Remarkably coherent population structure for a dominant Antarctic Chlorobium species

Background In Antarctica, summer sunlight enables phototrophic microorganisms to drive primary production, thereby “feeding” ecosystems to enable their persistence through the long, dark winter months. In Ace Lake, a stratified marine-derived system in the Vestfold Hills of East Antarctica, aChlorobiumspecies of green sulphur bacteria (GSB) is the dominant phototroph, although its seasonal abundance changes more than 100-fold. Here, we analysed 413 Gb of Antarctic metagenome data including 59Chlorobiummetagenome-assembled genomes (MAGs) from Ace Lake and nearby stratified marine basins to determine how genome variation and population structure across a 7-year period impacted ecosystem function. Results A single species,CandidatusChlorobium antarcticum (most similar toChlorobium phaeovibrioidesDSM265) prevails in all three aquatic systems and harbours very little genomic variation (≥ 99% average nucleotide identity). A notable feature of variation that did exist related to the genomic capacity to biosynthesize cobalamin. The abundance of phylotypes with this capacity changed seasonally ~ 2-fold, consistent with the population balancing the value of a bolstered photosynthetic capacity in summer against an energetic cost in winter. The very high GSB concentration (> 108cells ml−1in Ace Lake) and seasonal cycle of cell lysis likely makeCa.Chlorobium antarcticum a major provider of cobalamin to the food web. Analysis ofCa.Chlorobium antarcticum viruses revealed the species to be infected by generalist (rather than specialist) viruses with a broad host range (e.g., infecting Gammaproteobacteria) that were present in diverse Antarctic lakes. The marked seasonal decrease inCa.Chlorobium antarcticum abundance may restrict specialist viruses from establishing effective lifecycles, whereas generalist viruses may augment their proliferation using other hosts. Conclusion The factors shaping Antarctic microbial communities are gradually being defined. In addition to the cold, the annual variation in sunlight hours dictates which phototrophic species can grow and the extent to which they contribute to ecosystem processes. TheChlorobiumpopulation studied was inferred to provide cobalamin, in addition to carbon, nitrogen, hydrogen, and sulphur cycling, as critical ecosystem services. The specific Antarctic environmental factors and major ecosystem benefits afforded by this GSB likely explain why such a coherent population structure has developed in thisChlorobiumspecies.