Flavobacterium columnare ferric iron uptake systems are required for virulence
Flavobacterium columnare, which causes columnaris disease, is one of the costliest pathogens in the freshwater fish-farming industry. The virulence mechanisms of F. columnare are not well understood and current methods to control columnaris outbreaks are inadequate. Iron is an essential nutrient nee...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-10-01
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| Series: | Frontiers in Cellular and Infection Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcimb.2022.1029833/full |
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| author | Rachel A. Conrad Jason P. Evenhuis Ryan S. Lipscomb David Pérez-Pascual Rebecca J. Stevick Clayton Birkett Jean-Marc Ghigo Mark J. McBride |
| author_facet | Rachel A. Conrad Jason P. Evenhuis Ryan S. Lipscomb David Pérez-Pascual Rebecca J. Stevick Clayton Birkett Jean-Marc Ghigo Mark J. McBride |
| author_sort | Rachel A. Conrad |
| collection | DOAJ |
| description | Flavobacterium columnare, which causes columnaris disease, is one of the costliest pathogens in the freshwater fish-farming industry. The virulence mechanisms of F. columnare are not well understood and current methods to control columnaris outbreaks are inadequate. Iron is an essential nutrient needed for metabolic processes and is often required for bacterial virulence. F. columnare produces siderophores that bind ferric iron for transport into the cell. The genes needed for siderophore production have been identified, but other components involved in F. columnare iron uptake have not been studied in detail. We identified the genes encoding the predicted secreted heme-binding protein HmuY, the outer membrane iron receptors FhuA, FhuE, and FecA, and components of an ATP binding cassette (ABC) transporter predicted to transport ferric iron across the cytoplasmic membrane. Deletion mutants were constructed and examined for growth defects under iron-limited conditions and for virulence against zebrafish and rainbow trout. Mutants with deletions in genes encoding outer membrane receptors, and ABC transporter components exhibited growth defects under iron-limited conditions. Mutants lacking multiple outer membrane receptors, the ABC transporter, or HmuY retained virulence against zebrafish and rainbow trout mirroring that exhibited by the wild type. Some mutants predicted to be deficient in multiple steps of iron uptake exhibited decreased virulence. Survivors of exposure to such mutants were partially protected against later infection by wild-type F. columnare. |
| first_indexed | 2024-04-13T23:36:33Z |
| format | Article |
| id | doaj.art-c12cd9f409104eda852e39c152e53ad3 |
| institution | Directory Open Access Journal |
| issn | 2235-2988 |
| language | English |
| last_indexed | 2024-04-13T23:36:33Z |
| publishDate | 2022-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular and Infection Microbiology |
| spelling | doaj.art-c12cd9f409104eda852e39c152e53ad32022-12-22T02:24:43ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882022-10-011210.3389/fcimb.2022.10298331029833Flavobacterium columnare ferric iron uptake systems are required for virulenceRachel A. Conrad0Jason P. Evenhuis1Ryan S. Lipscomb2David Pérez-Pascual3Rebecca J. Stevick4Clayton Birkett5Jean-Marc Ghigo6Mark J. McBride7Department of Biological Sciences, University of Wisconsin-Milwaukee, Milwaukee, WI, United StatesNational Center for Cool and Cold Water Aquaculture, Agricultural Research Service, United States Department of Agriculture (USDA), Kearneysville, WV, United StatesNational Center for Cool and Cold Water Aquaculture, Agricultural Research Service, United States Department of Agriculture (USDA), Kearneysville, WV, United StatesInstitut Pasteur, Université de Paris-Cité, CNRS UMR 6047, Genetics of Biofilms Laboratory, Paris, FranceInstitut Pasteur, Université de Paris-Cité, CNRS UMR 6047, Genetics of Biofilms Laboratory, Paris, FranceNational Center for Cool and Cold Water Aquaculture, Agricultural Research Service, United States Department of Agriculture (USDA), Kearneysville, WV, United StatesInstitut Pasteur, Université de Paris-Cité, CNRS UMR 6047, Genetics of Biofilms Laboratory, Paris, FranceDepartment of Biological Sciences, University of Wisconsin-Milwaukee, Milwaukee, WI, United StatesFlavobacterium columnare, which causes columnaris disease, is one of the costliest pathogens in the freshwater fish-farming industry. The virulence mechanisms of F. columnare are not well understood and current methods to control columnaris outbreaks are inadequate. Iron is an essential nutrient needed for metabolic processes and is often required for bacterial virulence. F. columnare produces siderophores that bind ferric iron for transport into the cell. The genes needed for siderophore production have been identified, but other components involved in F. columnare iron uptake have not been studied in detail. We identified the genes encoding the predicted secreted heme-binding protein HmuY, the outer membrane iron receptors FhuA, FhuE, and FecA, and components of an ATP binding cassette (ABC) transporter predicted to transport ferric iron across the cytoplasmic membrane. Deletion mutants were constructed and examined for growth defects under iron-limited conditions and for virulence against zebrafish and rainbow trout. Mutants with deletions in genes encoding outer membrane receptors, and ABC transporter components exhibited growth defects under iron-limited conditions. Mutants lacking multiple outer membrane receptors, the ABC transporter, or HmuY retained virulence against zebrafish and rainbow trout mirroring that exhibited by the wild type. Some mutants predicted to be deficient in multiple steps of iron uptake exhibited decreased virulence. Survivors of exposure to such mutants were partially protected against later infection by wild-type F. columnare.https://www.frontiersin.org/articles/10.3389/fcimb.2022.1029833/fullFlavobacterium columnarevirulenceiron acquisitionouter membrane siderophore receptorheme binding protein |
| spellingShingle | Rachel A. Conrad Jason P. Evenhuis Ryan S. Lipscomb David Pérez-Pascual Rebecca J. Stevick Clayton Birkett Jean-Marc Ghigo Mark J. McBride Flavobacterium columnare ferric iron uptake systems are required for virulence Frontiers in Cellular and Infection Microbiology Flavobacterium columnare virulence iron acquisition outer membrane siderophore receptor heme binding protein |
| title | Flavobacterium columnare ferric iron uptake systems are required for virulence |
| title_full | Flavobacterium columnare ferric iron uptake systems are required for virulence |
| title_fullStr | Flavobacterium columnare ferric iron uptake systems are required for virulence |
| title_full_unstemmed | Flavobacterium columnare ferric iron uptake systems are required for virulence |
| title_short | Flavobacterium columnare ferric iron uptake systems are required for virulence |
| title_sort | flavobacterium columnare ferric iron uptake systems are required for virulence |
| topic | Flavobacterium columnare virulence iron acquisition outer membrane siderophore receptor heme binding protein |
| url | https://www.frontiersin.org/articles/10.3389/fcimb.2022.1029833/full |
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