Differential global distribution of marine picocyanobacteria gene clusters reveals distinct niche-related adaptive strategies.

Doré, H; Guyet, U; Leconte, J; Farrant, GK; Alric, B; Ratin, M; Ostrowski, M; Ferrieux, M; Brillet-Guéguen, L; Hoebeke, M; Siltanen, J; Le Corguillé, G; Corre, E; Wincker, P; Scanlan, DJ; Eveillard, D; Partensky, F; Garczarek, L

Differential global distribution of marine picocyanobacteria gene clusters reveals distinct niche-related adaptive strategies.

Doré, H Guyet, U Leconte, J Farrant, GK Alric, B Ratin, M Ostrowski, M

Ferrieux, M Brillet-Guéguen, L Hoebeke, M Siltanen, J Le Corguillé, G Corre, E Wincker, P Scanlan, DJ Eveillard, D Partensky, F Garczarek, L

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Publisher:: SPRINGERNATURE
Publication Type:: Journal Article
Citation:: ISME J, 2023, 17, (5), pp. 720-732
Issue Date:: 2023-05

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Field	Value	Language
dc.contributor.author	Doré, H
dc.contributor.author	Guyet, U
dc.contributor.author	Leconte, J
dc.contributor.author	Farrant, GK
dc.contributor.author	Alric, B
dc.contributor.author	Ratin, M
dc.contributor.author	Ostrowski, M https://orcid.org/0000-0002-4357-3023
dc.contributor.author	Ferrieux, M
dc.contributor.author	Brillet-Guéguen, L
dc.contributor.author	Hoebeke, M
dc.contributor.author	Siltanen, J
dc.contributor.author	Le Corguillé, G
dc.contributor.author	Corre, E
dc.contributor.author	Wincker, P
dc.contributor.author	Scanlan, DJ
dc.contributor.author	Eveillard, D
dc.contributor.author	Partensky, F
dc.contributor.author	Garczarek, L
dc.date.accessioned	2024-03-19T04:03:51Z
dc.date.available	2023-02-14
dc.date.available	2024-03-19T04:03:51Z
dc.date.issued	2023-05
dc.identifier.citation	ISME J, 2023, 17, (5), pp. 720-732
dc.identifier.issn	1751-7362
dc.identifier.issn	1751-7370
dc.identifier.uri	http://hdl.handle.net/10453/176912
dc.description.abstract	The ever-increasing number of available microbial genomes and metagenomes provides new opportunities to investigate the links between niche partitioning and genome evolution in the ocean, especially for the abundant and ubiquitous marine picocyanobacteria Prochlorococcus and Synechococcus. Here, by combining metagenome analyses of the Tara Oceans dataset with comparative genomics, including phyletic patterns and genomic context of individual genes from 256 reference genomes, we show that picocyanobacterial communities thriving in different niches possess distinct gene repertoires. We also identify clusters of adjacent genes that display specific distribution patterns in the field (eCAGs) and are thus potentially involved in the same metabolic pathway and may have a key role in niche adaptation. Several eCAGs are likely involved in the uptake or incorporation of complex organic forms of nutrients, such as guanidine, cyanate, cyanide, pyrimidine, or phosphonates, which might be either directly used by cells, for example for the biosynthesis of proteins or DNA, or degraded to inorganic nitrogen and/or phosphorus forms. We also highlight the enrichment of eCAGs involved in polysaccharide capsule biosynthesis in Synechococcus populations thriving in both nitrogen- and phosphorus-depleted areas vs. low-iron (Fe) regions, suggesting that the complexes they encode may be too energy-consuming for picocyanobacteria thriving in the latter areas. In contrast, Prochlorococcus populations thriving in Fe-depleted areas specifically possess an alternative respiratory terminal oxidase, potentially involved in the reduction of Fe(III) to Fe(II). Altogether, this study provides insights into how phytoplankton communities populate oceanic ecosystems, which is relevant to understanding their capacity to respond to ongoing climate change.
dc.format	Print-Electronic
dc.language	eng
dc.publisher	SPRINGERNATURE
dc.relation.ispartof	ISME J
dc.relation.isbasedon	10.1038/s41396-023-01386-0
dc.rights	info:eu-repo/semantics/openAccess
dc.subject	05 Environmental Sciences, 06 Biological Sciences, 10 Technology
dc.subject.classification	Microbiology
dc.subject.classification	31 Biological sciences
dc.subject.classification	41 Environmental sciences
dc.subject.mesh	Seawater
dc.subject.mesh	Ecosystem
dc.subject.mesh	Ferric Compounds
dc.subject.mesh	Oceans and Seas
dc.subject.mesh	Synechococcus
dc.subject.mesh	Metagenome
dc.subject.mesh	Multigene Family
dc.subject.mesh	Nitrogen
dc.subject.mesh	Phosphorus
dc.subject.mesh	Prochlorococcus
dc.subject.mesh	Phylogeny
dc.subject.mesh	Synechococcus
dc.subject.mesh	Prochlorococcus
dc.subject.mesh	Nitrogen
dc.subject.mesh	Phosphorus
dc.subject.mesh	Ferric Compounds
dc.subject.mesh	Ecosystem
dc.subject.mesh	Seawater
dc.subject.mesh	Phylogeny
dc.subject.mesh	Multigene Family
dc.subject.mesh	Oceans and Seas
dc.subject.mesh	Metagenome
dc.subject.mesh	Seawater
dc.subject.mesh	Ecosystem
dc.subject.mesh	Ferric Compounds
dc.subject.mesh	Oceans and Seas
dc.subject.mesh	Synechococcus
dc.subject.mesh	Metagenome
dc.subject.mesh	Multigene Family
dc.subject.mesh	Nitrogen
dc.subject.mesh	Phosphorus
dc.subject.mesh	Prochlorococcus
dc.subject.mesh	Phylogeny
dc.title	Differential global distribution of marine picocyanobacteria gene clusters reveals distinct niche-related adaptive strategies.
dc.type	Journal Article
utslib.citation.volume	17
utslib.location.activity	England
utslib.for	05 Environmental Sciences
utslib.for	06 Biological Sciences
utslib.for	10 Technology
pubs.organisational-group	University of Technology Sydney
pubs.organisational-group	University of Technology Sydney/Faculty of Science
utslib.copyright.status	open_access	*
dc.date.updated	2024-03-19T04:03:47Z
pubs.issue	5
pubs.publication-status	Published
pubs.volume	17
utslib.citation.issue	5

Abstract:

The ever-increasing number of available microbial genomes and metagenomes provides new opportunities to investigate the links between niche partitioning and genome evolution in the ocean, especially for the abundant and ubiquitous marine picocyanobacteria Prochlorococcus and Synechococcus. Here, by combining metagenome analyses of the Tara Oceans dataset with comparative genomics, including phyletic patterns and genomic context of individual genes from 256 reference genomes, we show that picocyanobacterial communities thriving in different niches possess distinct gene repertoires. We also identify clusters of adjacent genes that display specific distribution patterns in the field (eCAGs) and are thus potentially involved in the same metabolic pathway and may have a key role in niche adaptation. Several eCAGs are likely involved in the uptake or incorporation of complex organic forms of nutrients, such as guanidine, cyanate, cyanide, pyrimidine, or phosphonates, which might be either directly used by cells, for example for the biosynthesis of proteins or DNA, or degraded to inorganic nitrogen and/or phosphorus forms. We also highlight the enrichment of eCAGs involved in polysaccharide capsule biosynthesis in Synechococcus populations thriving in both nitrogen- and phosphorus-depleted areas vs. low-iron (Fe) regions, suggesting that the complexes they encode may be too energy-consuming for picocyanobacteria thriving in the latter areas. In contrast, Prochlorococcus populations thriving in Fe-depleted areas specifically possess an alternative respiratory terminal oxidase, potentially involved in the reduction of Fe(III) to Fe(II). Altogether, this study provides insights into how phytoplankton communities populate oceanic ecosystems, which is relevant to understanding their capacity to respond to ongoing climate change.

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http://hdl.handle.net/10453/176912