4.8 Article

Remarkably coherent population structure for a dominant Antarctic Chlorobium species

Journal

MICROBIOME
Volume 9, Issue 1, Pages -

Publisher

BMC
DOI: 10.1186/s40168-021-01173-z

Keywords

Antarctic microbiology; Green sulphur bacteria; Chlorobi; Vitamin B12; Metagenome-assembled genomes; Phylotype; Ecotype; Population structure; Host-virus interactions; Generalist virus; Meromictic lake; Microbial food web

Categories

Funding

  1. Australian Research Council [DP150100244]
  2. Australian Antarctic Science programme [4031]
  3. Office of Science of the US Department of Energy [DE-AC02-05CH11231]

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The formation of Antarctic microbial communities is influenced by various factors, with sunlight hours and the population structure of green sulfur bacteria playing important roles. Studies show that a specific population of green sulfur bacteria provides essential ecosystem services in Antarctica.
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, a Chlorobium species 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 59 Chlorobium metagenome-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, Candidatus Chlorobium antarcticum (most similar to Chlorobium phaeovibrioides DSM265) 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 similar to 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 (> 10(8) cells ml(-1) in Ace Lake) and seasonal cycle of cell lysis likely make Ca. Chlorobium antarcticum a major provider of cobalamin to the food web. Analysis of Ca. 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 in Ca. 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. The Chlorobium population 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 this Chlorobium species.

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