Genome sequence of Xanthomonas fuscans subsp. fuscans strain 4834-R reveals that flagellar motility is not a general feature of xanthomonads

Xanthomonads are plant-associated bacteria responsible for diseases on economically important crops. Xanthomonas fuscans subsp. fuscans (Xff) is one of the causal agents of common bacterial blight of bean. In this study, the complete genome sequence of strain Xff 4834-R was determined and compared t...

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Veröffentlicht in:BMC genomics 2013-11, Vol.14 (1), p.761-761
Hauptverfasser: Darrasse, Armelle, Carrère, Sébastien, Barbe, Valérie, Boureau, Tristan, Arrieta-Ortiz, Mario L, Bonneau, Sophie, Briand, Martial, Brin, Chrystelle, Cociancich, Stéphane, Durand, Karine, Fouteau, Stéphanie, Gagnevin, Lionel, Guérin, Fabien, Guy, Endrick, Indiana, Arnaud, Koebnik, Ralf, Lauber, Emmanuelle, Munoz, Alejandra, Noël, Laurent D, Pieretti, Isabelle, Poussier, Stéphane, Pruvost, Olivier, Robène-Soustrade, Isabelle, Rott, Philippe, Royer, Monique, Serres-Giardi, Laurana, Szurek, Boris, van Sluys, Marie-Anne, Verdier, Valérie, Vernière, Christian, Arlat, Matthieu, Manceau, Charles, Jacques, Marie-Agnès
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container_title BMC genomics
container_volume 14
creator Darrasse, Armelle
Carrère, Sébastien
Barbe, Valérie
Boureau, Tristan
Arrieta-Ortiz, Mario L
Bonneau, Sophie
Briand, Martial
Brin, Chrystelle
Cociancich, Stéphane
Durand, Karine
Fouteau, Stéphanie
Gagnevin, Lionel
Guérin, Fabien
Guy, Endrick
Indiana, Arnaud
Koebnik, Ralf
Lauber, Emmanuelle
Munoz, Alejandra
Noël, Laurent D
Pieretti, Isabelle
Poussier, Stéphane
Pruvost, Olivier
Robène-Soustrade, Isabelle
Rott, Philippe
Royer, Monique
Serres-Giardi, Laurana
Szurek, Boris
van Sluys, Marie-Anne
Verdier, Valérie
Vernière, Christian
Arlat, Matthieu
Manceau, Charles
Jacques, Marie-Agnès
description Xanthomonads are plant-associated bacteria responsible for diseases on economically important crops. Xanthomonas fuscans subsp. fuscans (Xff) is one of the causal agents of common bacterial blight of bean. In this study, the complete genome sequence of strain Xff 4834-R was determined and compared to other Xanthomonas genome sequences. Comparative genomics analyses revealed core characteristics shared between Xff 4834-R and other xanthomonads including chemotaxis elements, two-component systems, TonB-dependent transporters, secretion systems (from T1SS to T6SS) and multiple effectors. For instance a repertoire of 29 Type 3 Effectors (T3Es) with two Transcription Activator-Like Effectors was predicted. Mobile elements were associated with major modifications in the genome structure and gene content in comparison to other Xanthomonas genomes. Notably, a deletion of 33 kbp affects flagellum biosynthesis in Xff 4834-R. The presence of a complete flagellar cluster was assessed in a collection of more than 300 strains representing different species and pathovars of Xanthomonas. Five percent of the tested strains presented a deletion in the flagellar cluster and were non-motile. Moreover, half of the Xff strains isolated from the same epidemic than 4834-R was non-motile and this ratio was conserved in the strains colonizing the next bean seed generations. This work describes the first genome of a Xanthomonas strain pathogenic on bean and reports the existence of non-motile xanthomonads belonging to different species and pathovars. Isolation of such Xff variants from a natural epidemic may suggest that flagellar motility is not a key function for in planta fitness.
doi_str_mv 10.1186/1471-2164-14-761
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Xanthomonas fuscans subsp. fuscans (Xff) is one of the causal agents of common bacterial blight of bean. In this study, the complete genome sequence of strain Xff 4834-R was determined and compared to other Xanthomonas genome sequences. Comparative genomics analyses revealed core characteristics shared between Xff 4834-R and other xanthomonads including chemotaxis elements, two-component systems, TonB-dependent transporters, secretion systems (from T1SS to T6SS) and multiple effectors. For instance a repertoire of 29 Type 3 Effectors (T3Es) with two Transcription Activator-Like Effectors was predicted. Mobile elements were associated with major modifications in the genome structure and gene content in comparison to other Xanthomonas genomes. Notably, a deletion of 33 kbp affects flagellum biosynthesis in Xff 4834-R. The presence of a complete flagellar cluster was assessed in a collection of more than 300 strains representing different species and pathovars of Xanthomonas. Five percent of the tested strains presented a deletion in the flagellar cluster and were non-motile. Moreover, half of the Xff strains isolated from the same epidemic than 4834-R was non-motile and this ratio was conserved in the strains colonizing the next bean seed generations. This work describes the first genome of a Xanthomonas strain pathogenic on bean and reports the existence of non-motile xanthomonads belonging to different species and pathovars. 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Xanthomonas fuscans subsp. fuscans (Xff) is one of the causal agents of common bacterial blight of bean. In this study, the complete genome sequence of strain Xff 4834-R was determined and compared to other Xanthomonas genome sequences. Comparative genomics analyses revealed core characteristics shared between Xff 4834-R and other xanthomonads including chemotaxis elements, two-component systems, TonB-dependent transporters, secretion systems (from T1SS to T6SS) and multiple effectors. For instance a repertoire of 29 Type 3 Effectors (T3Es) with two Transcription Activator-Like Effectors was predicted. Mobile elements were associated with major modifications in the genome structure and gene content in comparison to other Xanthomonas genomes. Notably, a deletion of 33 kbp affects flagellum biosynthesis in Xff 4834-R. The presence of a complete flagellar cluster was assessed in a collection of more than 300 strains representing different species and pathovars of Xanthomonas. Five percent of the tested strains presented a deletion in the flagellar cluster and were non-motile. Moreover, half of the Xff strains isolated from the same epidemic than 4834-R was non-motile and this ratio was conserved in the strains colonizing the next bean seed generations. This work describes the first genome of a Xanthomonas strain pathogenic on bean and reports the existence of non-motile xanthomonads belonging to different species and pathovars. 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Carrère, Sébastien ; Barbe, Valérie ; Boureau, Tristan ; Arrieta-Ortiz, Mario L ; Bonneau, Sophie ; Briand, Martial ; Brin, Chrystelle ; Cociancich, Stéphane ; Durand, Karine ; Fouteau, Stéphanie ; Gagnevin, Lionel ; Guérin, Fabien ; Guy, Endrick ; Indiana, Arnaud ; Koebnik, Ralf ; Lauber, Emmanuelle ; Munoz, Alejandra ; Noël, Laurent D ; Pieretti, Isabelle ; Poussier, Stéphane ; Pruvost, Olivier ; Robène-Soustrade, Isabelle ; Rott, Philippe ; Royer, Monique ; Serres-Giardi, Laurana ; Szurek, Boris ; van Sluys, Marie-Anne ; Verdier, Valérie ; Vernière, Christian ; Arlat, Matthieu ; Manceau, Charles ; Jacques, Marie-Agnès</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-b393t-3c94a2ebccf11cf4fad9f21d2601643c5617f01144a5d9830626cc341e56bf323</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Base Sequence</topic><topic>Evolution, Molecular</topic><topic>Fabaceae - genetics</topic><topic>Fabaceae - growth &amp; development</topic><topic>Fabaceae - microbiology</topic><topic>Flagella - genetics</topic><topic>Flagella - physiology</topic><topic>Genetic Fitness</topic><topic>Genome, Bacterial</topic><topic>Life Sciences</topic><topic>Phylogeny</topic><topic>Plant Diseases - genetics</topic><topic>Plant Diseases - microbiology</topic><topic>Seeds - genetics</topic><topic>Seeds - microbiology</topic><topic>Sequence Analysis, DNA</topic><topic>Vegetal Biology</topic><topic>Xanthomonas</topic><topic>Xanthomonas - classification</topic><topic>Xanthomonas - genetics</topic><topic>Xanthomonas - pathogenicity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Darrasse, Armelle</creatorcontrib><creatorcontrib>Carrère, Sébastien</creatorcontrib><creatorcontrib>Barbe, Valérie</creatorcontrib><creatorcontrib>Boureau, Tristan</creatorcontrib><creatorcontrib>Arrieta-Ortiz, Mario L</creatorcontrib><creatorcontrib>Bonneau, Sophie</creatorcontrib><creatorcontrib>Briand, Martial</creatorcontrib><creatorcontrib>Brin, Chrystelle</creatorcontrib><creatorcontrib>Cociancich, Stéphane</creatorcontrib><creatorcontrib>Durand, Karine</creatorcontrib><creatorcontrib>Fouteau, Stéphanie</creatorcontrib><creatorcontrib>Gagnevin, Lionel</creatorcontrib><creatorcontrib>Guérin, Fabien</creatorcontrib><creatorcontrib>Guy, Endrick</creatorcontrib><creatorcontrib>Indiana, Arnaud</creatorcontrib><creatorcontrib>Koebnik, Ralf</creatorcontrib><creatorcontrib>Lauber, Emmanuelle</creatorcontrib><creatorcontrib>Munoz, Alejandra</creatorcontrib><creatorcontrib>Noël, Laurent D</creatorcontrib><creatorcontrib>Pieretti, Isabelle</creatorcontrib><creatorcontrib>Poussier, Stéphane</creatorcontrib><creatorcontrib>Pruvost, Olivier</creatorcontrib><creatorcontrib>Robène-Soustrade, Isabelle</creatorcontrib><creatorcontrib>Rott, Philippe</creatorcontrib><creatorcontrib>Royer, Monique</creatorcontrib><creatorcontrib>Serres-Giardi, Laurana</creatorcontrib><creatorcontrib>Szurek, Boris</creatorcontrib><creatorcontrib>van Sluys, Marie-Anne</creatorcontrib><creatorcontrib>Verdier, Valérie</creatorcontrib><creatorcontrib>Vernière, Christian</creatorcontrib><creatorcontrib>Arlat, Matthieu</creatorcontrib><creatorcontrib>Manceau, Charles</creatorcontrib><creatorcontrib>Jacques, Marie-Agnès</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</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>BMC genomics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Darrasse, Armelle</au><au>Carrère, Sébastien</au><au>Barbe, Valérie</au><au>Boureau, Tristan</au><au>Arrieta-Ortiz, Mario L</au><au>Bonneau, Sophie</au><au>Briand, Martial</au><au>Brin, Chrystelle</au><au>Cociancich, Stéphane</au><au>Durand, Karine</au><au>Fouteau, Stéphanie</au><au>Gagnevin, Lionel</au><au>Guérin, Fabien</au><au>Guy, Endrick</au><au>Indiana, Arnaud</au><au>Koebnik, Ralf</au><au>Lauber, Emmanuelle</au><au>Munoz, Alejandra</au><au>Noël, Laurent D</au><au>Pieretti, Isabelle</au><au>Poussier, Stéphane</au><au>Pruvost, Olivier</au><au>Robène-Soustrade, Isabelle</au><au>Rott, Philippe</au><au>Royer, Monique</au><au>Serres-Giardi, Laurana</au><au>Szurek, Boris</au><au>van Sluys, Marie-Anne</au><au>Verdier, Valérie</au><au>Vernière, Christian</au><au>Arlat, Matthieu</au><au>Manceau, Charles</au><au>Jacques, Marie-Agnès</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genome sequence of Xanthomonas fuscans subsp. fuscans strain 4834-R reveals that flagellar motility is not a general feature of xanthomonads</atitle><jtitle>BMC genomics</jtitle><addtitle>BMC Genomics</addtitle><date>2013-11-06</date><risdate>2013</risdate><volume>14</volume><issue>1</issue><spage>761</spage><epage>761</epage><pages>761-761</pages><issn>1471-2164</issn><eissn>1471-2164</eissn><abstract>Xanthomonads are plant-associated bacteria responsible for diseases on economically important crops. Xanthomonas fuscans subsp. fuscans (Xff) is one of the causal agents of common bacterial blight of bean. In this study, the complete genome sequence of strain Xff 4834-R was determined and compared to other Xanthomonas genome sequences. Comparative genomics analyses revealed core characteristics shared between Xff 4834-R and other xanthomonads including chemotaxis elements, two-component systems, TonB-dependent transporters, secretion systems (from T1SS to T6SS) and multiple effectors. For instance a repertoire of 29 Type 3 Effectors (T3Es) with two Transcription Activator-Like Effectors was predicted. Mobile elements were associated with major modifications in the genome structure and gene content in comparison to other Xanthomonas genomes. Notably, a deletion of 33 kbp affects flagellum biosynthesis in Xff 4834-R. The presence of a complete flagellar cluster was assessed in a collection of more than 300 strains representing different species and pathovars of Xanthomonas. Five percent of the tested strains presented a deletion in the flagellar cluster and were non-motile. Moreover, half of the Xff strains isolated from the same epidemic than 4834-R was non-motile and this ratio was conserved in the strains colonizing the next bean seed generations. This work describes the first genome of a Xanthomonas strain pathogenic on bean and reports the existence of non-motile xanthomonads belonging to different species and pathovars. Isolation of such Xff variants from a natural epidemic may suggest that flagellar motility is not a key function for in planta fitness.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>24195767</pmid><doi>10.1186/1471-2164-14-761</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0001-6196-4856</orcidid><orcidid>https://orcid.org/0000-0002-0110-1423</orcidid><orcidid>https://orcid.org/0000-0001-6085-6159</orcidid><orcidid>https://orcid.org/0000-0003-4720-4951</orcidid><orcidid>https://orcid.org/0000-0002-2348-0778</orcidid><orcidid>https://orcid.org/0000-0002-2312-2073</orcidid><orcidid>https://orcid.org/0000-0003-0421-982X</orcidid><orcidid>https://orcid.org/0000-0002-4419-0542</orcidid><orcidid>https://orcid.org/0000-0002-9334-5862</orcidid><orcidid>https://orcid.org/0000-0001-5933-4476</orcidid><orcidid>https://orcid.org/0000-0002-5822-2824</orcidid><orcidid>https://orcid.org/0000-0002-1808-7082</orcidid><orcidid>https://orcid.org/0000-0001-5425-9454</orcidid><orcidid>https://orcid.org/0000-0002-8162-3343</orcidid><orcidid>https://orcid.org/0000-0002-1442-917X</orcidid><orcidid>https://orcid.org/0000-0001-6518-8401</orcidid><oa>free_for_read</oa></addata></record>
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subjects Base Sequence
Evolution, Molecular
Fabaceae - genetics
Fabaceae - growth & development
Fabaceae - microbiology
Flagella - genetics
Flagella - physiology
Genetic Fitness
Genome, Bacterial
Life Sciences
Phylogeny
Plant Diseases - genetics
Plant Diseases - microbiology
Seeds - genetics
Seeds - microbiology
Sequence Analysis, DNA
Vegetal Biology
Xanthomonas
Xanthomonas - classification
Xanthomonas - genetics
Xanthomonas - pathogenicity
title Genome sequence of Xanthomonas fuscans subsp. fuscans strain 4834-R reveals that flagellar motility is not a general feature of xanthomonads
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