Elucidating the picocyanobacteria salinity divide through ecogenomics of new freshwater isolates
Abstract 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 marin...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-08-01
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| Series: | BMC Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12915-022-01379-z |
| _version_ | 1811215695497658368 |
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| author | Pedro J. Cabello-Yeves Cristiana Callieri Antonio Picazo Lena Schallenberg Paula Huber Juan J. Roda-Garcia Maciej Bartosiewicz Olga I. Belykh Irina V. Tikhonova Alberto Torcello-Requena Paula Martin De Prado Richard J. Puxty Andrew D. Millard Antonio Camacho Francisco Rodriguez-Valera David J. Scanlan |
| author_facet | Pedro J. Cabello-Yeves Cristiana Callieri Antonio Picazo Lena Schallenberg Paula Huber Juan J. Roda-Garcia Maciej Bartosiewicz Olga I. Belykh Irina V. Tikhonova Alberto Torcello-Requena Paula Martin De Prado Richard J. Puxty Andrew D. Millard Antonio Camacho Francisco Rodriguez-Valera David J. Scanlan |
| author_sort | Pedro J. Cabello-Yeves |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-04-12T06:26:45Z |
| format | Article |
| id | doaj.art-2efb0966c7fa459e8977033264bdefda |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-12T06:26:45Z |
| publishDate | 2022-08-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-2efb0966c7fa459e8977033264bdefda2022-12-22T03:44:07ZengBMCBMC Biology1741-70072022-08-0120112410.1186/s12915-022-01379-zElucidating the picocyanobacteria salinity divide through ecogenomics of new freshwater isolatesPedro J. Cabello-Yeves0Cristiana Callieri1Antonio Picazo2Lena Schallenberg3Paula Huber4Juan J. Roda-Garcia5Maciej Bartosiewicz6Olga I. Belykh7Irina V. Tikhonova8Alberto Torcello-Requena9Paula Martin De Prado10Richard J. Puxty11Andrew D. Millard12Antonio Camacho13Francisco Rodriguez-Valera14David J. Scanlan15Evolutionary Genomics Group, Departamento de Producción Vegetal y Microbiología, Universidad Miguel, HernándezNational Research Council (CNR), Institute of Water Research (IRSA)Cavanilles Institute of Biodiversity and Evolutionary Biology, University of ValenciaDepartment of Zoology, University of OtagoInstituto Tecnológico de Chascomús (INTECH), UNSAM-CONICETEvolutionary Genomics Group, Departamento de Producción Vegetal y Microbiología, Universidad Miguel, HernándezDepartment of Environmental Sciences, University of BaselLimnological Institute, Russian Academy of SciencesLimnological Institute, Russian Academy of SciencesSchool of Life Sciences, University of WarwickSchool of Life Sciences, University of WarwickSchool of Life Sciences, University of WarwickDepartment of Genetics and Genome Biology, University of LeicesterCavanilles Institute of Biodiversity and Evolutionary Biology, University of ValenciaEvolutionary Genomics Group, Departamento de Producción Vegetal y Microbiología, Universidad Miguel, HernándezSchool of Life Sciences, University of WarwickAbstract 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.https://doi.org/10.1186/s12915-022-01379-zSynechococcusCyanobiumFreshwaterMarineBrackishSalinity divide |
| spellingShingle | Pedro J. Cabello-Yeves Cristiana Callieri Antonio Picazo Lena Schallenberg Paula Huber Juan J. Roda-Garcia Maciej Bartosiewicz Olga I. Belykh Irina V. Tikhonova Alberto Torcello-Requena Paula Martin De Prado Richard J. Puxty Andrew D. Millard Antonio Camacho Francisco Rodriguez-Valera David J. Scanlan Elucidating the picocyanobacteria salinity divide through ecogenomics of new freshwater isolates BMC Biology Synechococcus Cyanobium Freshwater Marine Brackish Salinity divide |
| title | Elucidating the picocyanobacteria salinity divide through ecogenomics of new freshwater isolates |
| title_full | Elucidating the picocyanobacteria salinity divide through ecogenomics of new freshwater isolates |
| title_fullStr | Elucidating the picocyanobacteria salinity divide through ecogenomics of new freshwater isolates |
| title_full_unstemmed | Elucidating the picocyanobacteria salinity divide through ecogenomics of new freshwater isolates |
| title_short | Elucidating the picocyanobacteria salinity divide through ecogenomics of new freshwater isolates |
| title_sort | elucidating the picocyanobacteria salinity divide through ecogenomics of new freshwater isolates |
| topic | Synechococcus Cyanobium Freshwater Marine Brackish Salinity divide |
| url | https://doi.org/10.1186/s12915-022-01379-z |
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