Remarkably coherent population structure for a dominant Antarctic Chlorobium species

Abstract 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,...

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Autores principales:	Pratibha Panwar, Michelle A. Allen, Timothy J. Williams, Sabrina Haque, Sarah Brazendale, Alyce M. Hancock, David Paez-Espino, Ricardo Cavicchioli
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Antarctic microbiology Green sulphur bacteria Chlorobi Vitamin B12 Metagenome-assembled genomes Phylotype Microbial ecology QR100-130
Acceso en línea:	https://doaj.org/article/1a7f88f0b8a046659544a26a77333b29
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spelling	oai:doaj.org-article:1a7f88f0b8a046659544a26a77333b292021-11-28T12:08:11ZRemarkably coherent population structure for a dominant Antarctic Chlorobium species10.1186/s40168-021-01173-z2049-2618https://doaj.org/article/1a7f88f0b8a046659544a26a77333b292021-11-01T00:00:00Zhttps://doi.org/10.1186/s40168-021-01173-zhttps://doaj.org/toc/2049-2618Abstract 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 ~ 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 (> 108 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. Video abstractPratibha PanwarMichelle A. AllenTimothy J. WilliamsSabrina HaqueSarah BrazendaleAlyce M. HancockDavid Paez-EspinoRicardo CavicchioliBMCarticleAntarctic microbiologyGreen sulphur bacteriaChlorobiVitamin B12Metagenome-assembled genomesPhylotypeMicrobial ecologyQR100-130ENMicrobiome, Vol 9, Iss 1, Pp 1-23 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Antarctic microbiology Green sulphur bacteria Chlorobi Vitamin B12 Metagenome-assembled genomes Phylotype Microbial ecology QR100-130
spellingShingle	Antarctic microbiology Green sulphur bacteria Chlorobi Vitamin B12 Metagenome-assembled genomes Phylotype Microbial ecology QR100-130 Pratibha Panwar Michelle A. Allen Timothy J. Williams Sabrina Haque Sarah Brazendale Alyce M. Hancock David Paez-Espino Ricardo Cavicchioli Remarkably coherent population structure for a dominant Antarctic Chlorobium species
description	Abstract 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 ~ 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 (> 108 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. Video abstract
format	article
author	Pratibha Panwar Michelle A. Allen Timothy J. Williams Sabrina Haque Sarah Brazendale Alyce M. Hancock David Paez-Espino Ricardo Cavicchioli
author_facet	Pratibha Panwar Michelle A. Allen Timothy J. Williams Sabrina Haque Sarah Brazendale Alyce M. Hancock David Paez-Espino Ricardo Cavicchioli
author_sort	Pratibha Panwar
title	Remarkably coherent population structure for a dominant Antarctic Chlorobium species
title_short	Remarkably coherent population structure for a dominant Antarctic Chlorobium species
title_full	Remarkably coherent population structure for a dominant Antarctic Chlorobium species
title_fullStr	Remarkably coherent population structure for a dominant Antarctic Chlorobium species
title_full_unstemmed	Remarkably coherent population structure for a dominant Antarctic Chlorobium species
title_sort	remarkably coherent population structure for a dominant antarctic chlorobium species
publisher	BMC
publishDate	2021
url	https://doaj.org/article/1a7f88f0b8a046659544a26a77333b29
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Remarkably coherent population structure for a dominant Antarctic Chlorobium species

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