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Discordant population structure among rhizobium divided genomes and their legume hosts
Symbiosis often occurs between partners with distinct life history characteristics and dispersal mechanisms. Many bacterial symbionts have genomes comprising multiple replicons with distinct rates of evolution and horizontal transmission. Such differences might drive differences in population struct...
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Published in: | Molecular ecology 2023-05, Vol.32 (10), p.2646-2659 |
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container_title | Molecular ecology |
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creator | Riley, Alex B. Grillo, Michael A. Epstein, Brendan Tiffin, Peter Heath, Katy D. |
description | Symbiosis often occurs between partners with distinct life history characteristics and dispersal mechanisms. Many bacterial symbionts have genomes comprising multiple replicons with distinct rates of evolution and horizontal transmission. Such differences might drive differences in population structure between hosts and symbionts and among the elements of the divided genomes of bacterial symbionts. These differences might, in turn, shape the evolution of symbiotic interactions and bacterial evolution. Here we use whole genome resequencing of a hierarchically structured sample of 191 strains of Sinorhizobium meliloti collected from 21 locations in southern Europe to characterize population structures of this bacterial symbiont, which forms a root nodule symbiosis with the host plant Medicago truncatula. S. meliloti genomes showed high local (within‐site) variation and little isolation by distance. This was particularly true for the two symbiosis elements, pSymA and pSymB, which have population structures that are similar to each other, but distinct from both the bacterial chromosome and the host plant. Given limited recombination on the chromosome, compared to the symbiosis elements, distinct population structures may result from differences in effective gene flow. Alternatively, positive or purifying selection, with little recombination, may explain distinct geographical patterns at the chromosome. Discordant population structure between hosts and symbionts indicates that geographically and genetically distinct host populations in different parts of the range might interact with genetically similar symbionts, potentially minimizing local specialization. |
doi_str_mv | 10.1111/mec.16704 |
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Many bacterial symbionts have genomes comprising multiple replicons with distinct rates of evolution and horizontal transmission. Such differences might drive differences in population structure between hosts and symbionts and among the elements of the divided genomes of bacterial symbionts. These differences might, in turn, shape the evolution of symbiotic interactions and bacterial evolution. Here we use whole genome resequencing of a hierarchically structured sample of 191 strains of Sinorhizobium meliloti collected from 21 locations in southern Europe to characterize population structures of this bacterial symbiont, which forms a root nodule symbiosis with the host plant Medicago truncatula. S. meliloti genomes showed high local (within‐site) variation and little isolation by distance. This was particularly true for the two symbiosis elements, pSymA and pSymB, which have population structures that are similar to each other, but distinct from both the bacterial chromosome and the host plant. Given limited recombination on the chromosome, compared to the symbiosis elements, distinct population structures may result from differences in effective gene flow. Alternatively, positive or purifying selection, with little recombination, may explain distinct geographical patterns at the chromosome. Discordant population structure between hosts and symbionts indicates that geographically and genetically distinct host populations in different parts of the range might interact with genetically similar symbionts, potentially minimizing local specialization.</description><identifier>ISSN: 0962-1083</identifier><identifier>EISSN: 1365-294X</identifier><identifier>DOI: 10.1111/mec.16704</identifier><identifier>PMID: 36161739</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Alfalfa ; Bacteria ; Chromosomes ; co‐evolution ; Dispersal ; Ensifer ; Evolution ; Gene flow ; Genome, Bacterial - genetics ; Genomes ; horizontal gene transfer ; Host plants ; Legumes ; Life history ; Medicago truncatula - genetics ; Medicago truncatula - microbiology ; MGE ; mutualism ; plasmid ; Population genetics ; Population structure ; Recombination ; Rhizobium - genetics ; Sequence Analysis, DNA ; Sinorhizobium meliloti - genetics ; Symbionts ; Symbiosis ; Symbiosis - genetics</subject><ispartof>Molecular ecology, 2023-05, Vol.32 (10), p.2646-2659</ispartof><rights>2022 The Authors. published by John Wiley & Sons Ltd.</rights><rights>2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.</rights><rights>2022. This article is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3884-ca3853740017705f03ed8aa54babffd383528dc94ce241fbe938f345717641363</citedby><cites>FETCH-LOGICAL-c3884-ca3853740017705f03ed8aa54babffd383528dc94ce241fbe938f345717641363</cites><orcidid>0000-0001-7083-1588 ; 0000-0003-1975-610X ; 0000-0002-6368-744X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36161739$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Riley, Alex B.</creatorcontrib><creatorcontrib>Grillo, Michael A.</creatorcontrib><creatorcontrib>Epstein, Brendan</creatorcontrib><creatorcontrib>Tiffin, Peter</creatorcontrib><creatorcontrib>Heath, Katy D.</creatorcontrib><title>Discordant population structure among rhizobium divided genomes and their legume hosts</title><title>Molecular ecology</title><addtitle>Mol Ecol</addtitle><description>Symbiosis often occurs between partners with distinct life history characteristics and dispersal mechanisms. Many bacterial symbionts have genomes comprising multiple replicons with distinct rates of evolution and horizontal transmission. Such differences might drive differences in population structure between hosts and symbionts and among the elements of the divided genomes of bacterial symbionts. These differences might, in turn, shape the evolution of symbiotic interactions and bacterial evolution. Here we use whole genome resequencing of a hierarchically structured sample of 191 strains of Sinorhizobium meliloti collected from 21 locations in southern Europe to characterize population structures of this bacterial symbiont, which forms a root nodule symbiosis with the host plant Medicago truncatula. S. meliloti genomes showed high local (within‐site) variation and little isolation by distance. This was particularly true for the two symbiosis elements, pSymA and pSymB, which have population structures that are similar to each other, but distinct from both the bacterial chromosome and the host plant. Given limited recombination on the chromosome, compared to the symbiosis elements, distinct population structures may result from differences in effective gene flow. Alternatively, positive or purifying selection, with little recombination, may explain distinct geographical patterns at the chromosome. Discordant population structure between hosts and symbionts indicates that geographically and genetically distinct host populations in different parts of the range might interact with genetically similar symbionts, potentially minimizing local specialization.</description><subject>Alfalfa</subject><subject>Bacteria</subject><subject>Chromosomes</subject><subject>co‐evolution</subject><subject>Dispersal</subject><subject>Ensifer</subject><subject>Evolution</subject><subject>Gene flow</subject><subject>Genome, Bacterial - genetics</subject><subject>Genomes</subject><subject>horizontal gene transfer</subject><subject>Host plants</subject><subject>Legumes</subject><subject>Life history</subject><subject>Medicago truncatula - genetics</subject><subject>Medicago truncatula - microbiology</subject><subject>MGE</subject><subject>mutualism</subject><subject>plasmid</subject><subject>Population genetics</subject><subject>Population structure</subject><subject>Recombination</subject><subject>Rhizobium - genetics</subject><subject>Sequence Analysis, DNA</subject><subject>Sinorhizobium meliloti - genetics</subject><subject>Symbionts</subject><subject>Symbiosis</subject><subject>Symbiosis - genetics</subject><issn>0962-1083</issn><issn>1365-294X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNp1kEtLxDAUhYMoOj4W_gEJuNFFNWmSNl3K-ATFjYq7kDa3M5G2GZNG0V9vdNSF4N3czcfhnA-hXUqOaLrjHpojWpSEr6AJZYXI8oo_rqIJqYo8o0SyDbQZwhMhlOVCrKMNVtCClqyaoIdTGxrnjR5GvHCL2OnRugGH0cdmjB6w7t0ww35u311tY4-NfbEGDJ7B4HoIWA8Gj3OwHncwiz3guQtj2EZrre4C7Hz_LXR_fnY3vcyuby-upifXWcOk5FmjmRSs5KlZWRLREgZGai14reu2NUwykUvTVLyBnNO2horJlnFR0rLgaSnbQgfL3IV3zxHCqPq0B7pOD-BiUHlJZcGJYHlC9_-gTy76IbVTuUwWBSXkkzpcUo13IXho1cLbXvs3RYn6lK2SbPUlO7F734mx7sH8kj92E3C8BF5tB2__J6mbs-ky8gNasogr</recordid><startdate>202305</startdate><enddate>202305</enddate><creator>Riley, Alex B.</creator><creator>Grillo, Michael A.</creator><creator>Epstein, Brendan</creator><creator>Tiffin, Peter</creator><creator>Heath, Katy D.</creator><general>Blackwell Publishing Ltd</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>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-7083-1588</orcidid><orcidid>https://orcid.org/0000-0003-1975-610X</orcidid><orcidid>https://orcid.org/0000-0002-6368-744X</orcidid></search><sort><creationdate>202305</creationdate><title>Discordant population structure among rhizobium divided genomes and their legume hosts</title><author>Riley, Alex B. ; Grillo, Michael A. ; Epstein, Brendan ; Tiffin, Peter ; Heath, Katy D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3884-ca3853740017705f03ed8aa54babffd383528dc94ce241fbe938f345717641363</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Alfalfa</topic><topic>Bacteria</topic><topic>Chromosomes</topic><topic>co‐evolution</topic><topic>Dispersal</topic><topic>Ensifer</topic><topic>Evolution</topic><topic>Gene flow</topic><topic>Genome, Bacterial - genetics</topic><topic>Genomes</topic><topic>horizontal gene transfer</topic><topic>Host plants</topic><topic>Legumes</topic><topic>Life history</topic><topic>Medicago truncatula - genetics</topic><topic>Medicago truncatula - microbiology</topic><topic>MGE</topic><topic>mutualism</topic><topic>plasmid</topic><topic>Population genetics</topic><topic>Population structure</topic><topic>Recombination</topic><topic>Rhizobium - genetics</topic><topic>Sequence Analysis, DNA</topic><topic>Sinorhizobium meliloti - genetics</topic><topic>Symbionts</topic><topic>Symbiosis</topic><topic>Symbiosis - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Riley, Alex B.</creatorcontrib><creatorcontrib>Grillo, Michael A.</creatorcontrib><creatorcontrib>Epstein, Brendan</creatorcontrib><creatorcontrib>Tiffin, Peter</creatorcontrib><creatorcontrib>Heath, Katy D.</creatorcontrib><collection>Wiley-Blackwell Open Access Titles(OpenAccess)</collection><collection>Wiley Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Riley, Alex B.</au><au>Grillo, Michael A.</au><au>Epstein, Brendan</au><au>Tiffin, Peter</au><au>Heath, Katy D.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Discordant population structure among rhizobium divided genomes and their legume hosts</atitle><jtitle>Molecular ecology</jtitle><addtitle>Mol Ecol</addtitle><date>2023-05</date><risdate>2023</risdate><volume>32</volume><issue>10</issue><spage>2646</spage><epage>2659</epage><pages>2646-2659</pages><issn>0962-1083</issn><eissn>1365-294X</eissn><abstract>Symbiosis often occurs between partners with distinct life history characteristics and dispersal mechanisms. Many bacterial symbionts have genomes comprising multiple replicons with distinct rates of evolution and horizontal transmission. Such differences might drive differences in population structure between hosts and symbionts and among the elements of the divided genomes of bacterial symbionts. These differences might, in turn, shape the evolution of symbiotic interactions and bacterial evolution. Here we use whole genome resequencing of a hierarchically structured sample of 191 strains of Sinorhizobium meliloti collected from 21 locations in southern Europe to characterize population structures of this bacterial symbiont, which forms a root nodule symbiosis with the host plant Medicago truncatula. S. meliloti genomes showed high local (within‐site) variation and little isolation by distance. This was particularly true for the two symbiosis elements, pSymA and pSymB, which have population structures that are similar to each other, but distinct from both the bacterial chromosome and the host plant. Given limited recombination on the chromosome, compared to the symbiosis elements, distinct population structures may result from differences in effective gene flow. Alternatively, positive or purifying selection, with little recombination, may explain distinct geographical patterns at the chromosome. 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subjects | Alfalfa Bacteria Chromosomes co‐evolution Dispersal Ensifer Evolution Gene flow Genome, Bacterial - genetics Genomes horizontal gene transfer Host plants Legumes Life history Medicago truncatula - genetics Medicago truncatula - microbiology MGE mutualism plasmid Population genetics Population structure Recombination Rhizobium - genetics Sequence Analysis, DNA Sinorhizobium meliloti - genetics Symbionts Symbiosis Symbiosis - genetics |
title | Discordant population structure among rhizobium divided genomes and their legume hosts |
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