FcpB Is a Surface Filament Protein of the Endoflagellum Required for the Motility of the Spirochete Leptospira
The spirochete endoflagellum is a unique motility apparatus among bacteria. Despite its critical importance for pathogenesis, the full composition of the flagellum remains to be determined. We have recently reported that FcpA is a novel flagellar protein and a major component of the sheath of the fi...
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Frontiers Media S.A.
2018-05-01
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Series: | Frontiers in Cellular and Infection Microbiology |
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Online Access: | http://journal.frontiersin.org/article/10.3389/fcimb.2018.00130/full |
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author | Elsio A. Wunder Elsio A. Wunder Leyla Slamti David N. Suwondo Kimberley H. Gibson Zhiguo Shang Charles V. Sindelar Felipe Trajtenberg Alejandro Buschiazzo Alejandro Buschiazzo Albert I. Ko Albert I. Ko Mathieu Picardeau |
author_facet | Elsio A. Wunder Elsio A. Wunder Leyla Slamti David N. Suwondo Kimberley H. Gibson Zhiguo Shang Charles V. Sindelar Felipe Trajtenberg Alejandro Buschiazzo Alejandro Buschiazzo Albert I. Ko Albert I. Ko Mathieu Picardeau |
author_sort | Elsio A. Wunder |
collection | DOAJ |
description | The spirochete endoflagellum is a unique motility apparatus among bacteria. Despite its critical importance for pathogenesis, the full composition of the flagellum remains to be determined. We have recently reported that FcpA is a novel flagellar protein and a major component of the sheath of the filament of the spirochete Leptospira. By screening a library of random transposon mutants in the spirochete Leptospira biflexa, we found a motility-deficient mutant harboring a disruption in a hypothetical gene of unknown function. Here, we show that this gene encodes a surface component of the endoflagellar filament and is required for typical hook- and spiral-shaped ends of the cell body, coiled structure of the endoflagella, and high velocity phenotype. We therefore named the gene fcpB for flagellar-coiling protein B. fcpB is conserved in all members of the Leptospira genus, but not present in other organisms including other spirochetes. Complementation of the fcpB− mutant restored the wild-type morphology and motility phenotypes. Immunoblotting with anti-FcpA and anti-FcpB antisera and cryo-electron microscopy of the filament indicated that FcpB assembled onto the surface of the sheath of the filament and mostly located on the outer (convex) side of the coiled filament. We provide evidence that FcpB, together with FcpA, are Leptospira-specific novel components of the sheath of the filament, key determinants of the coiled and asymmetric structure of the endoflagella and are essential for high velocity. Defining the components of the endoflagella and their functions in these atypical bacteria should greatly enhance our understanding of the mechanisms by which these bacteria produce motility. |
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issn | 2235-2988 |
language | English |
last_indexed | 2024-12-21T21:26:17Z |
publishDate | 2018-05-01 |
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spelling | doaj.art-f62bb77cc6ea497a99f4e387a216ff412022-12-21T18:49:45ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882018-05-01810.3389/fcimb.2018.00130355654FcpB Is a Surface Filament Protein of the Endoflagellum Required for the Motility of the Spirochete LeptospiraElsio A. Wunder0Elsio A. Wunder1Leyla Slamti2David N. Suwondo3Kimberley H. Gibson4Zhiguo Shang5Charles V. Sindelar6Felipe Trajtenberg7Alejandro Buschiazzo8Alejandro Buschiazzo9Albert I. Ko10Albert I. Ko11Mathieu Picardeau12Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, United StatesOswaldo Cruz Foundation, Brazilian Ministry of Health, Salvador, BrazilInstitut Pasteur, Biology of Spirochetes Unit, Paris, FranceDepartment of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, United StatesDepartments of Molecular Biophysics and Biochemistry, Yale University School of Medicine, New Haven, CT, United StatesDepartments of Molecular Biophysics and Biochemistry, Yale University School of Medicine, New Haven, CT, United StatesDepartments of Molecular Biophysics and Biochemistry, Yale University School of Medicine, New Haven, CT, United StatesInstitut Pasteur de Montevideo, Laboratory of Molecular and Structural Microbiology, Montevideo, UruguayInstitut Pasteur de Montevideo, Laboratory of Molecular and Structural Microbiology, Montevideo, UruguayDepartment of Microbiology, Institut Pasteur, Paris, FranceDepartment of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, United StatesOswaldo Cruz Foundation, Brazilian Ministry of Health, Salvador, BrazilInstitut Pasteur, Biology of Spirochetes Unit, Paris, FranceThe spirochete endoflagellum is a unique motility apparatus among bacteria. Despite its critical importance for pathogenesis, the full composition of the flagellum remains to be determined. We have recently reported that FcpA is a novel flagellar protein and a major component of the sheath of the filament of the spirochete Leptospira. By screening a library of random transposon mutants in the spirochete Leptospira biflexa, we found a motility-deficient mutant harboring a disruption in a hypothetical gene of unknown function. Here, we show that this gene encodes a surface component of the endoflagellar filament and is required for typical hook- and spiral-shaped ends of the cell body, coiled structure of the endoflagella, and high velocity phenotype. We therefore named the gene fcpB for flagellar-coiling protein B. fcpB is conserved in all members of the Leptospira genus, but not present in other organisms including other spirochetes. Complementation of the fcpB− mutant restored the wild-type morphology and motility phenotypes. Immunoblotting with anti-FcpA and anti-FcpB antisera and cryo-electron microscopy of the filament indicated that FcpB assembled onto the surface of the sheath of the filament and mostly located on the outer (convex) side of the coiled filament. We provide evidence that FcpB, together with FcpA, are Leptospira-specific novel components of the sheath of the filament, key determinants of the coiled and asymmetric structure of the endoflagella and are essential for high velocity. Defining the components of the endoflagella and their functions in these atypical bacteria should greatly enhance our understanding of the mechanisms by which these bacteria produce motility.http://journal.frontiersin.org/article/10.3389/fcimb.2018.00130/fullLeptospiraspirochetesflagellamotilityflagellar system |
spellingShingle | Elsio A. Wunder Elsio A. Wunder Leyla Slamti David N. Suwondo Kimberley H. Gibson Zhiguo Shang Charles V. Sindelar Felipe Trajtenberg Alejandro Buschiazzo Alejandro Buschiazzo Albert I. Ko Albert I. Ko Mathieu Picardeau FcpB Is a Surface Filament Protein of the Endoflagellum Required for the Motility of the Spirochete Leptospira Frontiers in Cellular and Infection Microbiology Leptospira spirochetes flagella motility flagellar system |
title | FcpB Is a Surface Filament Protein of the Endoflagellum Required for the Motility of the Spirochete Leptospira |
title_full | FcpB Is a Surface Filament Protein of the Endoflagellum Required for the Motility of the Spirochete Leptospira |
title_fullStr | FcpB Is a Surface Filament Protein of the Endoflagellum Required for the Motility of the Spirochete Leptospira |
title_full_unstemmed | FcpB Is a Surface Filament Protein of the Endoflagellum Required for the Motility of the Spirochete Leptospira |
title_short | FcpB Is a Surface Filament Protein of the Endoflagellum Required for the Motility of the Spirochete Leptospira |
title_sort | fcpb is a surface filament protein of the endoflagellum required for the motility of the spirochete leptospira |
topic | Leptospira spirochetes flagella motility flagellar system |
url | http://journal.frontiersin.org/article/10.3389/fcimb.2018.00130/full |
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