The widespread capability of methylphosphonate utilization in filamentous cyanobacteria and its ecological significance

Aquatic ecosystems comprise almost half of total global methane emissions. Recent evidence indicates that a few strains of cyanobacteria, the predominant primary producers in bodies of water, can produce methane under oxic conditions with methylphosphonate serving as substrate. In this work, we have screened the published 2 568 cyanobacterial genomes for genetic elements encoding phosphonate-metabolizing enzymes. We show that phosphonate degradation (phn) gene clusters are widely distributed in filamentous cyanobacteria, including several bloom-forming genera. Algal growth experiments revealed that methylphosphonate is an alternative phosphorous source for four of five tested strains carrying phn clusters, and can sustain cellular metabolic homeostasis of strains under phosphorus stress. Liberation of methane by cyanobacteria in the presence of methylphosphonate occurred mostly during the light period of a 12 h/12 h diurnal cycle and was suppressed in the presence of orthophosphate, features that are consistent with observations in natural aquatic systems under oxic conditions. The results presented here demonstrate a genetic basis for ubiquitous methane emission via cyanobacterial methylphosphonate mineralization, while contributing to the phosphorus redox cycle.

Automated summary

Cyanobacteria in aquatic ecosystems can produce methane through methylphosphonate under oxic conditions, which is consistent with observations in natural water systems. Screening of cyanobacterial genomes revealed the widespread distribution of phosphonate degradation gene clusters in filamentous cyanobacteria. This study demonstrates the genetic basis for cyanobacterial methane emission via methylphosphonate mineralization and its contribution to the phosphorus redox cycle.