Elucidating the picocyanobacteria salinity divide through ecogenomics of new freshwater isolates.

Brackish Cyanobium Freshwater Genomics Marine Salinity divide Synechococcus

Journal

BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720

Informations de publication

Date de publication:
08 08 2022
Historique:
received: 21 02 2022
accepted: 26 07 2022
entrez: 8 8 2022
pubmed: 9 8 2022
medline: 11 8 2022
Statut: epublish

Résumé

Cyanobacteria are the major prokaryotic primary producers occupying a range of aquatic habitats worldwide that differ in levels of salinity, making them a group of interest to study one of the major unresolved conundrums in aquatic microbiology which is what distinguishes a marine microbe from a freshwater one? We address this question using ecogenomics of a group of picocyanobacteria (cluster 5) that have recently evolved to inhabit geographically disparate salinity niches. Our analysis is made possible by the sequencing of 58 new genomes from freshwater representatives of this group that are presented here, representing a 6-fold increase in the available genomic data. Overall, freshwater strains had larger genomes (≈2.9 Mb) and %GC content (≈64%) compared to brackish (2.69 Mb and 64%) and marine (2.5 Mb and 58.5%) isolates. Genomic novelties/differences across the salinity divide highlighted acidic proteomes and specific salt adaptation pathways in marine isolates (e.g., osmolytes/compatible solutes - glycine betaine/ggp/gpg/gmg clusters and glycerolipids glpK/glpA), while freshwater strains possessed distinct ion/potassium channels, permeases (aquaporin Z), fatty acid desaturases, and more neutral/basic proteomes. Sulfur, nitrogen, phosphorus, carbon (photosynthesis), or stress tolerance metabolism while showing distinct genomic footprints between habitats, e.g., different types of transporters, did not obviously translate into major functionality differences between environments. Brackish microbes show a mixture of marine (salt adaptation pathways) and freshwater features, highlighting their transitional nature. The plethora of freshwater isolates provided here, in terms of trophic status preference and genetic diversity, exemplifies their ability to colonize ecologically diverse waters across the globe. Moreover, a trend towards larger and more flexible/adaptive genomes in freshwater picocyanobacteria may hint at a wider number of ecological niches in this environment compared to the relatively homogeneous marine system.

Sections du résumé

BACKGROUND
Cyanobacteria are the major prokaryotic primary producers occupying a range of aquatic habitats worldwide that differ in levels of salinity, making them a group of interest to study one of the major unresolved conundrums in aquatic microbiology which is what distinguishes a marine microbe from a freshwater one? We address this question using ecogenomics of a group of picocyanobacteria (cluster 5) that have recently evolved to inhabit geographically disparate salinity niches. Our analysis is made possible by the sequencing of 58 new genomes from freshwater representatives of this group that are presented here, representing a 6-fold increase in the available genomic data.
RESULTS
Overall, freshwater strains had larger genomes (≈2.9 Mb) and %GC content (≈64%) compared to brackish (2.69 Mb and 64%) and marine (2.5 Mb and 58.5%) isolates. Genomic novelties/differences across the salinity divide highlighted acidic proteomes and specific salt adaptation pathways in marine isolates (e.g., osmolytes/compatible solutes - glycine betaine/ggp/gpg/gmg clusters and glycerolipids glpK/glpA), while freshwater strains possessed distinct ion/potassium channels, permeases (aquaporin Z), fatty acid desaturases, and more neutral/basic proteomes. Sulfur, nitrogen, phosphorus, carbon (photosynthesis), or stress tolerance metabolism while showing distinct genomic footprints between habitats, e.g., different types of transporters, did not obviously translate into major functionality differences between environments. Brackish microbes show a mixture of marine (salt adaptation pathways) and freshwater features, highlighting their transitional nature.
CONCLUSIONS
The plethora of freshwater isolates provided here, in terms of trophic status preference and genetic diversity, exemplifies their ability to colonize ecologically diverse waters across the globe. Moreover, a trend towards larger and more flexible/adaptive genomes in freshwater picocyanobacteria may hint at a wider number of ecological niches in this environment compared to the relatively homogeneous marine system.

Identifiants

pubmed: 35941649
doi: 10.1186/s12915-022-01379-z
pii: 10.1186/s12915-022-01379-z
pmc: PMC9361551
doi:

Substances chimiques

Proteome 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

175

Informations de copyright

© 2022. The Author(s).

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Auteurs

Pedro J Cabello-Yeves (PJ)

Evolutionary Genomics Group, Departamento de Producción Vegetal y Microbiología, Universidad Miguel, Hernández, San Juan de Alicante, Alicante, Spain. pedrito91vlc@gmail.com.

Cristiana Callieri (C)

National Research Council (CNR), Institute of Water Research (IRSA), Verbania, Italy.

Antonio Picazo (A)

Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, E-46980, Paterna, Valencia, Spain.

Lena Schallenberg (L)

Department of Zoology, University of Otago, Dunedin, New Zealand.

Paula Huber (P)

Instituto Tecnológico de Chascomús (INTECH), UNSAM-CONICET, Av. Intendente Marino Km 8,200, (7130) Chascomús, Buenos Aires, Argentina.
Instituto Nacional de Limnología (INALI), CONICET-UNL, Ciudad Universitaria - Paraje el Pozo s/n, (3000), Santa Fé, Argentina.

Juan J Roda-Garcia (JJ)

Evolutionary Genomics Group, Departamento de Producción Vegetal y Microbiología, Universidad Miguel, Hernández, San Juan de Alicante, Alicante, Spain.

Maciej Bartosiewicz (M)

Department of Environmental Sciences, University of Basel, Basel, Switzerland.

Olga I Belykh (OI)

Limnological Institute, Russian Academy of Sciences, P.O. Box 278, 664033, Irkutsk, Russia.

Irina V Tikhonova (IV)

Limnological Institute, Russian Academy of Sciences, P.O. Box 278, 664033, Irkutsk, Russia.

Alberto Torcello-Requena (A)

School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK.

Paula Martin De Prado (PM)

School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK.

Richard J Puxty (RJ)

School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK.

Andrew D Millard (AD)

Department of Genetics and Genome Biology, University of Leicester, Leicester, LE1 7RH, UK.

Antonio Camacho (A)

Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, E-46980, Paterna, Valencia, Spain.

Francisco Rodriguez-Valera (F)

Evolutionary Genomics Group, Departamento de Producción Vegetal y Microbiología, Universidad Miguel, Hernández, San Juan de Alicante, Alicante, Spain.
Moscow Institute of Physics and Technology, Dolgoprudny, 141701, Russia.

David J Scanlan (DJ)

School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK. d.j.scanlan@warwick.ac.uk.

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Classifications MeSH