1887

Abstract

is an efficient tool for creating transgenic host plants. The first step in the genetic transformation process involves chemotaxis, which is crucial to the survival of in changeable, harsh and even contaminated soil environments. However, a systematic study of its chemotactic signalling pathway is still lacking. In this study, the distribution and classification of chemotactic genes in the model C58 and 21 other strains were annotated. Local was used for comparative genomics, and was used for predicting protein domains. Chemotactic phenotypes for knockout mutants of ternary signalling complexes in C58 were evaluated using a swim agar plate. A major cluster, in which chemotaxis genes were consistently organized as MCP (methyl-accepting chemotaxis protein), CheS, CheY1, CheA, CheR, CheB, CheY2 and CheD, was found in , but two coupling CheW proteins were located outside the ‘’ cluster. In the ternary signalling complexes, the absence of MCP atu0514 significantly impaired chemotaxis, and the absence of CheA (atu0517) or the deletion of both CheWs abolished chemotaxis. A total of 465 MCPs were found in the 22 strains, and the cytoplasmic domains of these MCPs were composed of 38 heptad repeats. A high homology was observed between the chemotactic systems of the 22 strains with individual differences in the gene and receptor protein distributions, possibly related to their ecological niches. This preliminary study demonstrates the chemotactic system of , and provides some reference for sensing and chemotaxis to exogenous signals.

Funding
This study was supported by the:
  • Nan Xu , Natural Science Foundation of the Jiangsu Higher Education Institutions of China , (Award 18KJB180030)
  • Nan Xu , Postdoctoral Research Foundation of China , (Award 2018M632389)
  • Nan Xu , National Natural Science Foundation of China , (Award 21808196, 31870118)
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/content/journal/mgen/10.1099/mgen.0.000460
2020-10-29
2021-02-26
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References

  1. Erhardt M. Strategies to block bacterial pathogenesis by interference with motility and chemotaxis. Curr Top Microbiol Immunol 2016; 398:185–205 [CrossRef][PubMed]
    [Google Scholar]
  2. Alexandre G. Chemotaxis control of transient cell aggregation. J Bacteriol 2015; 197:3230–3237 [CrossRef][PubMed]
    [Google Scholar]
  3. Leonard S, Hommais F, Nasser W, Reverchon S. Plant-phytopathogen interactions: bacterial responses to environmental and plant stimuli. Environ Microbiol 2017; 19:1689–1716 [CrossRef][PubMed]
    [Google Scholar]
  4. Mangwani N, Kumari S, Das S. Bacterial biofilms and quorum sensing: fidelity in bioremediation technology. Biotechnol Genet Eng Rev 2016; 32:43–73 [CrossRef][PubMed]
    [Google Scholar]
  5. Adadevoh JS, Triolo S, Ramsburg CA, Ford RM. Chemotaxis increases the residence time of bacteria in granular media containing distributed contaminant sources. Environ Sci Technol 2016; 50:181–187 [CrossRef][PubMed]
    [Google Scholar]
  6. Jones CW, Armitage JP. Positioning of bacterial chemoreceptors. Trends Microbiol 2015; 23:247–256 [CrossRef][PubMed]
    [Google Scholar]
  7. Hazelbauer GL. Bacterial chemotaxis: the early years of molecular studies. Annu Rev Microbiol 2012; 66:285–303 [CrossRef][PubMed]
    [Google Scholar]
  8. Parkinson JS, Hazelbauer GL, Falke JJ. Signaling and sensory adaptation in Escherichia coli chemoreceptors: 2015 update. Trends Microbiol 2015; 23:257–266 [CrossRef][PubMed]
    [Google Scholar]
  9. Gan HM, Savka MA. One more decade of Agrobacterium taxonomy. Curr Top Microbiol Immunol 2018; 418:1–14 [CrossRef][PubMed]
    [Google Scholar]
  10. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013; 41:D590–D596 [CrossRef][PubMed]
    [Google Scholar]
  11. Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM et al. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 2014; 42:D633–D642 [CrossRef][PubMed]
    [Google Scholar]
  12. Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E et al. IMG: the Integrated Microbial Genomes database and comparative analysis system. Nucleic Acids Res 2012; 40:D115–D122 [CrossRef][PubMed]
    [Google Scholar]
  13. Slater SC, Goldman BS, Goodner B, Setubal JC, Farrand SK et al. Genome sequences of three agrobacterium biovars help elucidate the evolution of multichromosome genomes in bacteria. J Bacteriol 2009; 191:2501–2511 [CrossRef][PubMed]
    [Google Scholar]
  14. Braun AC. A physiological basis for autonomous growth of the crown-gall tumor cell. Proc Natl Acad Sci USA 1958; 44:344–349 [CrossRef][PubMed]
    [Google Scholar]
  15. Chilton MD, Montoya AL, Merlo DJ, Drummond MH, Nutter R et al. Restriction endonuclease mapping of a plasmid that confers oncogenicity upon Agrobacterium tumefaciens strain B6-806. Plasmid 1978; 1:254–269 [CrossRef][PubMed]
    [Google Scholar]
  16. Nonaka S, Someya T, Kadota Y, Nakamura K, Ezura H. Super-Agrobacterium ver. 4: improving the transformation frequencies and genetic engineering possibilities for crop plants. Front Plant Sci 2019; 10:1204 [CrossRef][PubMed]
    [Google Scholar]
  17. Lacroix B, Citovsky V. Transfer of DNA from bacteria to eukaryotes. mBio 2016; 7:e00863-16 [CrossRef][PubMed]
    [Google Scholar]
  18. Hawes MC, Smith LY. Requirement for chemotaxis in pathogenicity of Agrobacterium tumefaciens on roots of soil-grown pea plants. J Bacteriol 1989; 171:5668–5671 [CrossRef][PubMed]
    [Google Scholar]
  19. Winans SC. Two-way chemical signaling in Agrobacterium-plant interactions. Microbiol Rev 1992; 56:12–31 [CrossRef][PubMed]
    [Google Scholar]
  20. Shaw CH. Agrobacterium tumefaciens chemotaxis protocols. Methods Mol Biol 1995; 44:29–36 [CrossRef][PubMed]
    [Google Scholar]
  21. Ashby AM, Watson MD, Loake GJ, Shaw CH. Ti plasmid-specified chemotaxis of Agrobacterium tumefaciens C58C1 toward vir-inducing phenolic compounds and soluble factors from monocotyledonous and dicotyledonous plants. J Bacteriol 1988; 170:4181–4187 [CrossRef][PubMed]
    [Google Scholar]
  22. Loake GJ, Ashby AM, Shaw CH. Attraction of Agrobacterium tumefaciens C58C1 towards sugars involves a highly sensitive chemotaxis system. Microbiology 1988; 134:1427–1432 [CrossRef]
    [Google Scholar]
  23. Bolton GW, Nester EW, Gordon MP. Plant phenolic compounds induce expression of the Agrobacterium tumefaciens loci needed for virulence. Science 1986; 232:983–985 [CrossRef][PubMed]
    [Google Scholar]
  24. Cangelosi GA, Ankenbauer RG, Nester EW. Sugars induce the Agrobacterium virulence genes through a periplasmic binding protein and a transmembrane signal protein. Proc Natl Acad Sci USA 1990; 87:6708–6712 [CrossRef][PubMed]
    [Google Scholar]
  25. Stachel SE, Messens E, Van Montagu M, Zambryski P. Identification of the signal molecules produced by wounded plant cells that activate T-DNA transfer in Agrobacterium tumefaciens . Nature 1985; 318:624–629 [CrossRef]
    [Google Scholar]
  26. Harighi B. Genetic evidence for CheB- and CheR-dependent chemotaxis system in A. tumefaciens toward acetosyringone. Microbiol Res 2009; 164:634–641 [CrossRef][PubMed]
    [Google Scholar]
  27. Merritt PM, Danhorn T, Fuqua C. Motility and chemotaxis in Agrobacterium tumefaciens surface attachment and biofilm formation. J Bacteriol 2007; 189:8005–8014 [CrossRef][PubMed]
    [Google Scholar]
  28. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [CrossRef][PubMed]
    [Google Scholar]
  29. Potter SC, Luciani A, Eddy SR, Park Y, Lopez R et al. HMMER web server: 2018 update. Nucleic Acids Res 2018; 46:W200–W204 [CrossRef][PubMed]
    [Google Scholar]
  30. Sampedro I, Parales RE, Krell T, Hill JE. Pseudomonas chemotaxis. FEMS Microbiol Rev 2015; 39:17–46 [CrossRef][PubMed]
    [Google Scholar]
  31. Guo M, Huang Z, Yang J. Is there any crosstalk between the chemotaxis and virulence induction signaling in Agrobacterium tumefaciens?. Biotechnol Adv 2017; 35:505–511 [CrossRef][PubMed]
    [Google Scholar]
  32. Miller LD, Yost CK, Hynes MF, Alexandre G. The major chemotaxis gene cluster of Rhizobium leguminosarum bv. viciae is essential for competitive nodulation. Mol Microbiol 2007; 63:348–362 [CrossRef][PubMed]
    [Google Scholar]
  33. Alexander RP, Zhulin IB. Evolutionary genomics reveals conserved structural determinants of signaling and adaptation in microbial chemoreceptors. Proc Natl Acad Sci USA 2007; 104:2885–2890 [CrossRef][PubMed]
    [Google Scholar]
  34. Taylor BL, Zhulin IB. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 1999; 63:479–506 [CrossRef][PubMed]
    [Google Scholar]
  35. Hou S, Larsen RW, Boudko D, Riley CW, Karatan E et al. Myoglobin-like aerotaxis transducers in Archaea and Bacteria. Nature 2000; 403:540–544 [CrossRef][PubMed]
    [Google Scholar]
  36. Upadhyay AA, Fleetwood AD, Adebali O, Finn RD, Zhulin IB. Cache domains that are homologous to, but different from PAS domains comprise the largest superfamily of extracellular sensors in prokaryotes. PLoS Comput Biol 2016; 12:e1004862 [CrossRef][PubMed]
    [Google Scholar]
  37. Fan H, Su C, Wang Y, Yao J, Zhao K et al. Sedimentary arsenite-oxidizing and arsenate-reducing bacteria associated with high arsenic groundwater from Shanyin, Northwestern China. J Appl Microbiol 2008; 105:529–539 [CrossRef][PubMed]
    [Google Scholar]
  38. Rapp BJ, Kemp JD, White F. Isolation of a non-tumor-inducing mutant of the Ti plasmid of Agrobacterium tumefaciens strain B6 . Can J Microbiol 1979; 25:291–297 [CrossRef][PubMed]
    [Google Scholar]
  39. Bi S, Lai L. Bacterial chemoreceptors and chemoeffectors. Cell Mol Life Sci 2015; 72:691–708 [CrossRef][PubMed]
    [Google Scholar]
  40. Salah Ud-Din AIM, Roujeinikova A. Methyl-accepting chemotaxis proteins: a core sensing element in prokaryotes and archaea. Cell Mol Life Sci 2017; 74:3293–3303 [CrossRef][PubMed]
    [Google Scholar]
  41. Nishiyama SI, Takahashi Y, Yamamoto K, Suzuki D, Itoh Y et al. Identification of a Vibrio cholerae chemoreceptor that senses taurine and amino acids as attractants. Sci Rep 2016; 6:20866 [CrossRef][PubMed]
    [Google Scholar]
  42. Corral-Lugo A, De la Torre J, Matilla MA, Fernández M, Morel B et al. Assessment of the contribution of chemoreceptor-based signalling to biofilm formation. Environ Microbiol 2016; 18:3355–3372 [CrossRef][PubMed]
    [Google Scholar]
  43. Lacal J, Alfonso C, Liu X, Parales RE, Morel B et al. Identification of a chemoreceptor for tricarboxylic acid cycle intermediates: differential chemotactic response towards receptor ligands. J Biol Chem 2010; 285:23126–23136 [CrossRef][PubMed]
    [Google Scholar]
  44. Xie Z, Ulrich LE, Zhulin IB, Alexandre G. PAS domain containing chemoreceptor couples dynamic changes in metabolism with chemotaxis. Proc Natl Acad Sci USA 2010; 107:2235–2240 [CrossRef][PubMed]
    [Google Scholar]
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