The genetic and structural basis of two distinct terminal side branch residues in stewartan and amylovoran exopolysaccharides and their potential role in host adaptation

Summary Stewartan and amylovoran exopolysaccharide (EPS) produced by the plant pathogenic bacteria Pantoea stewartii and Erwinia amylovora are virulence factors in the cause of Stewart's vascular wilt and fire blight. The biosynthesis of amylovoran and stewartan is encoded by a set of homologou...

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Veröffentlicht in:Molecular microbiology 2012-01, Vol.83 (1), p.195-207
Hauptverfasser: Wang, Xiaolei, Yang, Fan, von Bodman, Susanne B.
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description Summary Stewartan and amylovoran exopolysaccharide (EPS) produced by the plant pathogenic bacteria Pantoea stewartii and Erwinia amylovora are virulence factors in the cause of Stewart's vascular wilt and fire blight. The biosynthesis of amylovoran and stewartan is encoded by a set of homologous operons that have been partially characterized, although some annotations are solely on the basis of sequence homology. The major distinguishing features of these two EPS forms are the presence of a terminal pyruvate in amylovoran and glucose in stewartan, even though the gene systems to account for both are conserved and present in each bacterium. This study explores the genetic, structural and functional differences of amylovoran and stewartan, and their potential role in host adaptation. We report that the pyruvyl transferase gene in P. stewartii is non‐functional, while the terminal glucosyl transferase is catalytically active. Conversely, in E. amylovora, the homologous glucosyl transferase activity appears to be relatively ineffective, while the pyruvyl transferase function predominates. We also show that the terminally pyruvylated versus glucosylated EPS require specific repeating unit translocases (Wzx). We discuss the evolutionary, functional and biological implications of the terminally pyruvylated and glucosylated polymers and their potential contribution to plant and insect host adaptation.
doi_str_mv 10.1111/j.1365-2958.2011.07926.x
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The biosynthesis of amylovoran and stewartan is encoded by a set of homologous operons that have been partially characterized, although some annotations are solely on the basis of sequence homology. The major distinguishing features of these two EPS forms are the presence of a terminal pyruvate in amylovoran and glucose in stewartan, even though the gene systems to account for both are conserved and present in each bacterium. This study explores the genetic, structural and functional differences of amylovoran and stewartan, and their potential role in host adaptation. We report that the pyruvyl transferase gene in P. stewartii is non‐functional, while the terminal glucosyl transferase is catalytically active. Conversely, in E. amylovora, the homologous glucosyl transferase activity appears to be relatively ineffective, while the pyruvyl transferase function predominates. We also show that the terminally pyruvylated versus glucosylated EPS require specific repeating unit translocases (Wzx). We discuss the evolutionary, functional and biological implications of the terminally pyruvylated and glucosylated polymers and their potential contribution to plant and insect host adaptation.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/j.1365-2958.2011.07926.x</identifier><identifier>PMID: 22111898</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Amino Acid Sequence ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Biological and medical sciences ; Biosynthesis ; Carbohydrate Sequence ; Erwinia - genetics ; Erwinia - metabolism ; Erwinia - pathogenicity ; Erwinia amylovora ; Evolutionary biology ; Flowers &amp; plants ; Fundamental and applied biological sciences. Psychology ; Genetics ; Gram-negative bacteria ; Malus - microbiology ; Microbiology ; Molecular Sequence Data ; Operon ; Pantoea - genetics ; Pantoea - metabolism ; Pantoea - pathogenicity ; Pantoea stewartii ; Plant Diseases - microbiology ; Polysaccharides, Bacterial - biosynthesis ; Polysaccharides, Bacterial - chemistry ; Sequence Alignment ; Virulence ; Zea mays - microbiology</subject><ispartof>Molecular microbiology, 2012-01, Vol.83 (1), p.195-207</ispartof><rights>2011 Blackwell Publishing Ltd</rights><rights>2015 INIST-CNRS</rights><rights>2011 Blackwell Publishing Ltd.</rights><rights>Copyright Blackwell Publishing Ltd. 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The biosynthesis of amylovoran and stewartan is encoded by a set of homologous operons that have been partially characterized, although some annotations are solely on the basis of sequence homology. The major distinguishing features of these two EPS forms are the presence of a terminal pyruvate in amylovoran and glucose in stewartan, even though the gene systems to account for both are conserved and present in each bacterium. This study explores the genetic, structural and functional differences of amylovoran and stewartan, and their potential role in host adaptation. We report that the pyruvyl transferase gene in P. stewartii is non‐functional, while the terminal glucosyl transferase is catalytically active. Conversely, in E. amylovora, the homologous glucosyl transferase activity appears to be relatively ineffective, while the pyruvyl transferase function predominates. We also show that the terminally pyruvylated versus glucosylated EPS require specific repeating unit translocases (Wzx). We discuss the evolutionary, functional and biological implications of the terminally pyruvylated and glucosylated polymers and their potential contribution to plant and insect host adaptation.</description><subject>Amino Acid Sequence</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Biological and medical sciences</subject><subject>Biosynthesis</subject><subject>Carbohydrate Sequence</subject><subject>Erwinia - genetics</subject><subject>Erwinia - metabolism</subject><subject>Erwinia - pathogenicity</subject><subject>Erwinia amylovora</subject><subject>Evolutionary biology</subject><subject>Flowers &amp; plants</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Genetics</subject><subject>Gram-negative bacteria</subject><subject>Malus - microbiology</subject><subject>Microbiology</subject><subject>Molecular Sequence Data</subject><subject>Operon</subject><subject>Pantoea - genetics</subject><subject>Pantoea - metabolism</subject><subject>Pantoea - pathogenicity</subject><subject>Pantoea stewartii</subject><subject>Plant Diseases - microbiology</subject><subject>Polysaccharides, Bacterial - biosynthesis</subject><subject>Polysaccharides, Bacterial - chemistry</subject><subject>Sequence Alignment</subject><subject>Virulence</subject><subject>Zea mays - microbiology</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkkGP1CAYhhujcWdX_4IhJsa9dKTQUjh4WEddN9nVyxiNF0LpV8vYlhGoM_OT_JfSmXFMPBi5FMLzPgHeJgnK8DyL48VqnlFWpEQUfE5wls1xKQibb-8ls9PG_WSGRYFTysnns-Tc-xXGGcWMPkzOCIkWLvgs-blsAX2FAYLRSA018sGNOoxOdahS3nhkGxQ2FtXGBzPogAK43gxx25saUOXUoFvkIK5G8MgM0QAb5YIa9j7V7zr7w0YMwdaubbfzSutWuZj2eyK0YBxa2wBDMNHrbAeTp7U-IFWrdVDB2OFR8qBRnYfHx-9F8vHtm-XiXXr74fpmcXWb6iJnLFUgKkUb3uiy4mXBRV02VGjNC0GBMVpWFTQ607QCIKzSVa5yUWicaSh4Xtb0Inl-8K6d_R6vFGRvvIauUwPY0UuREZbjkpNIXv6TzDDhsZic5RF9-he6sqOLr7j38VwQgiPED5B21nsHjVw70yu3iyY59S5XcqpXTvXKqXe5711uY_TJ0T9WPdSn4O-iI_DsCCivVddMtRn_hytoToWgkXt54Damg91_H0De3d1Ms5hPD_n4u8D2lFfum2QlLQv56f21pItX7DXGX-SS_gIj_NxS</recordid><startdate>201201</startdate><enddate>201201</enddate><creator>Wang, Xiaolei</creator><creator>Yang, Fan</creator><creator>von Bodman, Susanne B.</creator><general>Blackwell Publishing Ltd</general><general>Blackwell</general><scope>BSCLL</scope><scope>IQODW</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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>201201</creationdate><title>The genetic and structural basis of two distinct terminal side branch residues in stewartan and amylovoran exopolysaccharides and their potential role in host adaptation</title><author>Wang, Xiaolei ; Yang, Fan ; von Bodman, Susanne B.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5466-ae9ba3f8fc7b87589d7f39cc8593e6637bbefc1c3bee26bcb4a495c01ce5847d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Amino Acid Sequence</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Biological and medical sciences</topic><topic>Biosynthesis</topic><topic>Carbohydrate Sequence</topic><topic>Erwinia - genetics</topic><topic>Erwinia - metabolism</topic><topic>Erwinia - pathogenicity</topic><topic>Erwinia amylovora</topic><topic>Evolutionary biology</topic><topic>Flowers &amp; plants</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Genetics</topic><topic>Gram-negative bacteria</topic><topic>Malus - microbiology</topic><topic>Microbiology</topic><topic>Molecular Sequence Data</topic><topic>Operon</topic><topic>Pantoea - genetics</topic><topic>Pantoea - metabolism</topic><topic>Pantoea - pathogenicity</topic><topic>Pantoea stewartii</topic><topic>Plant Diseases - microbiology</topic><topic>Polysaccharides, Bacterial - biosynthesis</topic><topic>Polysaccharides, Bacterial - chemistry</topic><topic>Sequence Alignment</topic><topic>Virulence</topic><topic>Zea mays - microbiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Xiaolei</creatorcontrib><creatorcontrib>Yang, Fan</creatorcontrib><creatorcontrib>von Bodman, Susanne B.</creatorcontrib><collection>Istex</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</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 microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Xiaolei</au><au>Yang, Fan</au><au>von Bodman, Susanne B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The genetic and structural basis of two distinct terminal side branch residues in stewartan and amylovoran exopolysaccharides and their potential role in host adaptation</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2012-01</date><risdate>2012</risdate><volume>83</volume><issue>1</issue><spage>195</spage><epage>207</epage><pages>195-207</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Summary Stewartan and amylovoran exopolysaccharide (EPS) produced by the plant pathogenic bacteria Pantoea stewartii and Erwinia amylovora are virulence factors in the cause of Stewart's vascular wilt and fire blight. The biosynthesis of amylovoran and stewartan is encoded by a set of homologous operons that have been partially characterized, although some annotations are solely on the basis of sequence homology. The major distinguishing features of these two EPS forms are the presence of a terminal pyruvate in amylovoran and glucose in stewartan, even though the gene systems to account for both are conserved and present in each bacterium. This study explores the genetic, structural and functional differences of amylovoran and stewartan, and their potential role in host adaptation. We report that the pyruvyl transferase gene in P. stewartii is non‐functional, while the terminal glucosyl transferase is catalytically active. Conversely, in E. amylovora, the homologous glucosyl transferase activity appears to be relatively ineffective, while the pyruvyl transferase function predominates. We also show that the terminally pyruvylated versus glucosylated EPS require specific repeating unit translocases (Wzx). We discuss the evolutionary, functional and biological implications of the terminally pyruvylated and glucosylated polymers and their potential contribution to plant and insect host adaptation.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>22111898</pmid><doi>10.1111/j.1365-2958.2011.07926.x</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record>
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subjects Amino Acid Sequence
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Biological and medical sciences
Biosynthesis
Carbohydrate Sequence
Erwinia - genetics
Erwinia - metabolism
Erwinia - pathogenicity
Erwinia amylovora
Evolutionary biology
Flowers & plants
Fundamental and applied biological sciences. Psychology
Genetics
Gram-negative bacteria
Malus - microbiology
Microbiology
Molecular Sequence Data
Operon
Pantoea - genetics
Pantoea - metabolism
Pantoea - pathogenicity
Pantoea stewartii
Plant Diseases - microbiology
Polysaccharides, Bacterial - biosynthesis
Polysaccharides, Bacterial - chemistry
Sequence Alignment
Virulence
Zea mays - microbiology
title The genetic and structural basis of two distinct terminal side branch residues in stewartan and amylovoran exopolysaccharides and their potential role in host adaptation
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