Photorhabdus phase variants express a novel fimbrial locus, mad, essential for symbiosis
Fimbriae are adhesive organelles known to enable pathogens to colonize animal tissue, but little is known of their function in mutualistic symbioses. Photorhabdus colonization of Heterorhabditis bacteriophora nematodes is essential for the pair's insect pathogenic lifestyle. Maternal nematodes...
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| Veröffentlicht in: | Molecular microbiology 2010-08, Vol.77 (4), p.1021-1038 |
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| creator | Somvanshi, Vishal S Kaufmann-Daszczuk, Bettina Kim, Kwi-suk Mallon, Shane Ciche, Todd A |
| description | Fimbriae are adhesive organelles known to enable pathogens to colonize animal tissue, but little is known of their function in mutualistic symbioses. Photorhabdus colonization of Heterorhabditis bacteriophora nematodes is essential for the pair's insect pathogenic lifestyle. Maternal nematodes acquire Photorhabdus symbionts as a persistent intestinal biofilm prior to transmission to infective juvenile (IJ) stage offspring developing inside the maternal body. Screening 8000 Photorhabdus mutants for defects in IJ colonization revealed that a single fimbrial locus, named mad for maternal adhesion defective, is essential. The mad genes encode a novel usher/chaperone assembled fimbria regulated by an ON/OFF invertible promoter switch. Adherent Photorhabdus cells in maternal nematode intestines had the switch ON opposite to the OFF orientation of most other cells. A ΔmadA mutant failed to adhere to maternal intestines and be transmitted to the IJs. Mad fimbriae were detected on TT01 phase ON cells but not on ΔmadA phase ON cells. Also required for transmission is madJ, predicted to encode a transcriptional activator related to GrlA. Expression of madA-K or madIJK restored the ability of madJ mutant to adhere. The Mad fimbriae were not required for insect pathogenesis, indicating the specialized function of Mad fimbriae for symbiosis. |
| doi_str_mv | 10.1111/j.1365-2958.2010.07270.x |
| format | Article |
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Photorhabdus colonization of Heterorhabditis bacteriophora nematodes is essential for the pair's insect pathogenic lifestyle. Maternal nematodes acquire Photorhabdus symbionts as a persistent intestinal biofilm prior to transmission to infective juvenile (IJ) stage offspring developing inside the maternal body. Screening 8000 Photorhabdus mutants for defects in IJ colonization revealed that a single fimbrial locus, named mad for maternal adhesion defective, is essential. The mad genes encode a novel usher/chaperone assembled fimbria regulated by an ON/OFF invertible promoter switch. Adherent Photorhabdus cells in maternal nematode intestines had the switch ON opposite to the OFF orientation of most other cells. A ΔmadA mutant failed to adhere to maternal intestines and be transmitted to the IJs. Mad fimbriae were detected on TT01 phase ON cells but not on ΔmadA phase ON cells. Also required for transmission is madJ, predicted to encode a transcriptional activator related to GrlA. Expression of madA-K or madIJK restored the ability of madJ mutant to adhere. The Mad fimbriae were not required for insect pathogenesis, indicating the specialized function of Mad fimbriae for symbiosis.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/j.1365-2958.2010.07270.x</identifier><identifier>PMID: 20572934</identifier><language>eng</language><publisher>Oxford, UK: Oxford, UK : Blackwell Publishing Ltd</publisher><subject>Animals ; Bacterial Adhesion ; Bacteriology ; Biofilms - growth & development ; Biological and medical sciences ; Fimbriae Proteins - genetics ; Fimbriae Proteins - metabolism ; Fundamental and applied biological sciences. 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Photorhabdus colonization of Heterorhabditis bacteriophora nematodes is essential for the pair's insect pathogenic lifestyle. Maternal nematodes acquire Photorhabdus symbionts as a persistent intestinal biofilm prior to transmission to infective juvenile (IJ) stage offspring developing inside the maternal body. Screening 8000 Photorhabdus mutants for defects in IJ colonization revealed that a single fimbrial locus, named mad for maternal adhesion defective, is essential. The mad genes encode a novel usher/chaperone assembled fimbria regulated by an ON/OFF invertible promoter switch. Adherent Photorhabdus cells in maternal nematode intestines had the switch ON opposite to the OFF orientation of most other cells. A ΔmadA mutant failed to adhere to maternal intestines and be transmitted to the IJs. Mad fimbriae were detected on TT01 phase ON cells but not on ΔmadA phase ON cells. Also required for transmission is madJ, predicted to encode a transcriptional activator related to GrlA. Expression of madA-K or madIJK restored the ability of madJ mutant to adhere. The Mad fimbriae were not required for insect pathogenesis, indicating the specialized function of Mad fimbriae for symbiosis.</description><subject>Animals</subject><subject>Bacterial Adhesion</subject><subject>Bacteriology</subject><subject>Biofilms - growth & development</subject><subject>Biological and medical sciences</subject><subject>Fimbriae Proteins - genetics</subject><subject>Fimbriae Proteins - metabolism</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gastrointestinal Tract - microbiology</subject><subject>Gene Deletion</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Genes, Bacterial</subject><subject>Genetic Loci</subject><subject>Microbiology</subject><subject>Miscellaneous</subject><subject>Multigene Family</subject><subject>Mutation</subject><subject>Nematodes</subject><subject>Operon</subject><subject>Pathogenesis</subject><subject>Photorhabdus - genetics</subject><subject>Photorhabdus - physiology</subject><subject>Promoter Regions, Genetic</subject><subject>Rhabditoidea - growth & development</subject><subject>Rhabditoidea - microbiology</subject><subject>Symbiosis</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkU1v1DAQhi0EotvCXwALCamHZvFH7NgHDqjio1IrkKBSb9YksdmsknjxbMruv8dhlyJxwhePZp53ZvyaEMrZkufzZr3kUqtCWGWWguUsq0TFlrtHZPFQeEwWzCpWSCPuTsgp4poxLpmWT8mJYKoSVpYLcvdlFbcxraBuJ6SbFaCn95A6GLdI_W6TPCIFOsZ739PQDXUu9bSPzYQXdID2gmbAj9s5G2KiuB_qLmKHz8iTAD3658f7jNx-eP_t8lNx_fnj1eW766JRWrOCK-YNKNNqI1kZIFSaC6MEKN42dY4k97rSulJl64M1wbYghfamVNJ7HuQZOT_03aT4Y_K4dUOHje97GH2c0PHceH6sVRl99Q-6jlMa83auKpUtteU2Q-YANSkiJh_cJnUDpL3jzM3mu7WbPXazx2423_023-2y9MWx_1QPvn0Q_nE7A6-PAGADfUgwNh3-5SQzhpuZe3vgfna93__3Au7m5mqOsv7lQR8gOvie8ozbr2L-fW6q0jIjfwFp-agH</recordid><startdate>201008</startdate><enddate>201008</enddate><creator>Somvanshi, Vishal S</creator><creator>Kaufmann-Daszczuk, Bettina</creator><creator>Kim, Kwi-suk</creator><creator>Mallon, Shane</creator><creator>Ciche, Todd A</creator><general>Oxford, UK : Blackwell Publishing Ltd</general><general>Blackwell Publishing Ltd</general><general>Blackwell</general><scope>FBQ</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>201008</creationdate><title>Photorhabdus phase variants express a novel fimbrial locus, mad, essential for symbiosis</title><author>Somvanshi, Vishal S ; Kaufmann-Daszczuk, Bettina ; Kim, Kwi-suk ; Mallon, Shane ; Ciche, Todd A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5660-150e8a58d68304faf7612852a51dcb28531e6766754def98f9da326e8453ee1f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Animals</topic><topic>Bacterial Adhesion</topic><topic>Bacteriology</topic><topic>Biofilms - growth & development</topic><topic>Biological and medical sciences</topic><topic>Fimbriae Proteins - genetics</topic><topic>Fimbriae Proteins - metabolism</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gastrointestinal Tract - microbiology</topic><topic>Gene Deletion</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Genes, Bacterial</topic><topic>Genetic Loci</topic><topic>Microbiology</topic><topic>Miscellaneous</topic><topic>Multigene Family</topic><topic>Mutation</topic><topic>Nematodes</topic><topic>Operon</topic><topic>Pathogenesis</topic><topic>Photorhabdus - genetics</topic><topic>Photorhabdus - physiology</topic><topic>Promoter Regions, Genetic</topic><topic>Rhabditoidea - growth & development</topic><topic>Rhabditoidea - microbiology</topic><topic>Symbiosis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Somvanshi, Vishal S</creatorcontrib><creatorcontrib>Kaufmann-Daszczuk, Bettina</creatorcontrib><creatorcontrib>Kim, Kwi-suk</creatorcontrib><creatorcontrib>Mallon, Shane</creatorcontrib><creatorcontrib>Ciche, Todd A</creatorcontrib><collection>AGRIS</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 & 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>Somvanshi, Vishal S</au><au>Kaufmann-Daszczuk, Bettina</au><au>Kim, Kwi-suk</au><au>Mallon, Shane</au><au>Ciche, Todd A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Photorhabdus phase variants express a novel fimbrial locus, mad, essential for symbiosis</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2010-08</date><risdate>2010</risdate><volume>77</volume><issue>4</issue><spage>1021</spage><epage>1038</epage><pages>1021-1038</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Fimbriae are adhesive organelles known to enable pathogens to colonize animal tissue, but little is known of their function in mutualistic symbioses. Photorhabdus colonization of Heterorhabditis bacteriophora nematodes is essential for the pair's insect pathogenic lifestyle. Maternal nematodes acquire Photorhabdus symbionts as a persistent intestinal biofilm prior to transmission to infective juvenile (IJ) stage offspring developing inside the maternal body. Screening 8000 Photorhabdus mutants for defects in IJ colonization revealed that a single fimbrial locus, named mad for maternal adhesion defective, is essential. The mad genes encode a novel usher/chaperone assembled fimbria regulated by an ON/OFF invertible promoter switch. Adherent Photorhabdus cells in maternal nematode intestines had the switch ON opposite to the OFF orientation of most other cells. A ΔmadA mutant failed to adhere to maternal intestines and be transmitted to the IJs. Mad fimbriae were detected on TT01 phase ON cells but not on ΔmadA phase ON cells. Also required for transmission is madJ, predicted to encode a transcriptional activator related to GrlA. Expression of madA-K or madIJK restored the ability of madJ mutant to adhere. The Mad fimbriae were not required for insect pathogenesis, indicating the specialized function of Mad fimbriae for symbiosis.</abstract><cop>Oxford, UK</cop><pub>Oxford, UK : Blackwell Publishing Ltd</pub><pmid>20572934</pmid><doi>10.1111/j.1365-2958.2010.07270.x</doi><tpages>18</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Bacterial Adhesion Bacteriology Biofilms - growth & development Biological and medical sciences Fimbriae Proteins - genetics Fimbriae Proteins - metabolism Fundamental and applied biological sciences. Psychology Gastrointestinal Tract - microbiology Gene Deletion Gene expression Gene Expression Regulation, Bacterial Genes, Bacterial Genetic Loci Microbiology Miscellaneous Multigene Family Mutation Nematodes Operon Pathogenesis Photorhabdus - genetics Photorhabdus - physiology Promoter Regions, Genetic Rhabditoidea - growth & development Rhabditoidea - microbiology Symbiosis |
| title | Photorhabdus phase variants express a novel fimbrial locus, mad, essential for symbiosis |
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