Oxic methane production from methylphosphonate in a large oligotrophic lake: limitation by substrate and organic carbon supply

Logan M. Peoples, John E. Dore, Evan M. Bilbrey, Trista J. Vick-Majors, John R. Ranieri, Kate A. Evans, Abigail M. Ross, Shawn P. Devlin, Matthew J. Church

Research output: Contribution to journalArticlepeer-review

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 possible in situ oxic 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 genera Acidovorax, Rhodoferax, and Allorhizobium, 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.

Original languageEnglish
Article numbere01097-23
JournalApplied and Environmental Microbiology
Volume89
Issue number12
DOIs
StatePublished - Dec 2023

Keywords

  • Acidovorax
  • freshwater
  • lake
  • methane
  • methylphosphonate
  • phosphorus

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