Phosphonate-driven oxic CH4 production by <i>Variovorax xiamenensis</i> sp. nov.: insights from marine and freshwater microbial adaptations to P-limitation

Methane (CH₄) emissions in oxygenated aquatic environments challenge traditional views of methanogenesis suggesting the presence of alternative microbial CH₄ production pathways. This study identifies a novel bacterial species, <i>Variovorax xiamenensis</i> W6^T, capable of utilizing methylphosphonate (MPn) as its sole phosphorus (P) source under laboratory conditions, thereby supporting growth and CH₄ production in phosphorus-limited conditions. Transcriptomic analyses, as well as incubation experiments, reveal that CH₄ emission via the phosphonate-degrading <i>phn</i> gene cluster, encoding a C-P lyase, is tightly regulated by inorganic phosphate (Pi) availability, linking nutrient scarcity to methane cycling. A genomic survey of over 16 000 prokaryotic genomes reveals the widespread occurrence of <i>phn</i> gene cluster in 9% of the analyzed genomes, predominantly within the phylum <i>Pseudomonadota</i>. While MPn metabolism has been well-documented in marine environments, its presence and ecological role in freshwater systems remain underexplored. Our findings highlight the potential for phosphonate-driven methane production in freshwater ecosystems and underscore the need for further research to quantify MPn concentrations and its contribution to global methane budgets. This study emphasizes the importance of integrating microbial phosphonate metabolism into models of biogeochemical cycling and climate predictions, particularly under scenarios of increasing phosphorus limitation driven by global warming.