Role of the major determinant of polar flagellation FlhG in the endoflagella‐containing spirochete Leptospira
Spirochetes can be distinguished from other bacteria by their spiral‐shaped morphology and subpolar periplasmic flagella. This study focused on FlhF and FlhG, which control the spatial and numerical regulation of flagella in many exoflagellated bacteria, in the spirochete Leptospira. In contrast to...
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creator | Fule, Lenka Halifa, Ruben Fontana, Celia Sismeiro, Odile Legendre, Rachel Varet, Hugo Coppée, Jean‐Yves Murray, Gerald L. Adler, Ben Hendrixson, David R. Buschiazzo, Alejandro Guo, Shuaiqi Liu, Jun Picardeau, Mathieu |
description | Spirochetes can be distinguished from other bacteria by their spiral‐shaped morphology and subpolar periplasmic flagella. This study focused on FlhF and FlhG, which control the spatial and numerical regulation of flagella in many exoflagellated bacteria, in the spirochete Leptospira. In contrast to flhF which seems to be essential in Leptospira, we demonstrated that flhG− mutants in both the saprophyte L. biflexa and the pathogen L. interrogans were less motile than the wild‐type strains in gel‐like environments but not hyperflagellated as reported previously in other bacteria. Cryo‐electron tomography revealed that the distance between the flagellar basal body and the tip of the cell decreased significantly in the flhG− mutant in comparison to wild‐type and complemented strains. Additionally, comparative transcriptome analyses of L. biflexa flhG− and wild‐type strains showed that FlhG acts as a negative regulator of transcription of some flagellar genes. We found that the L. interrogans flhG− mutant was attenuated for virulence in the hamster model. Cross‐species complementation also showed that flhG is not interchangeable between species. Our results indicate that FlhF and FlhG in Leptospira contribute to governing cell motility but our data support the hypothesis that FlhF and FlhG function differently in each bacterial species, including among spirochetes.
Spirochetes are helical or flat wave‐shaped cells that possess a cellular ultrastructure unique to bacteria: internal organelles of motility, called periplasmic flagella, that are attached at each cell end. Here we describe the role of FlhG in the biogenesis and localization of periplasmic flagella in Leptospira spp. |
doi_str_mv | 10.1111/mmi.14831 |
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Spirochetes are helical or flat wave‐shaped cells that possess a cellular ultrastructure unique to bacteria: internal organelles of motility, called periplasmic flagella, that are attached at each cell end. Here we describe the role of FlhG in the biogenesis and localization of periplasmic flagella in Leptospira spp.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/mmi.14831</identifier><identifier>PMID: 34657338</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Bacteria ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Complementation ; Cryoelectron Microscopy ; endoflagellum ; Flagella ; Flagella - genetics ; Flagella - metabolism ; FlhG ; Gene Expression Profiling ; Gene Expression Regulation, Bacterial ; Genetic Complementation Test ; Humans ; Leptospira ; Leptospira - cytology ; Leptospira - genetics ; Leptospira - metabolism ; Leptospirosis - microbiology ; Life Sciences ; Monomeric GTP-Binding Proteins - genetics ; Monomeric GTP-Binding Proteins - metabolism ; Morphology ; motility ; Mutants ; Mutation ; Species ; Spirochaetales - genetics ; Spirochaetales - metabolism ; Spirochetes ; Strains (organisms) ; Transcription ; Transcriptomes ; Virulence</subject><ispartof>Molecular microbiology, 2021-11, Vol.116 (5), p.1392-1406</ispartof><rights>2021 John Wiley & Sons Ltd</rights><rights>2021 John Wiley & Sons Ltd.</rights><rights>Copyright © 2021 John Wiley & Sons Ltd</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4261-490adc42239a3deab6be3c0e9a86289497d4a241a8bd5d1d5b10c4113b16fa023</citedby><cites>FETCH-LOGICAL-c4261-490adc42239a3deab6be3c0e9a86289497d4a241a8bd5d1d5b10c4113b16fa023</cites><orcidid>0000-0002-5338-5579 ; 0000-0003-4113-4606 ; 0000-0002-5196-9431 ; 0000-0003-3980-4463 ; 0000-0002-2509-6526</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%2Fmmi.14831$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmmi.14831$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,776,780,881,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34657338$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://pasteur.hal.science/pasteur-03411258$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Fule, Lenka</creatorcontrib><creatorcontrib>Halifa, Ruben</creatorcontrib><creatorcontrib>Fontana, Celia</creatorcontrib><creatorcontrib>Sismeiro, Odile</creatorcontrib><creatorcontrib>Legendre, Rachel</creatorcontrib><creatorcontrib>Varet, Hugo</creatorcontrib><creatorcontrib>Coppée, Jean‐Yves</creatorcontrib><creatorcontrib>Murray, Gerald L.</creatorcontrib><creatorcontrib>Adler, Ben</creatorcontrib><creatorcontrib>Hendrixson, David R.</creatorcontrib><creatorcontrib>Buschiazzo, Alejandro</creatorcontrib><creatorcontrib>Guo, Shuaiqi</creatorcontrib><creatorcontrib>Liu, Jun</creatorcontrib><creatorcontrib>Picardeau, Mathieu</creatorcontrib><title>Role of the major determinant of polar flagellation FlhG in the endoflagella‐containing spirochete Leptospira</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Spirochetes can be distinguished from other bacteria by their spiral‐shaped morphology and subpolar periplasmic flagella. This study focused on FlhF and FlhG, which control the spatial and numerical regulation of flagella in many exoflagellated bacteria, in the spirochete Leptospira. In contrast to flhF which seems to be essential in Leptospira, we demonstrated that flhG− mutants in both the saprophyte L. biflexa and the pathogen L. interrogans were less motile than the wild‐type strains in gel‐like environments but not hyperflagellated as reported previously in other bacteria. Cryo‐electron tomography revealed that the distance between the flagellar basal body and the tip of the cell decreased significantly in the flhG− mutant in comparison to wild‐type and complemented strains. Additionally, comparative transcriptome analyses of L. biflexa flhG− and wild‐type strains showed that FlhG acts as a negative regulator of transcription of some flagellar genes. We found that the L. interrogans flhG− mutant was attenuated for virulence in the hamster model. Cross‐species complementation also showed that flhG is not interchangeable between species. Our results indicate that FlhF and FlhG in Leptospira contribute to governing cell motility but our data support the hypothesis that FlhF and FlhG function differently in each bacterial species, including among spirochetes.
Spirochetes are helical or flat wave‐shaped cells that possess a cellular ultrastructure unique to bacteria: internal organelles of motility, called periplasmic flagella, that are attached at each cell end. Here we describe the role of FlhG in the biogenesis and localization of periplasmic flagella in Leptospira spp.</description><subject>Bacteria</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Complementation</subject><subject>Cryoelectron Microscopy</subject><subject>endoflagellum</subject><subject>Flagella</subject><subject>Flagella - genetics</subject><subject>Flagella - metabolism</subject><subject>FlhG</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Genetic Complementation Test</subject><subject>Humans</subject><subject>Leptospira</subject><subject>Leptospira - cytology</subject><subject>Leptospira - genetics</subject><subject>Leptospira - metabolism</subject><subject>Leptospirosis - microbiology</subject><subject>Life Sciences</subject><subject>Monomeric GTP-Binding Proteins - genetics</subject><subject>Monomeric GTP-Binding Proteins - metabolism</subject><subject>Morphology</subject><subject>motility</subject><subject>Mutants</subject><subject>Mutation</subject><subject>Species</subject><subject>Spirochaetales - genetics</subject><subject>Spirochaetales - metabolism</subject><subject>Spirochetes</subject><subject>Strains (organisms)</subject><subject>Transcription</subject><subject>Transcriptomes</subject><subject>Virulence</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kc9q3DAQh0VpabZJD32BIuilPTiRLNmWjiHkH2wolBZyE2NLzmqRJVeyE3LrI-QZ8yTVxkkOheoiifnmY4YfQp8oOaT5HA2DPaRcMPoGrSirq6KUlXiLVkRWpGCivN5DH1LaEkIZqdl7tMd4XTWMiRUKP4IzOPR42hg8wDZErM1k4mA9-GlXGIODiHsHN8Y5mGzw-MxtzrH1Tz3G6_BSfPzz0AU_gfXW3-A02hi6TbbhtRmnsPvDAXrXg0vm4_O9j36dnf48uSjW388vT47XRcfLmhZcEtD5WTIJTBto69awjhgJoi6F5LLRHEpOQbS60lRXLSUdp5S1tO6BlGwfFYt3A06N0Q4Q71UAqy6O12qENJk5KsJyS1mJW5r5rws_xvB7NmlSg03dbilvwpxUphijgjR1Rr_8g27DHH3eJlOykYyzRmTq20J1MaQUTf86BSVql5rKqamn1DL7-dk4t4PRr-RLTBk4WoA768z9_03q6upyUf4F_4CiGg</recordid><startdate>202111</startdate><enddate>202111</enddate><creator>Fule, Lenka</creator><creator>Halifa, Ruben</creator><creator>Fontana, Celia</creator><creator>Sismeiro, Odile</creator><creator>Legendre, Rachel</creator><creator>Varet, Hugo</creator><creator>Coppée, Jean‐Yves</creator><creator>Murray, Gerald L.</creator><creator>Adler, Ben</creator><creator>Hendrixson, David R.</creator><creator>Buschiazzo, Alejandro</creator><creator>Guo, Shuaiqi</creator><creator>Liu, Jun</creator><creator>Picardeau, Mathieu</creator><general>Blackwell Publishing Ltd</general><general>Wiley</general><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><scope>1XC</scope><orcidid>https://orcid.org/0000-0002-5338-5579</orcidid><orcidid>https://orcid.org/0000-0003-4113-4606</orcidid><orcidid>https://orcid.org/0000-0002-5196-9431</orcidid><orcidid>https://orcid.org/0000-0003-3980-4463</orcidid><orcidid>https://orcid.org/0000-0002-2509-6526</orcidid></search><sort><creationdate>202111</creationdate><title>Role of the major determinant of polar flagellation FlhG in the endoflagella‐containing spirochete Leptospira</title><author>Fule, Lenka ; Halifa, Ruben ; Fontana, Celia ; Sismeiro, Odile ; Legendre, Rachel ; Varet, Hugo ; Coppée, Jean‐Yves ; Murray, Gerald L. ; Adler, Ben ; Hendrixson, David R. ; Buschiazzo, Alejandro ; Guo, Shuaiqi ; Liu, Jun ; Picardeau, Mathieu</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4261-490adc42239a3deab6be3c0e9a86289497d4a241a8bd5d1d5b10c4113b16fa023</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Bacteria</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Complementation</topic><topic>Cryoelectron Microscopy</topic><topic>endoflagellum</topic><topic>Flagella</topic><topic>Flagella - genetics</topic><topic>Flagella - metabolism</topic><topic>FlhG</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Genetic Complementation Test</topic><topic>Humans</topic><topic>Leptospira</topic><topic>Leptospira - cytology</topic><topic>Leptospira - genetics</topic><topic>Leptospira - metabolism</topic><topic>Leptospirosis - microbiology</topic><topic>Life Sciences</topic><topic>Monomeric GTP-Binding Proteins - genetics</topic><topic>Monomeric GTP-Binding Proteins - metabolism</topic><topic>Morphology</topic><topic>motility</topic><topic>Mutants</topic><topic>Mutation</topic><topic>Species</topic><topic>Spirochaetales - genetics</topic><topic>Spirochaetales - metabolism</topic><topic>Spirochetes</topic><topic>Strains (organisms)</topic><topic>Transcription</topic><topic>Transcriptomes</topic><topic>Virulence</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Fule, Lenka</creatorcontrib><creatorcontrib>Halifa, Ruben</creatorcontrib><creatorcontrib>Fontana, Celia</creatorcontrib><creatorcontrib>Sismeiro, Odile</creatorcontrib><creatorcontrib>Legendre, Rachel</creatorcontrib><creatorcontrib>Varet, Hugo</creatorcontrib><creatorcontrib>Coppée, Jean‐Yves</creatorcontrib><creatorcontrib>Murray, Gerald L.</creatorcontrib><creatorcontrib>Adler, Ben</creatorcontrib><creatorcontrib>Hendrixson, David R.</creatorcontrib><creatorcontrib>Buschiazzo, Alejandro</creatorcontrib><creatorcontrib>Guo, Shuaiqi</creatorcontrib><creatorcontrib>Liu, Jun</creatorcontrib><creatorcontrib>Picardeau, Mathieu</creatorcontrib><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><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fule, Lenka</au><au>Halifa, Ruben</au><au>Fontana, Celia</au><au>Sismeiro, Odile</au><au>Legendre, Rachel</au><au>Varet, Hugo</au><au>Coppée, Jean‐Yves</au><au>Murray, Gerald L.</au><au>Adler, Ben</au><au>Hendrixson, David R.</au><au>Buschiazzo, Alejandro</au><au>Guo, Shuaiqi</au><au>Liu, Jun</au><au>Picardeau, Mathieu</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Role of the major determinant of polar flagellation FlhG in the endoflagella‐containing spirochete Leptospira</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2021-11</date><risdate>2021</risdate><volume>116</volume><issue>5</issue><spage>1392</spage><epage>1406</epage><pages>1392-1406</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Spirochetes can be distinguished from other bacteria by their spiral‐shaped morphology and subpolar periplasmic flagella. This study focused on FlhF and FlhG, which control the spatial and numerical regulation of flagella in many exoflagellated bacteria, in the spirochete Leptospira. In contrast to flhF which seems to be essential in Leptospira, we demonstrated that flhG− mutants in both the saprophyte L. biflexa and the pathogen L. interrogans were less motile than the wild‐type strains in gel‐like environments but not hyperflagellated as reported previously in other bacteria. Cryo‐electron tomography revealed that the distance between the flagellar basal body and the tip of the cell decreased significantly in the flhG− mutant in comparison to wild‐type and complemented strains. Additionally, comparative transcriptome analyses of L. biflexa flhG− and wild‐type strains showed that FlhG acts as a negative regulator of transcription of some flagellar genes. We found that the L. interrogans flhG− mutant was attenuated for virulence in the hamster model. Cross‐species complementation also showed that flhG is not interchangeable between species. Our results indicate that FlhF and FlhG in Leptospira contribute to governing cell motility but our data support the hypothesis that FlhF and FlhG function differently in each bacterial species, including among spirochetes.
Spirochetes are helical or flat wave‐shaped cells that possess a cellular ultrastructure unique to bacteria: internal organelles of motility, called periplasmic flagella, that are attached at each cell end. Here we describe the role of FlhG in the biogenesis and localization of periplasmic flagella in Leptospira spp.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>34657338</pmid><doi>10.1111/mmi.14831</doi><tpages>0</tpages><orcidid>https://orcid.org/0000-0002-5338-5579</orcidid><orcidid>https://orcid.org/0000-0003-4113-4606</orcidid><orcidid>https://orcid.org/0000-0002-5196-9431</orcidid><orcidid>https://orcid.org/0000-0003-3980-4463</orcidid><orcidid>https://orcid.org/0000-0002-2509-6526</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Bacteria Bacterial Proteins - genetics Bacterial Proteins - metabolism Complementation Cryoelectron Microscopy endoflagellum Flagella Flagella - genetics Flagella - metabolism FlhG Gene Expression Profiling Gene Expression Regulation, Bacterial Genetic Complementation Test Humans Leptospira Leptospira - cytology Leptospira - genetics Leptospira - metabolism Leptospirosis - microbiology Life Sciences Monomeric GTP-Binding Proteins - genetics Monomeric GTP-Binding Proteins - metabolism Morphology motility Mutants Mutation Species Spirochaetales - genetics Spirochaetales - metabolism Spirochetes Strains (organisms) Transcription Transcriptomes Virulence |
title | Role of the major determinant of polar flagellation FlhG in the endoflagella‐containing spirochete Leptospira |
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