The Homologous Components of Flagellar Type III Protein Apparatus Have Acquired a Novel Function to Control Twitching Motility in a Non-Flagellated Biocontrol Bacterium
The bacterial flagellum is one of the best-studied surface-attached appendages in bacteria. Flagellar assembly in vivo is promoted by its own protein export apparatus, a type III secretion system (T3SS) in pathogenic bacteria. <i>Lysobacter enzymogenes</i> OH11 is a non-flagellated soil...
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MDPI AG
2020-05-01
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| Series: | Biomolecules |
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| Online Access: | https://www.mdpi.com/2218-273X/10/5/733 |
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| author | Alex M. Fulano Danyu Shen Miki Kinoshita Shan-Ho Chou Guoliang Qian |
| author_facet | Alex M. Fulano Danyu Shen Miki Kinoshita Shan-Ho Chou Guoliang Qian |
| author_sort | Alex M. Fulano |
| collection | DOAJ |
| description | The bacterial flagellum is one of the best-studied surface-attached appendages in bacteria. Flagellar assembly in vivo is promoted by its own protein export apparatus, a type III secretion system (T3SS) in pathogenic bacteria. <i>Lysobacter enzymogenes</i> OH11 is a non-flagellated soil bacterium that utilizes type IV pilus (T4P)-driven twitching motility to prey upon nearby fungi for food. Interestingly, the strain OH11 encodes components homologous to the flagellar type III protein apparatus (FT3SS) on its genome, but it remains unknown whether this FT3SS-like system is functional. Here, we report that, despite the absence of flagella, the FT3SS homologous genes are responsible not only for the export of the heterologous flagellin in strain OH11 but also for twitching motility. Blocking the FT3SS-like system by in-frame deletion mutations in either <i>flhB</i> or <i>fliI</i> abolished the secretion of heterologous flagellin molecules into the culture medium, indicating that the FT3SS is functional in strain OH11. A deletion of <i>flhA</i>, <i>flhB</i>, <i>fliI</i>, or <i>fliR</i> inhibited T4P-driven twitching motility, whereas neither that of <i>fliP</i> nor <i>fliQ</i> did, suggesting that FlhA, FlhB, FliI, and FliR may obtain a novel function to modulate the twitching motility. The flagellar FliI ATPase was required for the secretion of the major pilus subunit, PilA, suggesting that FliI would have evolved to act as a PilB-like pilus ATPase. These observations lead to a plausible hypothesis that the non-flagellated <i>L. enzymogenes</i> OH11 could preserve FT3SS-like genes for acquiring a distinct function to regulate twitching motility associated with its predatory behavior. |
| first_indexed | 2024-03-10T19:59:09Z |
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| institution | Directory Open Access Journal |
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| language | English |
| last_indexed | 2024-03-10T19:59:09Z |
| publishDate | 2020-05-01 |
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| series | Biomolecules |
| spelling | doaj.art-3313dbc16f924870a61de9e21543e9c22023-11-19T23:42:45ZengMDPI AGBiomolecules2218-273X2020-05-0110573310.3390/biom10050733The Homologous Components of Flagellar Type III Protein Apparatus Have Acquired a Novel Function to Control Twitching Motility in a Non-Flagellated Biocontrol BacteriumAlex M. Fulano0Danyu Shen1Miki Kinoshita2Shan-Ho Chou3Guoliang Qian4College of Plant Protection (Laboratory of Plant Immunity; Key Laboratory of Integrated Management of Crop Diseases and Pests), Nanjing Agricultural University, Nanjing 210095, ChinaCollege of Plant Protection (Laboratory of Plant Immunity; Key Laboratory of Integrated Management of Crop Diseases and Pests), Nanjing Agricultural University, Nanjing 210095, ChinaGraduate School of Frontier Biosciences, Osaka University, 1-3 Yamadaoka, Suita, Osaka 565-0871, JapanInstitute of Biochemistry, and NCHU Agricultural Biotechnology Center, National Chung Hsing University, Taichung 402, TaiwanCollege of Plant Protection (Laboratory of Plant Immunity; Key Laboratory of Integrated Management of Crop Diseases and Pests), Nanjing Agricultural University, Nanjing 210095, ChinaThe bacterial flagellum is one of the best-studied surface-attached appendages in bacteria. Flagellar assembly in vivo is promoted by its own protein export apparatus, a type III secretion system (T3SS) in pathogenic bacteria. <i>Lysobacter enzymogenes</i> OH11 is a non-flagellated soil bacterium that utilizes type IV pilus (T4P)-driven twitching motility to prey upon nearby fungi for food. Interestingly, the strain OH11 encodes components homologous to the flagellar type III protein apparatus (FT3SS) on its genome, but it remains unknown whether this FT3SS-like system is functional. Here, we report that, despite the absence of flagella, the FT3SS homologous genes are responsible not only for the export of the heterologous flagellin in strain OH11 but also for twitching motility. Blocking the FT3SS-like system by in-frame deletion mutations in either <i>flhB</i> or <i>fliI</i> abolished the secretion of heterologous flagellin molecules into the culture medium, indicating that the FT3SS is functional in strain OH11. A deletion of <i>flhA</i>, <i>flhB</i>, <i>fliI</i>, or <i>fliR</i> inhibited T4P-driven twitching motility, whereas neither that of <i>fliP</i> nor <i>fliQ</i> did, suggesting that FlhA, FlhB, FliI, and FliR may obtain a novel function to modulate the twitching motility. The flagellar FliI ATPase was required for the secretion of the major pilus subunit, PilA, suggesting that FliI would have evolved to act as a PilB-like pilus ATPase. These observations lead to a plausible hypothesis that the non-flagellated <i>L. enzymogenes</i> OH11 could preserve FT3SS-like genes for acquiring a distinct function to regulate twitching motility associated with its predatory behavior.https://www.mdpi.com/2218-273X/10/5/733flagellar type III apparatustype IV pilusnon-flagellated bacteria<i>Lysobacter</i>twitching motility |
| spellingShingle | Alex M. Fulano Danyu Shen Miki Kinoshita Shan-Ho Chou Guoliang Qian The Homologous Components of Flagellar Type III Protein Apparatus Have Acquired a Novel Function to Control Twitching Motility in a Non-Flagellated Biocontrol Bacterium Biomolecules flagellar type III apparatus type IV pilus non-flagellated bacteria <i>Lysobacter</i> twitching motility |
| title | The Homologous Components of Flagellar Type III Protein Apparatus Have Acquired a Novel Function to Control Twitching Motility in a Non-Flagellated Biocontrol Bacterium |
| title_full | The Homologous Components of Flagellar Type III Protein Apparatus Have Acquired a Novel Function to Control Twitching Motility in a Non-Flagellated Biocontrol Bacterium |
| title_fullStr | The Homologous Components of Flagellar Type III Protein Apparatus Have Acquired a Novel Function to Control Twitching Motility in a Non-Flagellated Biocontrol Bacterium |
| title_full_unstemmed | The Homologous Components of Flagellar Type III Protein Apparatus Have Acquired a Novel Function to Control Twitching Motility in a Non-Flagellated Biocontrol Bacterium |
| title_short | The Homologous Components of Flagellar Type III Protein Apparatus Have Acquired a Novel Function to Control Twitching Motility in a Non-Flagellated Biocontrol Bacterium |
| title_sort | homologous components of flagellar type iii protein apparatus have acquired a novel function to control twitching motility in a non flagellated biocontrol bacterium |
| topic | flagellar type III apparatus type IV pilus non-flagellated bacteria <i>Lysobacter</i> twitching motility |
| url | https://www.mdpi.com/2218-273X/10/5/733 |
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