1887

Abstract

Gram-negative sp. strain A1, originally identified as a non-motile and aflagellate bacterium, possesses two sets of genes required for flagellar formation. In this study, we characterized the flagellar genes and flagellum formation in strain A1. Flagellar gene cluster set I contained 35 flagellar genes, including one flagellin gene (), where the gene assembly structure resembled that required for the formation of lateral flagella in gammaproteobacteria. The set II flagellar genes were arranged in eight shorter clusters with 46 flagellar genes, including two flagellin genes ( and ) and , which is required for polar flagella. Our molecular phylogenetic analysis of the bacterial flagellins also demonstrated that, in contrast to p5 and p5′, p6 was categorized as a lateral flagellin group. The motile phenotype appeared in strain A1 cells when they were subcultured on semisolid media. The motile strain A1 cells produced a single flagellum at the cell pole. DNA microarray analyses using non-motile and motile strain A1 cells indicated that flagellar formation was accompanied by increased transcription of both flagellar gene sets. The two flagellins p5 and p6 were major components of the flagellar filaments isolated from motile strain A1 cells, indicating that the polar flagellum is formed by lateral and non-lateral flagellins.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000119
2015-08-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/161/8/1552.html?itemId=/content/journal/micro/10.1099/mic.0.000119&mimeType=html&fmt=ahah

References

  1. Aizawa S. 2014 The Flagellar World New York, NY: Academic Press;
    [Google Scholar]
  2. Bailey T.L., Elkan C. 1994; Fitting a mixture model by expectation maximization to discover motifs in biopolymers. In Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology pp. 28–36 Edited by Altman R., Brutlag D., Karp P., Lathrop R., Searls D. Menlo Park, CA: AAAI Press;
    [Google Scholar]
  3. Barrios H., Valderrama B., Morett E. 1999; Compilation and analysis of σ54-dependent promoter sequences. Nucleic Acids Res 27:4305–4313[PubMed] [CrossRef]
    [Google Scholar]
  4. Canals R., Ramirez S., Vilches S., Horsburgh G., Shaw J.G., Tomás J.M., Merino S. 2006; Polar flagellum biogenesis in Aeromonas hydrophila . J Bacteriol 188:542–555[PubMed] [CrossRef]
    [Google Scholar]
  5. Chilcott G.S., Hughes K.T. 2000; Coupling of flagellar gene expression to flagellar assembly in Salmonella enterica serovar typhimurium and Escherichia coli . Microbiol Mol Biol Rev 64:694–708[PubMed] [CrossRef]
    [Google Scholar]
  6. Claret L., Hughes C. 2002; Interaction of the atypical prokaryotic transcription activator FlhD2C2 with early promoters of the flagellar gene hierarchy. J Mol Biol 321:185–199 [View Article][PubMed]
    [Google Scholar]
  7. Covelli J.M., Althabegoiti M.J., López M.F., Lodeiro A.R. 2013; Swarming motility in Bradyrhizobium japonicum . Res Microbiol 164:136–144 [View Article][PubMed]
    [Google Scholar]
  8. Dasgupta N., Wolfgang M.C., Goodman A.L., Arora S.K., Jyot J., Lory S., Ramphal R. 2003; A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa . Mol Microbiol 50:809–824 [View Article][PubMed]
    [Google Scholar]
  9. Driks A., Bryan R., Shapiro L., DeRosier D.J. 1989; The organization of the Caulobacter crescentus flagellar filament. J Mol Biol 206:627–636 [View Article][PubMed]
    [Google Scholar]
  10. Eloe E.A., Lauro F.M., Vogel R.F., Bartlett D.H. 2008; The deep-sea bacterium Photobacterium profundum SS9 utilizes separate flagellar systems for swimming and swarming under high-pressure conditions. Appl Environ Microbiol 74:6298–6305 [View Article][PubMed]
    [Google Scholar]
  11. Faulds-Pain A., Birchall C., Aldridge C., Smith W.D., Grimaldi G., Nakamura S., Miyata T., Gray J., Li G., other authors. 2011; Flagellin redundancy in Caulobacter crescentus and its implications for flagellar filament assembly. J Bacteriol 193:2695–2707 [View Article][PubMed]
    [Google Scholar]
  12. Hashimoto W., He J., Wada Y., Nankai H., Mikami B., Murata K. 2005; Proteomics-based identification of outer-membrane proteins responsible for import of macromolecules in Sphingomonas sp. A1: alginate-binding flagellin on the cell surface. Biochemistry 44:13783–13794 [View Article][PubMed]
    [Google Scholar]
  13. Hayashi C., Takase R., Momma K., Maruyama Y., Murata K., Hashimoto W. 2014; Alginate-dependent gene expression mechanism in Sphingomonas sp. strain A1. J Bacteriol 196:2691–2700 [View Article][PubMed]
    [Google Scholar]
  14. Hisano T., Yonemoto Y., Yamashita T., Fukuda Y., Kimura A., Murata K. 1995; Direct uptake of alginate molecules through a pit on the bacterial cell surface: a novel mechanism for the uptake of macromolecules. J Ferment Bioeng 79:538–544 [View Article]
    [Google Scholar]
  15. Ide N., Ikebe T., Kutsukake K. 1999; Reevaluation of the promoter structure of the class 3 flagellar operons of Escherichia coli Salmonella . Genes Genet Syst 74:113–116 [View Article][PubMed]
    [Google Scholar]
  16. Iida Y., Hobley L., Lambert C., Fenton A.K., Sockett R.E., Aizawa S. 2009; Roles of multiple flagellins in flagellar formation and flagellar growth post bdelloplast lysis in Bdellovibrio bacteriovorus . J Mol Biol 394:1011–1021 [View Article][PubMed]
    [Google Scholar]
  17. Irizarry R.A., Bolstad B.M., Collin F., Cope L.M., Hobbs B., Speed T.P. 2003a; Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31:e15 [View Article][PubMed]
    [Google Scholar]
  18. Irizarry R.A., Hobbs B., Collin F., Beazer-Barclay Y.D., Antonellis K.J., Scherf U., Speed T.P. 2003b; Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249–264 [View Article][PubMed]
    [Google Scholar]
  19. Kanbe M., Yagasaki J., Zehner S., Göttfert M., Aizawa S. 2007; Characterization of two sets of subpolar flagella in Bradyrhizobium japonicum . J Bacteriol 189:1083–1089 [View Article][PubMed]
    [Google Scholar]
  20. Kazmierczak B.I., Hendrixson D.R. 2013; Spatial and numerical regulation of flagellar biosynthesis in polarly flagellated bacteria. Mol Microbiol 88:655–663 [View Article][PubMed]
    [Google Scholar]
  21. Kim Y.K., McCarter L.L. 2000; Analysis of the polar flagellar gene system of Vibrio parahaemolyticus . J Bacteriol 182:3693–3704 [View Article][PubMed]
    [Google Scholar]
  22. Kusumoto A., Kamisaka K., Yakushi T., Terashima H., Shinohara A., Homma M. 2006; Regulation of polar flagellar number by the flhF flhG genes in Vibrio alginolyticus . J Biochem 139:113–121 [View Article][PubMed]
    [Google Scholar]
  23. Leifson E. 1960 Atlas of Bacterial Flagellation New York, NY: Academic Press;
    [Google Scholar]
  24. Madden T.L., Tatusov R.L., Zhang J. 1996; Applications of network blast server. Methods Enzymol 266:131–141[PubMed] [CrossRef]
    [Google Scholar]
  25. McCarter L.L. 2004; Dual flagellar systems enable motility under different circumstances. J Mol Microbiol Biotechnol 7:18–29[PubMed] [CrossRef]
    [Google Scholar]
  26. Merino S., Shaw J.G., Tomás J.M. 2006; Bacterial lateral flagella: an inducible flagella system. FEMS Microbiol Lett 263:127–135[PubMed] [CrossRef]
    [Google Scholar]
  27. Miake F., Murata K., Kuroiwa A., Kumamoto T., Kuroda S., Terasawa T., Tone H., Watanabe K. 1995; Characterization of Pseudomonas paucimobilis FP2001 which forms flagella depending upon the presence of rhamnose in liquid medium. Microbiol Immunol 39:437–442 [View Article][PubMed]
    [Google Scholar]
  28. Moens S., Michiels K., Keijers V., Van Leuven F., Vanderleyden J. 1995; Cloning, sequencing, and phenotypic analysis of laf1, encoding the flagellin of the lateral flagella of Azospirillum brasilense Sp7. J Bacteriol 177:5419–5426[PubMed]
    [Google Scholar]
  29. Negrete-Abascal E., Reyes M.E., García R.M., Vaca S., Girón J.A., García O., Zenteno E., De La Garza M. 2003; Flagella and motility in Actinobacillus pleuropneumoniae . J Bacteriol 185:664–668[PubMed] [CrossRef]
    [Google Scholar]
  30. Page R.D.M. 1996; TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358[PubMed]
    [Google Scholar]
  31. Poggio S., Abreu-Goodger C., Fabela S., Osorio A., Dreyfus G., Vinuesa P., Camarena L. 2007; A complete set of flagellar genes acquired by horizontal transfer coexists with the endogenous flagellar system in Rhodobacter sphaeroides . J Bacteriol 189:3208–3216[PubMed] [CrossRef]
    [Google Scholar]
  32. Ren C.P., Beatson S.A., Parkhill J., Pallen M.J. 2005; The Flag-2 locus, an ancestral gene cluster, is potentially associated with a novel flagellar system from Escherichia coli . J Bacteriol 187:1430–1440 [View Article][PubMed]
    [Google Scholar]
  33. Roche NimbleGen 2010 NimbleGen Arrays User's Guide: Gene Expression Arrays Version 5.1 Madison, WI: Roche NimbleGen;
    [Google Scholar]
  34. Sackett M.J., Armitage J.P., Sherwood E.E., Pitta T.P. 1997; Photoresponses of the purple nonsulfur bacteria Rhodospirillum centenum Rhodobacter sphaeroides . J Bacteriol 179:6764–6768[PubMed]
    [Google Scholar]
  35. Shimada T., Sakazaki R., Suzuki K. 1985; Peritrichous flagella in mesophilic strains of Aeromonas . Jpn J Med Sci Biol 38:141–145 [View Article][PubMed]
    [Google Scholar]
  36. Stafford G.P., Ogi T., Hughes C. 2005; Binding and transcriptional activation of non-flagellar genes by the Escherichia coli flagellar master regulator FlhD2C2. Microbiology 151:1779–1788 [View Article][PubMed]
    [Google Scholar]
  37. Stewart B.J., McCarter L.L. 2003; Lateral flagellar gene system of Vibrio parahaemolyticus . J Bacteriol 185:4508–4518 [View Article][PubMed]
    [Google Scholar]
  38. Thompson J.D., Higgins D.G., Gibson T.J. 1994; Clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [View Article][PubMed]
    [Google Scholar]
  39. Wilhelms M., Gonzalez V., Tomás J.M., Merino S. 2013; Aeromonas hydrophila lateral flagellar gene transcriptional hierarchy. J Bacteriol 195:1436–1445 [View Article][PubMed]
    [Google Scholar]
  40. Yabuuchi E., Yamamoto H., Terakubo S., Okamura N., Naka T., Fujiwara N., Kobayashi K., Kosako Y., Hiraishi A. 2001; Proposal of Sphingomonas wittichii sp. nov. for strain RW1T, known as a dibenzo-p-dioxin metabolizer. Int J Syst Evol Microbiol 51:281–292[PubMed]
    [Google Scholar]
  41. Yonemoto Y., Murata K., Kimura A., Yamaguchi H., Okayama K. 1991; Bacterial alginate lyase: characterization of alginate lyase-producing bacteria and purification of the enzyme. J Ferment Bioeng 72:152–157 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000119
Loading
/content/journal/micro/10.1099/mic.0.000119
Loading

Data & Media loading...

Supplements

Supplementary Data

Supplementary Data

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error