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Flagellar-Dependent Motility in Mesorhizobium tianshanense is Involved in the Early Stage of Plant Host Interaction: Study of an flgE Mutant

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Abstract

Bacterial motility is most likely a critical factor for rhizobium to chemotactically colonize on the root surface prior to infecting leguminous plant hosts. Several studies of the rhizobium flagellar filament have been reported, but little is known about the rhizobium flagellum hook. To investigate the roles of the hook protein in flagellum synthesis in Mesorhizobium tianshanense, the hook protein-encoding gene flgE of M. tianshanense was amplified by PCR and sequenced. Comparison of the deduced amino acid sequences revealed pronounced similarities in Domain 1 and lower similarities in Domain 2, which are supposed to be related to hook structure assembly and antigenic diversity, respectively. The level of transcription of flgE increased along with the cell growth and reached its maximum at the middle log phase. Disruption of the flgE gene caused a flagellar-less phenotype, thereby causing complete loss of swimming ability, modified nutrient-related swarming ability and biofilm formation. Moreover, the absence of flagellar caused decreased bacterial attachment on the root hair, suggesting that flagellar is involved in the early stage of symbiosis process.

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References

  1. Ames P, Bergman K (1981) Competitive advantage provided by bacterial motility in the formation of nodules by Rhizobium meliloti. J Bacteriol 148(2):728–729

    CAS  PubMed Central  PubMed  Google Scholar 

  2. Ballado T et al (2001) The hook gene (flgE) is expressed from the flgBCDEF operon in Rhodobacter sphaeroides: Study of an flgE mutant. J Bacteriol 183(5):1680–1687

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Beringer JE (1974) R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84(1):188–198

    Article  CAS  PubMed  Google Scholar 

  4. Caetano-Anollés G, Wall LG, De Micheli AT, Macchi EM, Bauer WD, Favelukes G (1988) Role of motility and chemotaxis in efficiency of nodulation by Rhizobium meliloti. Plant Physiol 86(4):1228–1235

    Article  PubMed Central  PubMed  Google Scholar 

  5. Chen W, Wang E, Wang S, Li Y, Chen X, Li Y (1995) Characteristics of Rhizobium tianshanense sp nov, a moderately and slowly growing root nodule bacterium isolated from an arid saline environment in Xinjiang, People’s Republic of China. Int J Syst Bacteriol 45(1):153–159

    Article  CAS  PubMed  Google Scholar 

  6. Cooper JE (2004) Multiple responses of rhizobia to flavonoids during legume root infection. Adv Bot Res 41:1–62

    Article  CAS  Google Scholar 

  7. Covelli JM, Althabegoiti MJ, Lo´pez MF, Lodeiro AR (2013) Swarming motility in Bradyrhizobium japonicum. Res Microbiol 164:136–144

    Article  CAS  PubMed  Google Scholar 

  8. Eggenhofer E, Rachel R, Haslbeck M, Scharf B (2006) MotD of Sinorhizobium meliloti and related α-proteobacteria is the flagellar-hook-length regulator and therefore reassigned as FliK. J Bacteriol 188(6):2144–2153

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Fujishige NA, Kapadia NN, De Hoff PL, Hirsch AM (2006) Investigations of Rhizobium biofilm formation. FEMS Microbiol Ecol 56(2):195–206

    Article  CAS  PubMed  Google Scholar 

  10. Glenn-Calvo E, Bär W, Frosch M (1994) Isolation and characterization of the flagellar hook of Campylobacter jejuni. FEMS Microbiol Lett 123(3):209–304

    Article  Google Scholar 

  11. Harshey RM (2003) Bacterial motility on a surface : many ways to a common goal. Annu Rev Microbiol 57(1):249–273

    Article  CAS  PubMed  Google Scholar 

  12. Hellweg C, Pühler A, Weidner S (2009) The time course of the transcriptomic response of Sinorhizobium meliloti 1021 following a shift to acidic pH. BMC Microbiol 9(1):37

    Article  PubMed Central  PubMed  Google Scholar 

  13. Henrichsen J (1972) Bacterial surface translocation : a survey and a classification. Bacteriol Rev 36(4):478

    CAS  PubMed Central  PubMed  Google Scholar 

  14. Hirano T, Shibata S, Ohnishi K, Tani T, Aizawa SI (2005) N-terminal signal region of FliK is dispensable for length control of the flagellar hook. Mol Microbiol 56(2):346–360

    Article  CAS  PubMed  Google Scholar 

  15. Kinsella N, Guerry P, Cooney J (1997) The flgE gene of Campylobacter coli is under the control of the alternative sigma factor sigma54. J Bacteriol 179(15):4647–4653

    CAS  PubMed Central  PubMed  Google Scholar 

  16. Lüneberg E, Glenn-Calvo E, Hartmann M, Bär W, Frosch M (1998) The central, surface-exposed region of the flagellar hook protein FlgE of Campylobacter jejuni Shows hypervariability among strains. J Bacteriol 180(14):3711–3714

    PubMed Central  PubMed  Google Scholar 

  17. Le MT, Porcelli I, Weight CM, Gaskin DJ, Carding SR, Vliet AH (2012) Acid-shock of Campylobacter jejuni induces flagellar gene expression and host cell invasion. Eur J Microbiol Immunol 2(1):12–19

    Article  CAS  Google Scholar 

  18. Li H, Ruby J, Charon N, Kuramitsu H (1996) Gene inactivation in the oral spirochete Treponema denticola: construction of an flgE mutant. J Bacteriol 178(12):3664–3667

    CAS  PubMed Central  PubMed  Google Scholar 

  19. Macnab RM (2003) How bacteria assemble flagella. Annu Rev Microbiol 57(1):77–100

    Article  CAS  PubMed  Google Scholar 

  20. Malek W (1992) The role of motility in the efficiency of nodulation by Rhizobium meliloti. Arch Microbiol 158(1):26–28

    Article  Google Scholar 

  21. Mellor HY, Glenn AR, Arwas R, Dilworth MJ (1987) Symbiotic and competitive properties of motility mutants of Rhizobium trifolii TA1. Arch Microbiol 148(1):34–39

    Article  CAS  Google Scholar 

  22. Merritt JH, Brothers KM, Kuchma SL, O’toole GA (2007) SadC reciprocally influences biofilm formation and swarming motility via modulation of exopolysaccharide production and flagellar function. J Bacteriol 189(22):8154–8164

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

  24. Miller LD, Yost CK, Hynes MF, Alexandre G (2007) The major chemotaxis gene cluster of Rhizobium leguminosarum bv viciae is essential for competitive nodulation. Mol Microbiol 63(2):348–362

    Article  CAS  PubMed  Google Scholar 

  25. Murray TS, Kazmierczak BI (2008) Pseudomonas aeruginosa exhibits sliding motility in the absence of type IV pili and flagella. J Bacteriol 190(8):2700–2708

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Platzer J, Sterr W, Hausmann M, Schmitt R (1997) Three genes of a motility operon and their role in flagellar rotary speed variation in Rhizobium meliloti. J Bacteriol 179(20):6391–6399

    CAS  PubMed Central  PubMed  Google Scholar 

  27. Rinaudi L, Fujishige NA, Hirsch AM, Banchio E, Zorreguieta A, Giordano W (2006) Effects of nutritional and environmental conditions on Sinorhizobium meliloti biofilm formation. Res Microbiol 157(9):867–875

    Article  CAS  PubMed  Google Scholar 

  28. Sal MS, Li C, Motalab M, Shibata S, Aizawa SI, Charon NW (2008) Borrelia burgdorferi uniquely regulates its motility genes and has an intricate flagellar hook-basal body structure. J Bacteriol 190(6):1912–1921

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Samatey FA, Matsunami H, Imada K, Nagashima S, Shaikh TR, Thomas DR, Chen JZ, DeRosier DJ, Kitao A, Namba K (2004) Structure of the bacterial flagellar hook and implication for the molecular universal joint mechanism. Nature 431(7012):1062–1068

    Article  CAS  PubMed  Google Scholar 

  30. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

  31. Santaella C, Schue M, Berge O, Heulin T, Achouak W (2008) The exopolysaccharide of Rhizobium sp. YAS34 is not necessary for biofilm formation on Arabidopsis thaliana and Brassica napus roots but contributes to root colonization. Environ Microbiol 10(8):2150–2163

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Sauer K, Cullen M, Rickard A, Zeef L, Davies D, Gilbert P (2004) Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 186(21):7312–7326

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Scharf B, Schuster-Wolff-Bühring H, Rachel R, Schmitt R (2001) Mutational analysis of the Rhizobium lupini H13-3 and Sinorhizobium meliloti flagellin genes: importance of flagellin A for flagellar filament structure and transcriptional regulation. J Bacteriol 183(18):5334–5342

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Skorupska A, Deryło M, Lorkiewicz Z (1989) Siderophore production and utilization by Rhizobium trifolii. Biol Metals 2(1):45–49

    Article  CAS  Google Scholar 

  35. Smit G, Logman T, Boerrigter M, Kijne J, Lugtenberg B (1989) Purification and partial characterization of the Rhizobium leguminosarum biovar viciae Ca2+-dependent adhesin, which mediates the first step in attachment of cells of the family Rhizobiaceae to plant root hair tips. J Bacteriol 171(7):4054–4062

    CAS  PubMed Central  PubMed  Google Scholar 

  36. Soby S, Bergman K (1983) Motility and chemotaxis of Rhizobium meliloti in soil. Appl Environ Microbiol 46(5):995–998

    CAS  PubMed Central  PubMed  Google Scholar 

  37. Sourjik V, Muschler P, Scharf B, Schmitt R (2000) VisN and VisR are global regulators of chemotaxis, flagellar, and motility genes in Sinorhizobium (Rhizobium) meliloti. J Bacteriol 182(3):782–788

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Tambalo DD, Bustard DE, Del Bel KL, Koval SF, Khan MF, Hynes MF (2010) Characterization and functional analysis of seven flagellin genes in Rhizobium leguminosarum bv. viciae. characterization of R. leguminosarum flagellins. BMC Microbiol 10(1):219

    Article  PubMed Central  PubMed  Google Scholar 

  39. Tambalo DD, Del Bel KL, Bustard DE, Greenwood PR, Steedman AE, Hynes MF (2010) Regulation of flagellar, motility and chemotaxis genes in Rhizobium leguminosarum by the VisN/R-Rem cascade. Microbiology 156(6):1673–1685

    Article  CAS  PubMed  Google Scholar 

  40. Thomason MK, Fontaine F, De Lay N, Storz G (2012) A small RNA that regulates motility and biofilm formation in response to changes in nutrient availability in Escherichia coli. Mol Microbiol 84(1):17–35

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Van Houdt R, Michiels CW (2005) Role of bacterial cell surface structures in Escherichia coli biofilm formation. Res Microbiol 156(5):626–633

    Article  PubMed  Google Scholar 

  42. Vatanyoopaisarn S, Nazli A, Dodd CE, Rees CE, Waites WM (2000) Effect of flagella on initial attachment of Listeria monocytogenes to stainless steel. Appl Environ Microbiol 66(2):860–863

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132(1):44–51

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Wang P, Zhong Z, Zhou J, Cai T, Zhu J (2008) Exopolysaccharide biosynthesis is important for Mesorhizobium tianshanense: plant host interaction. Arch Microbiol 189(5):525–530

    Article  CAS  PubMed  Google Scholar 

  45. Zheng H, Zhong Z, Lai X, Chen WX, Li S, Zhu J (2006) A LuxR/LuxI-type quorum-sensing system in a plant bacterium, Mesorhizobium tianshanense, controls symbiotic nodulation. J Bacteriol 188(5):1943–1949

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank Dr. Jun Zhu for helpful discussion, and Dr. Yunduan Wang for the gene sequence determination. This study was supported by a 973 project (CB126502, to J.Z.), the Ph.D. programs foundation of the Ministry of Education (MOE) (20120097110016, to J.Z.), and an NSFC award (31170077, to Z.Z).

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Authors and Affiliations

  1. Department of Microbiology, Nanjing Agricultural University, Nanjing, China

    Huiming Zheng, Yiling Mao, Jiao Teng, Qingcheng Zhu, Jun Ling & Zengtao Zhong

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  1. Huiming Zheng
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  2. Yiling Mao
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  3. Jiao Teng
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  4. Qingcheng Zhu
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Correspondence to Huiming Zheng or Zengtao Zhong.

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Zheng, H., Mao, Y., Teng, J. et al. Flagellar-Dependent Motility in Mesorhizobium tianshanense is Involved in the Early Stage of Plant Host Interaction: Study of an flgE Mutant. Curr Microbiol 70, 219–227 (2015). https://doi.org/10.1007/s00284-014-0701-x

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