springs integrate hydrologic and geologic processes that vary over short‐ and long‐term time scales. However, the influence of temporal hydrologic and geologic change on hot spring biodiversity is unknown. Here, we coordinated near‐weekly, cross‐seasonal (~140 days) geochemical and microbial community analyses of three widely studied hot springs with local precipitation data in Yellowstone National Park. One spring (‘HFS’) exhibited statistically significant, coupled microbial and geochemical variation across seasons that was associated with recent precipitation patterns. Two other spring communities, ‘CP’ and ‘DS’, exhibited minimal to no variation across seasons. Variability in the seasonal response of springs is attributed to differences in the timing and extent of aquifer recharge with oxidized near‐surface water from precipitation. This influx of oxidized water is associated with changes in community composition, and in particular, the abundances of aerobic sulfide‐/sulfur‐oxidizers that can acidify waters. During sampling, a new spring formed after a period of heavy precipitation and its successional dynamics were also influenced by surface water recharge. Collectively, these results indicate that changes in short‐term hydrology associated with precipitation can impact hot spring geochemistry and microbial biodiversity. These results point to potential susceptibility of certain hot springs and their biodiversity to sustained, longer‐term hydrologic changes.