Transposon mutagenesis and genome sequencing identify two novel, tandem genes involved in the colony spreading of Flavobacterium collinsii, isolated from an ayu fish, Plecoglossus altivelis
Bacteria of the family Flavobacteriaceae (flavobacteria) primarily comprise nonpathogenic bacteria that inhabit soil and water (both marine and freshwater). However, some bacterial species in the family, including Flavobacterium psychrophilum and Flavobacterium columnare, are known to be pathogenic...
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Frontiers Media S.A.
2023-02-01
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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.2023.1095919/full |
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| author | Yoshio Kondo Kenichi Ohara Ryoji Fujii Yudai Nakai Chikara Sato Chikara Sato Chikara Sato Chikara Sato Mariko Naito Takayuki Tsukuba Tomoko Kadowaki Keiko Sato |
| author_facet | Yoshio Kondo Kenichi Ohara Ryoji Fujii Yudai Nakai Chikara Sato Chikara Sato Chikara Sato Chikara Sato Mariko Naito Takayuki Tsukuba Tomoko Kadowaki Keiko Sato |
| author_sort | Yoshio Kondo |
| collection | DOAJ |
| description | Bacteria of the family Flavobacteriaceae (flavobacteria) primarily comprise nonpathogenic bacteria that inhabit soil and water (both marine and freshwater). However, some bacterial species in the family, including Flavobacterium psychrophilum and Flavobacterium columnare, are known to be pathogenic to fish. Flavobacteria, including the abovementioned pathogenic bacteria, belong to the phylum Bacteroidota and possess two phylum-specific features, gliding motility and a protein secretion system, which are energized by a common motor complex. Herein, we focused on Flavobacterium collinsii (GiFuPREF103) isolated from a diseased fish (Plecoglossus altivelis). Genomic analysis of F. collinsii GiFuPREF103 revealed the presence of a type IX secretion system and additional genes associated with gliding motility and spreading. Using transposon mutagenesis, we isolated two mutants with altered colony morphology and colony spreading ability; these mutants had transposon insertions in pep25 and lbp26. The glycosylation material profiles revealed that these mutants lacked the high-molecular-weight glycosylated materials present in the wild-type strain. In addition, the wild-type strains exhibited fast cell population movement at the edge of the spreading colony, whereas reduced cell population behavior was observed in the pep25- and lbp26-mutant strains. In the aqueous environment, the surface layers of these mutant strains were more hydrophobic, and they formed biofilms with enhanced microcolony growth compared to those with the wild-type. In Flavobacterium johnsoniae, the Fjoh_0352 and Fjoh_0353 mutant strains were generated, which were based on the ortholog genes of pep25 and lbp26. In these F. johnsoniae mutants, as in F. collinsii GiFuPREF103, colonies with diminished spreading capacity were formed. Furthermore, cell population migration was observed at the edge of the colony in wild-type F. johnsoniae, whereas individual cells, and not cell populations, migrated in these mutant strains. The findings of the present study indicate that pep25 and lbp26 contribute to the colony spreading of F. collinsii. |
| first_indexed | 2024-04-10T16:03:37Z |
| format | Article |
| id | doaj.art-5de2a315bbfa44eda48fbc705a9cab24 |
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| issn | 2235-2988 |
| language | English |
| last_indexed | 2024-04-10T16:03:37Z |
| publishDate | 2023-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular and Infection Microbiology |
| spelling | doaj.art-5de2a315bbfa44eda48fbc705a9cab242023-02-10T06:46:42ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882023-02-011310.3389/fcimb.2023.10959191095919Transposon mutagenesis and genome sequencing identify two novel, tandem genes involved in the colony spreading of Flavobacterium collinsii, isolated from an ayu fish, Plecoglossus altivelisYoshio Kondo0Kenichi Ohara1Ryoji Fujii2Yudai Nakai3Chikara Sato4Chikara Sato5Chikara Sato6Chikara Sato7Mariko Naito8Takayuki Tsukuba9Tomoko Kadowaki10Keiko Sato11Department of Pediatric Dentistry, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki, JapanGifu Prefectural Research Institute for Fisheries and Aquatic Environments, Gifu, JapanGifu Prefectural Research Institute for Fisheries and Aquatic Environments, Gifu, JapanDepartment of Frontier Oral Science, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki, JapanSchool of Integrative and Global Majors (SIGMA), University of Tsukuba, Ibaraki, JapanBiological Science Course, Graduate School of Science and Engineering, Aoyama Gakuin University, Kanagawa, JapanDivision of Immune Homeostasis, Department of Pathology and Microbiology, Nihon University School of Medicine, Tokyo, JapanDivision of Microbiology, Department of Pathology and Microbiology, Nihon University School of Medicine, Tokyo, JapanDepartment of Microbiology and Oral Infection, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki, JapanDepartment of Dental Pharmacology, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki, JapanDepartment of Frontier Oral Science, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki, JapanDepartment of Frontier Oral Science, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki, JapanBacteria of the family Flavobacteriaceae (flavobacteria) primarily comprise nonpathogenic bacteria that inhabit soil and water (both marine and freshwater). However, some bacterial species in the family, including Flavobacterium psychrophilum and Flavobacterium columnare, are known to be pathogenic to fish. Flavobacteria, including the abovementioned pathogenic bacteria, belong to the phylum Bacteroidota and possess two phylum-specific features, gliding motility and a protein secretion system, which are energized by a common motor complex. Herein, we focused on Flavobacterium collinsii (GiFuPREF103) isolated from a diseased fish (Plecoglossus altivelis). Genomic analysis of F. collinsii GiFuPREF103 revealed the presence of a type IX secretion system and additional genes associated with gliding motility and spreading. Using transposon mutagenesis, we isolated two mutants with altered colony morphology and colony spreading ability; these mutants had transposon insertions in pep25 and lbp26. The glycosylation material profiles revealed that these mutants lacked the high-molecular-weight glycosylated materials present in the wild-type strain. In addition, the wild-type strains exhibited fast cell population movement at the edge of the spreading colony, whereas reduced cell population behavior was observed in the pep25- and lbp26-mutant strains. In the aqueous environment, the surface layers of these mutant strains were more hydrophobic, and they formed biofilms with enhanced microcolony growth compared to those with the wild-type. In Flavobacterium johnsoniae, the Fjoh_0352 and Fjoh_0353 mutant strains were generated, which were based on the ortholog genes of pep25 and lbp26. In these F. johnsoniae mutants, as in F. collinsii GiFuPREF103, colonies with diminished spreading capacity were formed. Furthermore, cell population migration was observed at the edge of the colony in wild-type F. johnsoniae, whereas individual cells, and not cell populations, migrated in these mutant strains. The findings of the present study indicate that pep25 and lbp26 contribute to the colony spreading of F. collinsii.https://www.frontiersin.org/articles/10.3389/fcimb.2023.1095919/fullFlavobacterium collinsiiFlavobacterium johnsoniaecolony spreadinggliding motilitytype IX secretion systembiofilm formation |
| spellingShingle | Yoshio Kondo Kenichi Ohara Ryoji Fujii Yudai Nakai Chikara Sato Chikara Sato Chikara Sato Chikara Sato Mariko Naito Takayuki Tsukuba Tomoko Kadowaki Keiko Sato Transposon mutagenesis and genome sequencing identify two novel, tandem genes involved in the colony spreading of Flavobacterium collinsii, isolated from an ayu fish, Plecoglossus altivelis Frontiers in Cellular and Infection Microbiology Flavobacterium collinsii Flavobacterium johnsoniae colony spreading gliding motility type IX secretion system biofilm formation |
| title | Transposon mutagenesis and genome sequencing identify two novel, tandem genes involved in the colony spreading of Flavobacterium collinsii, isolated from an ayu fish, Plecoglossus altivelis |
| title_full | Transposon mutagenesis and genome sequencing identify two novel, tandem genes involved in the colony spreading of Flavobacterium collinsii, isolated from an ayu fish, Plecoglossus altivelis |
| title_fullStr | Transposon mutagenesis and genome sequencing identify two novel, tandem genes involved in the colony spreading of Flavobacterium collinsii, isolated from an ayu fish, Plecoglossus altivelis |
| title_full_unstemmed | Transposon mutagenesis and genome sequencing identify two novel, tandem genes involved in the colony spreading of Flavobacterium collinsii, isolated from an ayu fish, Plecoglossus altivelis |
| title_short | Transposon mutagenesis and genome sequencing identify two novel, tandem genes involved in the colony spreading of Flavobacterium collinsii, isolated from an ayu fish, Plecoglossus altivelis |
| title_sort | transposon mutagenesis and genome sequencing identify two novel tandem genes involved in the colony spreading of flavobacterium collinsii isolated from an ayu fish plecoglossus altivelis |
| topic | Flavobacterium collinsii Flavobacterium johnsoniae colony spreading gliding motility type IX secretion system biofilm formation |
| url | https://www.frontiersin.org/articles/10.3389/fcimb.2023.1095919/full |
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