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Effects of salinity and nutrient stress on a toxic freshwater cyanobacterial community and its associated microbiome: An experimental study
We aimed to evaluate the ability of naturally occurring colonies of Microcystis, embedded in a thick mucilage, to persist in estuarine waters. In two batch experiments, we examined the dynamics of microbial communities, including cyanobacteria and associated heterotrophic bacteria, sampled from the...
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Published in: | Environmental microbiology reports 2024-10, Vol.16 (5), p.e70029-n/a |
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description | We aimed to evaluate the ability of naturally occurring colonies of Microcystis, embedded in a thick mucilage, to persist in estuarine waters. In two batch experiments, we examined the dynamics of microbial communities, including cyanobacteria and associated heterotrophic bacteria, sampled from the field during both a cyanobacterial bloom (non‐limiting nutrient condition) and the post‐bloom period (limiting nutrient condition), and subjected them to a salinity gradient representative of the freshwater‐marine continuum. We demonstrated that both Microcystis aeruginosa and M. wesenbergii survived high salinities due to osmolyte accumulation. Specifically, prolonged exposure to high salinity led to betaine accumulation in the cyanobacterial biomass. The relative abundance of the mcyB gene remained around 30%, suggesting no selection for toxic genotypes with salinity or nutrient changes. Microcystins were predominantly intracellular, except at high salinity levels (>15), where more than 50% of the total microcystin concentration was extracellular. In both nutrient conditions, over 70% of the heterotrophic bacterial community belonged to the Gammaproteobacteria family, followed by the Bacteroidota. Bacterial community composition differed in both size fractions, as well as along the salinity gradient over time. Finally, genus‐specific core microbiomes were identified and conserved even under highly stressful conditions, suggesting interactions that support community stability and resilience.
This study demonstrated the strong halotolerance of natural Microcystis colonies, which was associated with the production of osmolytes. Bacterial community composition was primarily structured by salinity, followed by time, and differed between the attached and free fractions. The identified attached core microbiomes were genus‐specific and conserved across the salinity gradient, even under highly stressful conditions. These results suggest interactions within the cyanosphere that support community stability and resilience. |
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This study demonstrated the strong halotolerance of natural Microcystis colonies, which was associated with the production of osmolytes. Bacterial community composition was primarily structured by salinity, followed by time, and differed between the attached and free fractions. The identified attached core microbiomes were genus‐specific and conserved across the salinity gradient, even under highly stressful conditions. These results suggest interactions within the cyanosphere that support community stability and resilience.</description><identifier>ISSN: 1758-2229</identifier><identifier>EISSN: 1758-2229</identifier><identifier>DOI: 10.1111/1758-2229.70029</identifier><identifier>PMID: 39444304</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Biodiversity and Ecology ; Cyanobacteria ; Cyanobacteria - classification ; Cyanobacteria - genetics ; Cyanobacteria - growth & development ; Cyanobacteria - metabolism ; Environmental Sciences ; Fresh Water ; Fresh Water - chemistry ; Fresh Water - microbiology ; Microbiota ; Microcystins ; Microcystins - metabolism ; Microcystis ; Microcystis - genetics ; Microcystis - growth & development ; Microcystis - metabolism ; Nutrients ; Nutrients - metabolism ; Salinity ; Stress, Physiological</subject><ispartof>Environmental microbiology reports, 2024-10, Vol.16 (5), p.e70029-n/a</ispartof><rights>2024 The Author(s). published by John Wiley & Sons Ltd.</rights><rights>2024 The Author(s). Environmental Microbiology Reports published by John Wiley & Sons Ltd.</rights><rights>Attribution</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3599-be2ccd165deb5b5ce98e23319f87740683b2356e369ba65c302f7614fe1b1d103</cites><orcidid>0000-0001-8996-0072 ; 0000-0002-4755-6327</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1758-2229.70029$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1758-2229.70029$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,11562,27924,27925,46052,46476</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39444304$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://univ-rennes.hal.science/hal-04765212$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Reignier, Océane</creatorcontrib><creatorcontrib>Briand, Enora</creatorcontrib><creatorcontrib>Hervé, Fabienne</creatorcontrib><creatorcontrib>Robert, Elise</creatorcontrib><creatorcontrib>Savar, Véronique</creatorcontrib><creatorcontrib>Tanniou, Simon</creatorcontrib><creatorcontrib>Amzil, Zouher</creatorcontrib><creatorcontrib>Noël, Cyril</creatorcontrib><creatorcontrib>Bormans, Myriam</creatorcontrib><title>Effects of salinity and nutrient stress on a toxic freshwater cyanobacterial community and its associated microbiome: An experimental study</title><title>Environmental microbiology reports</title><addtitle>Environ Microbiol Rep</addtitle><description>We aimed to evaluate the ability of naturally occurring colonies of Microcystis, embedded in a thick mucilage, to persist in estuarine waters. In two batch experiments, we examined the dynamics of microbial communities, including cyanobacteria and associated heterotrophic bacteria, sampled from the field during both a cyanobacterial bloom (non‐limiting nutrient condition) and the post‐bloom period (limiting nutrient condition), and subjected them to a salinity gradient representative of the freshwater‐marine continuum. We demonstrated that both Microcystis aeruginosa and M. wesenbergii survived high salinities due to osmolyte accumulation. Specifically, prolonged exposure to high salinity led to betaine accumulation in the cyanobacterial biomass. The relative abundance of the mcyB gene remained around 30%, suggesting no selection for toxic genotypes with salinity or nutrient changes. Microcystins were predominantly intracellular, except at high salinity levels (>15), where more than 50% of the total microcystin concentration was extracellular. In both nutrient conditions, over 70% of the heterotrophic bacterial community belonged to the Gammaproteobacteria family, followed by the Bacteroidota. Bacterial community composition differed in both size fractions, as well as along the salinity gradient over time. Finally, genus‐specific core microbiomes were identified and conserved even under highly stressful conditions, suggesting interactions that support community stability and resilience.
This study demonstrated the strong halotolerance of natural Microcystis colonies, which was associated with the production of osmolytes. Bacterial community composition was primarily structured by salinity, followed by time, and differed between the attached and free fractions. The identified attached core microbiomes were genus‐specific and conserved across the salinity gradient, even under highly stressful conditions. These results suggest interactions within the cyanosphere that support community stability and resilience.</description><subject>Biodiversity and Ecology</subject><subject>Cyanobacteria</subject><subject>Cyanobacteria - classification</subject><subject>Cyanobacteria - genetics</subject><subject>Cyanobacteria - growth & development</subject><subject>Cyanobacteria - metabolism</subject><subject>Environmental Sciences</subject><subject>Fresh Water</subject><subject>Fresh Water - chemistry</subject><subject>Fresh Water - microbiology</subject><subject>Microbiota</subject><subject>Microcystins</subject><subject>Microcystins - metabolism</subject><subject>Microcystis</subject><subject>Microcystis - genetics</subject><subject>Microcystis - growth & development</subject><subject>Microcystis - metabolism</subject><subject>Nutrients</subject><subject>Nutrients - metabolism</subject><subject>Salinity</subject><subject>Stress, Physiological</subject><issn>1758-2229</issn><issn>1758-2229</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNqFUUtv1DAQthCIloUzN-QjPWzrV5w1F7SqFlppERc4W7YzYY0Se4mdtvkN_Gm8pF21XPDFo5nvMfaH0FtKzmk5F7SuVkvGmDqvCWHqGTo9dp4_qk_Qq5R-EiKFIuwlOuFKCMGJOEW_N20LLiccW5xM54PPEzahwWHMg4eQccoDpDIP2OAc77zDbWnsbk2GAbvJhGiNK7U3HXax78ejhC-yJqXofME2uPduiNbHHj7gdcBwty-kvlgUYspjM71GL1rTJXhzfy_Q90-bb5dXy-3Xz9eX6-3S8UqppQXmXENl1YCtbOVArYBxTlW7qmtB5IpbxisJXCprZOU4YW0tqWiBWtpQwhfo46y7H20PjSsrDKbT-7KNGSYdjddPJ8Hv9I94oykVSsnitUBns8LuH97VeqsPPSJqWTHKbmjBvr93G-KvEVLWvU8Ous4EiGPSnDJCKlUIBXoxQ8tHpTRAe9SmRB_y1odE9SFR_Tfvwnj3-ClH_EPABSBnwK3vYPqfnt58uRaz8h_rIbg8</recordid><startdate>202410</startdate><enddate>202410</enddate><creator>Reignier, Océane</creator><creator>Briand, Enora</creator><creator>Hervé, Fabienne</creator><creator>Robert, Elise</creator><creator>Savar, Véronique</creator><creator>Tanniou, Simon</creator><creator>Amzil, Zouher</creator><creator>Noël, Cyril</creator><creator>Bormans, Myriam</creator><general>John Wiley & Sons, Inc</general><general>Wiley</general><scope>24P</scope><scope>WIN</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-8996-0072</orcidid><orcidid>https://orcid.org/0000-0002-4755-6327</orcidid></search><sort><creationdate>202410</creationdate><title>Effects of salinity and nutrient stress on a toxic freshwater cyanobacterial community and its associated microbiome: An experimental study</title><author>Reignier, Océane ; Briand, Enora ; Hervé, Fabienne ; Robert, Elise ; Savar, Véronique ; Tanniou, Simon ; Amzil, Zouher ; Noël, Cyril ; Bormans, Myriam</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3599-be2ccd165deb5b5ce98e23319f87740683b2356e369ba65c302f7614fe1b1d103</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Biodiversity and Ecology</topic><topic>Cyanobacteria</topic><topic>Cyanobacteria - classification</topic><topic>Cyanobacteria - genetics</topic><topic>Cyanobacteria - growth & development</topic><topic>Cyanobacteria - metabolism</topic><topic>Environmental Sciences</topic><topic>Fresh Water</topic><topic>Fresh Water - chemistry</topic><topic>Fresh Water - microbiology</topic><topic>Microbiota</topic><topic>Microcystins</topic><topic>Microcystins - metabolism</topic><topic>Microcystis</topic><topic>Microcystis - genetics</topic><topic>Microcystis - growth & development</topic><topic>Microcystis - metabolism</topic><topic>Nutrients</topic><topic>Nutrients - metabolism</topic><topic>Salinity</topic><topic>Stress, Physiological</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Reignier, Océane</creatorcontrib><creatorcontrib>Briand, Enora</creatorcontrib><creatorcontrib>Hervé, Fabienne</creatorcontrib><creatorcontrib>Robert, Elise</creatorcontrib><creatorcontrib>Savar, Véronique</creatorcontrib><creatorcontrib>Tanniou, Simon</creatorcontrib><creatorcontrib>Amzil, Zouher</creatorcontrib><creatorcontrib>Noël, Cyril</creatorcontrib><creatorcontrib>Bormans, Myriam</creatorcontrib><collection>Wiley-Blackwell Open Access Collection</collection><collection>Wiley Online Library Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Environmental microbiology reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Reignier, Océane</au><au>Briand, Enora</au><au>Hervé, Fabienne</au><au>Robert, Elise</au><au>Savar, Véronique</au><au>Tanniou, Simon</au><au>Amzil, Zouher</au><au>Noël, Cyril</au><au>Bormans, Myriam</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Effects of salinity and nutrient stress on a toxic freshwater cyanobacterial community and its associated microbiome: An experimental study</atitle><jtitle>Environmental microbiology reports</jtitle><addtitle>Environ Microbiol Rep</addtitle><date>2024-10</date><risdate>2024</risdate><volume>16</volume><issue>5</issue><spage>e70029</spage><epage>n/a</epage><pages>e70029-n/a</pages><issn>1758-2229</issn><eissn>1758-2229</eissn><abstract>We aimed to evaluate the ability of naturally occurring colonies of Microcystis, embedded in a thick mucilage, to persist in estuarine waters. In two batch experiments, we examined the dynamics of microbial communities, including cyanobacteria and associated heterotrophic bacteria, sampled from the field during both a cyanobacterial bloom (non‐limiting nutrient condition) and the post‐bloom period (limiting nutrient condition), and subjected them to a salinity gradient representative of the freshwater‐marine continuum. We demonstrated that both Microcystis aeruginosa and M. wesenbergii survived high salinities due to osmolyte accumulation. Specifically, prolonged exposure to high salinity led to betaine accumulation in the cyanobacterial biomass. The relative abundance of the mcyB gene remained around 30%, suggesting no selection for toxic genotypes with salinity or nutrient changes. Microcystins were predominantly intracellular, except at high salinity levels (>15), where more than 50% of the total microcystin concentration was extracellular. In both nutrient conditions, over 70% of the heterotrophic bacterial community belonged to the Gammaproteobacteria family, followed by the Bacteroidota. Bacterial community composition differed in both size fractions, as well as along the salinity gradient over time. Finally, genus‐specific core microbiomes were identified and conserved even under highly stressful conditions, suggesting interactions that support community stability and resilience.
This study demonstrated the strong halotolerance of natural Microcystis colonies, which was associated with the production of osmolytes. Bacterial community composition was primarily structured by salinity, followed by time, and differed between the attached and free fractions. The identified attached core microbiomes were genus‐specific and conserved across the salinity gradient, even under highly stressful conditions. These results suggest interactions within the cyanosphere that support community stability and resilience.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>39444304</pmid><doi>10.1111/1758-2229.70029</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0001-8996-0072</orcidid><orcidid>https://orcid.org/0000-0002-4755-6327</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Biodiversity and Ecology Cyanobacteria Cyanobacteria - classification Cyanobacteria - genetics Cyanobacteria - growth & development Cyanobacteria - metabolism Environmental Sciences Fresh Water Fresh Water - chemistry Fresh Water - microbiology Microbiota Microcystins Microcystins - metabolism Microcystis Microcystis - genetics Microcystis - growth & development Microcystis - metabolism Nutrients Nutrients - metabolism Salinity Stress, Physiological |
title | Effects of salinity and nutrient stress on a toxic freshwater cyanobacterial community and its associated microbiome: An experimental study |
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