Skip to main content
SpringerLink
Log in

Disruption of chemotaxis-related genes affects multiple cellular processes and the virulence of pathogenic Vibrio harveyi

  • Published:
Acta Oceanologica Sinica Aims and scope Submit manuscript

Abstract

Chemotactic motility is involved in the virulence of many pathogenic bacteria. In order to understand the role of chemotactic motility of Vibrio harveyi in cellular processes and virulence, mini-Tn10/Kan transposon-induced mutants with deficient chemotactic motility were constructed, screened, and identified. Sequence analysis revealed that the 465-bp fragment (Gen Bank accession number HM630274) flanking the transposon insertion site in mutant TS-CM1 had the highest identity (96.9%) with a hypothetical protein gene of V. harveyi ATCC BAA-1116 and the second-highest identity (91.8%) with the pgk gene of V. parahaemolyticus RIMD 2210633. In another mutant, TS-CM2, 356 bp of transposon-flanking sequence (Gen Bank accession number HM630275) also showed the highest identity (94.6%) with a hypothetical protein gene of V. harveyi ATCC BAA-1116 and the second-highest identity (92.4%) with the flaB gene of V. alginolyticus HY9901. Studies on virulence-related biological characteristics such as growth, motility, adhesion, and infectivity of themutants showed that disruption of either the flagellin gene or energy metabolism gene led to subsequent loss of chemotactic motility and changes in growth, motility, adhesion, and virulence of the pathogenic V. harveyi. Hence, the flagellin gene and crucial energy metabolism gene played an important role in the chemotactic motility of V. harveyi.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Austin B, Zhang Xiaohua. 2006. Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates. Lett Appl Microbiol, 43: 119–124

    Article  Google Scholar 

  • Balebona MC, MoriNigo MA, Faris A, et al. 1995. Influence of salinity and pH on the adhesion of pathogenic Vibrio strains to Sparus aurata skin mucus. Aquaculture, 132: 113–120

    Article  Google Scholar 

  • Banks R D, Blake C C, Evans P R, et al. 1979. Sequence, structure and activity of phosphoglycerate kinase: a possible hinge-bending enzyme. Nature, 279: 773–777

    Article  Google Scholar 

  • Boin M A, Austin M J, Hāse C C. 2004. Chemotaxis in Vibrio cholerae. FEMS Micro Lett, 239: 1–8

    Article  Google Scholar 

  • Bordas MA, Balebona MC, Rodriguez-Maroto JM, et al. 1998. Chemotaxis of pathogenic Vibrio strains towards mucus surfaces of gilt-head sea bream(Sparus aurata L.). Appl Environ Microbiol, 64: 1573–1575

    Google Scholar 

  • Butler S M, Camilli A. 2004. Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae. PNAS, 101: 5018–5023

    Article  Google Scholar 

  • Celani A, Vergassola M. 2010. Bacterial strategies for chemotaxis response. PANS, 107(4): 1391–1396

    Article  Google Scholar 

  • Deeraksa A, Moonmangmee S, Toyama H, et al. 2005. Characterization and spontaneous mutation of a novel gene, polE, involved in pellicle formation in Acetobacter tropicalis SKU1100. Microbiology, 151: 4111–4120

    Article  Google Scholar 

  • Haniford D B. 2006. Transpososome dynamics and regulation in Tn10 transposition. Crit Rev Biochem Mol Biol, 42: 407–424

    Article  Google Scholar 

  • Herrero M, Lorenzo V, Timmis K N. 1990. Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol, 172: 6557–6567

    Google Scholar 

  • Josenhans C, Labigne A, Suerbaum S. 1995. Comparative ultrastructural and functional studies of Helicobacter pylory and Helicobacter mustelae flagellin mutants: both flagellin subunits, FlaA and FlaB, are necessary for full motility in Helicobacter species. J Bacteriol, 177: 3010–3020

    Google Scholar 

  • Josenhans C, Suerbaum S. 2002. The role of motility as a virulence factor in bacteria. Int J Med Microbiol, 291: 605–614

    Article  Google Scholar 

  • Khanna M R, Bhavsar S P, Kapadnis B P. 2006. Effect of temperature on growth and chemotactic behaviour of Campylobacter jejuni. Lett Appl Microbiol, 43: 84–90

    Article  Google Scholar 

  • Kirby J R. 2009. Chemotaxis-like regulatory systems: unique roles in diverse bacteria. Annual Review of Microbiology, 63: 45–59

    Article  Google Scholar 

  • Kleckner N. 1989. Transposon Tn10. In: Berg D E, Howe M M, eds. Mobile DNA. Washington D C: American Society for Microbiology Press

    Google Scholar 

  • Klesius P H, Shoemaker C A, Evans J J. 2008. Flavobacterium columnare chemotaxis to channel catfish mucus. FEMS Microbiology Letters, 288(2): 216–220

    Article  Google Scholar 

  • Lacal J, Muñoz-Martínez F, Reyes-Darías J, et al. 2011. Bacterial chemotaxis towards aromatic hydrocarbons in Pseudomonas. Environmental Microbiology, 13(7): 1733–1744

    Article  Google Scholar 

  • Larsen M H, Larsen J L, Olsen J F. 2001. Chemotaxis of Vibrio anguillarum to fish mucus: role of the origin of the fish mucus, the fish species and the serogroup of the pathogen. FEMS Microbiol Ecol, 38: 77–80

    Article  Google Scholar 

  • Lee S E, Kim S Y, Jeong B C, et al. 2006. A bacterial flagellin, Vibrio vulnificus FlaB, has a strong mucosal adjuvant activity to induce protective immunity. Infec Immun, 74: 694–702

    Article  Google Scholar 

  • Liu Yaoguang, Mitsukawa N, Oosumi T, et al. 1995. Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J, 8: 457–463

    Article  Google Scholar 

  • Lux R, Moter A, Shi Wenyuan. 2000. Chemotaxis in pathogenic spirochetes: directed movement toward targeting tissues. J Mol Microbiol Biotechnol, 2: 355–364

    Google Scholar 

  • Lux R, Shi Wenyuan. 2004. Chemotaxis-guided movements in bacteria. Crit Rev Oral Biol Med, 15: 207–220

    Article  Google Scholar 

  • Macnab R M. 1996. Flagella and motility. In: Neidhardt F C, ed. Escherichia coli and Salmonella: Cellular and Molecular Biology. Washington D C: ASM Press

    Google Scholar 

  • Merrell D S, Butler S M, Qadri F, et al. 2002. Host-induced epidemic spread of the cholera bacterium. Nature, 417: 642–645

    Article  Google Scholar 

  • McCarter L L. 2001. Polar flagellarmotility of the Vibrionaceae. Microbiol Mol Biol Rev, 65: 445–462

    Article  Google Scholar 

  • O’Toole R, Miotom D L, Wolf-Watz H. 1996. Chemotactic motility is required for invasion of the host by the fish pathogen Vibrio anguillarum. Mol Microbiol, 19: 625–637

    Article  Google Scholar 

  • Porter S L, Wadhams G H, Armitage J P. 2011. Signal processing in complex chemotaxis pathways. Nature Reviews Microbiology, 9: 153–165

    Article  Google Scholar 

  • Qin Yingxue, Wang Jun, Su Yongquan, et al. 2006. Studies on the pathogenic bacterium of ulcer disease in Epinephelus awoara. Acta Oceanol Sin, 25: 147–153

    Google Scholar 

  • Rock J L, Nelson D R. 2006. Identification and characterization of a hemolysin gene cluster in Vibrio anguillarum. Infec Immun, 74: 2777–2786

    Article  Google Scholar 

  • Salvetti S, Celandroni F, Ceragioli M, et al. 2009. Identification of non-flagellar genes involved in swarm cell differentiation using a Bacillus thuringiensis mini-Tn10 mutant library. Microbiology, 155: 912–921

    Article  Google Scholar 

  • Sambrook J, Fritsch E F, Maniatis T. 1989. Molecular Cloning: A LaboratoryManual. NewYork: Cold Spring Harbor Laboratory Press

    Google Scholar 

  • Sawabe T, Inoue S, Fukui Y, et al. 2007. Mass mortality of Japanese abalone Haliotis discus hannai caused by Vibrio harveyi infection. Microbes Environ, 22: 300–308

    Article  Google Scholar 

  • Spohn G, Scarlato V. 2001. Motility, Chemotaxis, and Flagella. In: Mobley H L T, Mendz G L, Haze U S L, eds. Helicobacter pylory: Physiology and Genetics. Washington D C: ASM Press

    Google Scholar 

  • Valenzuela M, Cerda O, Toledo H. 2003. Overview on chemotaxis and acid resistance in Helicobacter pylori. Biol Res, 36: 429–436

    Google Scholar 

  • Vine NG, Leukes WD, Kaiser H. 2004. In vitro growth characteristics of five candidates aquaculture probiotics and two fish pathogens grown in fish intestinal mucus. FEMS Microbiol Lett, 231: 145–152

    Article  Google Scholar 

  • Vladimirov N, Sourjik V. 2009. Chemotaxis: how bacteria usememory. Biological Chemistry, 390(11): 1097–1104

    Article  Google Scholar 

  • Xie L, Altindal T, Chattopadhyay S, et al. 2011. Bacterial flagellum as a propeller and as a rudder for efficient chemotaxis. PNAS, 108(6): 2246–2251

    Article  Google Scholar 

  • Yan Qingpi, Zhao Minhui, Wang Xiaolu, et al. 2010. Adhesion mechanisms of Vibrio fluvialis to skin mucus of Epinephelus awoara. Chinese Journal of Oceanology and Limnology, 28(2): 260–266

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture, Jimei University, Xiamen, 361021, China

    Yingxue Qin, Qingpi Yan, Haiping Li & Wenzheng Zou

  2. Fisheries College, Jimei University, Xiamen, 361021, China

    Yingxue Qin, Qingpi Yan, Haiping Li & Wenzheng Zou

  3. College of Ocean and Earth Science, Xiamen University, Xiamen, 361005, China

    Yongquan Su

Authors
  1. Yingxue Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qingpi Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yongquan Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Haiping Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wenzheng Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qingpi Yan.

Additional information

Foundation item: The National Natural Science Foundation of China under contract Nos 31272699 and 41176115; National Department Public Benefit Research Foundation of China under contract No. 200903029; the Natural Science Foundation of Fujian Province under contract No. 2011J06014; the National Hi-Tech Research and Development Programof China (863 Program) under contract No. 2007AA09Z115.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Qin, Y., Yan, Q., Su, Y. et al. Disruption of chemotaxis-related genes affects multiple cellular processes and the virulence of pathogenic Vibrio harveyi . Acta Oceanol. Sin. 32, 55–60 (2013). https://doi.org/10.1007/s13131-013-0341-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13131-013-0341-1

Key words

Search

Navigation