1887

Abstract

Bacterial biofilms are dynamic and structurally complex communities, involving cell-to-cell interactions. In recent years, various environmental signals that induce the complex biofilm development of the Gram-positive bacterium have been identified. These signalling molecules are often media components or molecules produced by the cells themselves, as well as those of other interacting species. The responses can also be due to depletion of certain molecules in the vicinity of the cells. Extracellular manganese (Mn) is essential for proper biofilm development of . Mn is also a component of practically all laboratory biofilm-promoting media used for . Comparison of complex colony biofilms in the presence or absence of supplemented Mn using microarray analyses revealed that genes involved in biofilm formation are indeed downregulated in the absence of Mn. In addition, Mn also affects the transcription of several other genes involved in distinct differentiation pathways of various cellular processes. The effects of Mn on other biofilm-related traits like motility, antimicrobial production, stress and sporulation were followed using fluorescent reporter strains. The global transcriptome and morphology studies highlight the importance of Mn during biofilm development and provide an overview on the expressional changes in colony biofilms in . .

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2016-08-01
2019-11-12
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References

  1. Anagnostopoulos C., Spizizen J.. 1961; Requirements for transformation in Bacillus subtilis . J Bacteriol81:741
    [Google Scholar]
  2. Baldi P., Long A. D.. 2001; A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics17:509–519 [CrossRef][PubMed]
    [Google Scholar]
  3. Beauregard P. B., Chai Y., Vlamakis H., Losick R., Kolter R.. 2013; Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci U S A110:E1621E1630 [CrossRef]
    [Google Scholar]
  4. Branda S. S., Gonzalez-Pastor J. E., Ben-Yehuda S., Losick R., Kolter R.. 2001; Fruiting body formation by Bacillus subtilis . Proc Natl Acad Sci U S A98:11621–11626 [CrossRef]
    [Google Scholar]
  5. Branda S. S., Chu F., Kearns D. B., Losick R., Kolter R.. 2006; A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol59:1229–1238 [CrossRef][PubMed]
    [Google Scholar]
  6. Cairns L. S., Hobley L., Stanley-Wall N. R.. 2014; Biofilm formation by Bacillus subtilis: new insights into regulatory strategies and assembly mechanisms. Mol Microbiol93:587–598 [CrossRef][PubMed]
    [Google Scholar]
  7. Cangiano G., Mazzone A., Baccigalupi L., Isticato R., Eichenberger P., De Felice M., Ricca E.. 2010; Direct and indirect control of late sporulation genes by GerR of Bacillus subtilis . J Bacteriol192:3406–3413 [CrossRef]
    [Google Scholar]
  8. Casadaban M. J., Chou J., Cohen S. N.. 1980; In vitro gene fusions that join an enzymatically active beta-galactosidase segment to amino-terminal fragments of exogenous proteins: Escherichia coli plasmid vectors for the detection and cloning of translational initiation signals. J Bacteriol143:971–980[PubMed]
    [Google Scholar]
  9. Charney J., Fisher W., Hegarty C. P.. 1951; Managanese as an essential element for sporulation in the genus Bacillus. J Bacteriol62:145[PubMed]
    [Google Scholar]
  10. Chen Y., Cao S., Chai Y., Clardy J., Kolter R., Guo J. H., Losick R.. 2012; A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants. Mol Microbiol85:418–430 [CrossRef][PubMed]
    [Google Scholar]
  11. Devi S. N., Vishnoi M., Kiehler B., Haggett L., Fujita M.. 2015; In vivo functional characterization of the transmembrane histidine kinase KinC in Bacillus subtilis . Microbiology161:1092–1104 [CrossRef][PubMed]
    [Google Scholar]
  12. Eichenberger P., Fujita M., Jensen S. T., Conlon E. M., Rudner D. Z., Wang S. T., Ferguson C., Haga K., Sato T. et al. 2004; The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis . PLoS Biol2:e328 [CrossRef][PubMed]
    [Google Scholar]
  13. Fujita M., Gonzalez-Pastor J. E., Losick R.. 2005; High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis . J Bacteriol187:1357–1368 [CrossRef]
    [Google Scholar]
  14. González-Pastor J. E., Hobbs E. C., Losick R.. 2003; Cannibalism by sporulating bacteria. Science301:510–513 [CrossRef][PubMed]
    [Google Scholar]
  15. Grimshaw C. E., Huang S., Hanstein C. G., Strauch M. A., Burbulys D., Wang L., Hoch J. A., Whiteley J. M.. 1998; Synergistic kinetic interactions between components of the phosphorelay controlling sporulation in Bacillus subtilis . Biochemistry37:1365–1375 [CrossRef][PubMed]
    [Google Scholar]
  16. Hamon M. A., Lazazzera B. A.. 2001; The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis . Mol Microbiol42:1199–1209[PubMed][CrossRef]
    [Google Scholar]
  17. He K., Bauer C. E.. 2014; Chemosensory signaling systems that control bacterial survival. Trends Microbiol22:389–398 [CrossRef][PubMed]
    [Google Scholar]
  18. Helmann J. D.. 2014; Specificity of metal sensing: iron and manganese homeostasis in Bacillus subtilis . J Biol Chem289:28112–28120 [CrossRef][PubMed]
    [Google Scholar]
  19. Hobley L., Ostrowski A., Rao F. V., Bromley K. M., Porter M., Prescott A. R., MacPhee C. E., van Aalten D. M. F., Stanley-Wall N. R.. 2013; BslA is a self-assembling bacterial hydrophobin that coats the Bacillus subtilis biofilm. Proc Natl Acad Sci U S A110:13600–13605 [CrossRef]
    [Google Scholar]
  20. Hoch J. A.. 1993; Regulation of the phosphorelay and the initiation of sporulation in subtilis. Annu Rev Microbiol47:441–465 [CrossRef]
    [Google Scholar]
  21. Hölscher T., Bartels B., Lin Y. C., Gallegos-Monterrosa R., Price-Whelan A., Kolter R., Dietrich L. E., Kovács Á. T.. 2015; Motility, chemotaxis and aerotaxis contribute to competitiveness during bacterial pellicle biofilm development. J Mol Biol427:3695–3708 [CrossRef][PubMed]
    [Google Scholar]
  22. Hoover S. E., Xu W., Xiao W., Burkholder W. F.. 2010; Changes in DnaA-dependent gene expression contribute to the transcriptional and developmental response of Bacillus subtilis to manganese limitation in Luria-Bertani medium. J Bacteriol192:3915–3924 [CrossRef][PubMed]
    [Google Scholar]
  23. Ireton K., Gunther N. W., Grossman A. D., Gunther N. T.. 1994; spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis . J Bacteriol176:5320–5329[PubMed]
    [Google Scholar]
  24. Jakubovics N. S., Jenkinson H. F.. 2001; Out of the iron age: new insights into the critical role of manganese homeostasis in bacteria. Microbiology147:1709–1718 [CrossRef][PubMed]
    [Google Scholar]
  25. Jiang M., Shao W., Perego M., Hoch J. A.. 2000; Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis . Mol Microbiol38:535–542[PubMed][CrossRef]
    [Google Scholar]
  26. Kaiser D.. 2015; Signaling in swarming and aggregating myxobacteria. In Evolutionary Transitions to Multicellular Life, pp.469–485 Springer;
    [Google Scholar]
  27. Kearns D. B., Chu F., Branda S. S., Kolter R., Losick R.. 2005; A master regulator for biofilm formation by Bacillus subtilis . Mol Microbiol55:739–749 [CrossRef][PubMed]
    [Google Scholar]
  28. Kobayashi K.. 2007; Bacillus subtilis pellicle formation proceeds through genetically defined morphological changes. J Bacteriol189:4920–4931 [CrossRef][PubMed]
    [Google Scholar]
  29. Kobayashi K., Iwano M.. 2012; BslA(YuaB) forms a hydrophobic layer on the surface of Bacillus subtilis biofilms. Mol Microbiol85:51–66 [CrossRef][PubMed]
    [Google Scholar]
  30. Kobayashi K., Ehrlich S. D., Albertini A., Amati G., Andersen K. K., Arnaud M., Asai K., Ashikaga S., Aymerich S. et al. 2003; Essential Bacillus subtilis genes. Proc Natl Acad Sci U S A100:4678–4683 [CrossRef][PubMed]
    [Google Scholar]
  31. Kovács Á. T.. 2016; Bacterial differentiation via gradual activation of global regulators. Curr Genet62:125–128 [CrossRef][PubMed]
    [Google Scholar]
  32. Kovács . T., Kuipers O. P.. 2011; Rok regulates yuaB expression during architecturally complex colony development of Bacillus subtilis 168. J Bacteriol193:998–1002 [CrossRef][PubMed]
    [Google Scholar]
  33. Kovács Á. T., van Gestel J., Kuipers O. P.. 2012; The protective layer of biofilm: a repellent function for a new class of amphiphilic proteins. Mol Microbiol85:8–11 [CrossRef][PubMed]
    [Google Scholar]
  34. Kuipers O. P., de Jong A., Baerends R. J., van Hijum S. A., Zomer A. L., Karsens H. A., den Hengst C. D., Kramer N. E., Buist G. et al. 2002; Transcriptome analysis and related databases of Lactococcus lactis . Antonie Van Leeuwenhoek82:113–122[PubMed][CrossRef]
    [Google Scholar]
  35. Kunst F., Ogasawara N., Moszer I., Albertini A. M., Alloni G., Azevedo V., Bertero M. G., Bessières P., Bolotin A. et al. 1997; The complete genome sequence of the gram-positive bacterium Bacillus subtilis . Nature390:249–256 [CrossRef][PubMed]
    [Google Scholar]
  36. Kuwana R., Okumura T., Takamatsu H., Watabe K.. 2005; The ylbO gene product of Bacillus subtilis is involved in the coat development and lysozyme resistance of spore. FEMS Microbiol Lett242:51–57 [CrossRef][PubMed]
    [Google Scholar]
  37. López D.. 2015; Connection of KinC to flotillins and potassium leakage in Bacillus subtilis . Microbiology161:1180–1181 [CrossRef][PubMed]
    [Google Scholar]
  38. López D., Kolter R.. 2010; Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis . FEMS Microbiol Rev34:134–149 [CrossRef][PubMed]
    [Google Scholar]
  39. López D., Fischbach M. A., Chu F., Losick R., Kolter R.. 2009a; Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis . Proc Natl Acad Sci U S A106:280–285 [CrossRef]
    [Google Scholar]
  40. López D., Vlamakis H., Losick R., Kolter R.. 2009b; Cannibalism enhances biofilm development in Bacillus subtilis . Mol Microbiol74:609–618 [CrossRef]
    [Google Scholar]
  41. López D., Vlamakis H., Losick R., Kolter R.. 2009c; Paracrine signaling in a bacterium. Genes Dev23:1631–1638 [CrossRef]
    [Google Scholar]
  42. López D., Gontang E. A., Kolter R.. 2010; Potassium sensing histidine kinase in Bacillus subtilis . Methods Enzymol471:229–251 [CrossRef][PubMed]
    [Google Scholar]
  43. Mhatre E., Monterrosa R. G., Kovács Á. T.. 2014; From environmental signals to regulators: modulation of biofilm development in Gram-positive bacteria. J Basic Microbiol54:616–632 [CrossRef][PubMed]
    [Google Scholar]
  44. Ng W. L., Bassler B. L.. 2009; Bacterial quorum-sensing network architectures. Annu Rev Genet43:197–222 [CrossRef][PubMed]
    [Google Scholar]
  45. Nozaka S., Furukawa S., Sasaki M., Hirayama S., Ogihara H., Morinaga Y.. 2014; Manganese ion increases LAB-yeast mixed-species biofilm formation. Biosci Microbiota Food Health33:79–84 [CrossRef][PubMed]
    [Google Scholar]
  46. Resnekov O., Driks A., Losick R.. 1995; Identification and characterization of sporulation gene spoVS from Bacillus subtilis . J Bacteriol177:5628–5635[PubMed]
    [Google Scholar]
  47. Shemesh M., Kolter R., Losick R.. 2010; The biocide chlorine dioxide stimulates biofilm formation in Bacillus subtilis by activation of the histidine kinase KinC. J Bacteriol192:6352–6356 [CrossRef][PubMed]
    [Google Scholar]
  48. Shemesh M., Chai Y.. 2013; A combination of glycerol and manganese promotes biofilm formation in Bacillus subtilis via histidine kinase KinD signaling. J Bacteriol195:2747–2754 [CrossRef][PubMed]
    [Google Scholar]
  49. Stanley N. R., Lazazzera B. A.. 2005; Defining the genetic differences between wild and domestic strains of Bacillus subtilis that affect poly-gamma-dl-glutamic acid production and biofilm formation. Mol Microbiol57:1143–1158 [CrossRef][PubMed]
    [Google Scholar]
  50. Traxler M. F., Kolter R.. 2015; Natural products in soil microbe interactions and evolution. Nat Prod Rep32:956–970 [CrossRef][PubMed]
    [Google Scholar]
  51. van Gestel J., Weissing F. J., Kuipers O. P., Kovács Á. T.. 2014; Density of founder cells affects spatial pattern formation and cooperation in Bacillus subtilis biofilms. ISME J8:2069–2079 [CrossRef][PubMed]
    [Google Scholar]
  52. van Hijum S. A., García de la Nava J., Trelles O., Kok J., Kuipers O. P.. 2003; MicroPreP: a cDNA microarray data pre-processing framework. Appl Bioinformatics2:241–244[PubMed]
    [Google Scholar]
  53. Vasantha N., Freese E.. 1979; The role of manganese in growth and sporulation of Bacillus subtilis . J Gen Microbiol112: [CrossRef][PubMed]
    [Google Scholar]
  54. Veening J. W., Hamoen L. W., Kuipers O. P.. 2005; Phosphatases modulate the bistable sporulation gene expression pattern in Bacillus subtilis . Mol Microbiol56:1481–1494 [CrossRef][PubMed]
    [Google Scholar]
  55. Veening J. W., Kuipers O. P., Brul S., Hellingwerf K. J., Kort R.. 2006a; Effects of phosphorelay perturbations on architecture, sporulation, and spore resistance in biofilms of Bacillus subtilis . J Bacteriol188:3099–3109 [CrossRef]
    [Google Scholar]
  56. Veening J. W., Smits W. K., Hamoen L. W., Kuipers O. P.. 2006b; Single cell analysis of gene expression patterns of competence development and initiation of sporulation in Bacillus subtilis grown on chemically defined media. J Appl Microbiol101:531–541 [CrossRef]
    [Google Scholar]
  57. Veening J. W., Igoshin O. A., Eijlander R. T., Nijland R., Hamoen L. W., Kuipers O. P.. 2008; Transient heterogeneity in extracellular protease production by Bacillus subtilis . Mol Syst Biol4:184 [CrossRef][PubMed]
    [Google Scholar]
  58. Veening J. W., Murray H., Errington J.. 2009; A mechanism for cell cycle regulation of sporulation initiation in Bacillus subtilis . Genes Dev23:1959–1970 [CrossRef][PubMed]
    [Google Scholar]
  59. Vlamakis H., Chai Y., Beauregard P., Losick R., Kolter R.. 2013; Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol11:157–168 [CrossRef][PubMed]
    [Google Scholar]
  60. Webb J. S., Thompson L. S., James S., Charlton T., Tolker-Nielsen T., Koch B., Givskov M., Kjelleberg S.. 2003; Cell death in Pseudomonas aeruginosa biofilm development. J Bacteriol185:4585–4592[PubMed][CrossRef]
    [Google Scholar]
  61. Yudkin M. D.. 1987; Structure and function in a Bacillus subtilis sporulation-specific sigma factor: molecular nature of mutations in spoIIAC . J Gen Microbiol133:475–481 [CrossRef][PubMed]
    [Google Scholar]
  62. Zheng G., Yan L. Z., Vederas J. C., Zuber P.. 1999; Genes of the sbo-alb locus of Bacillus subtilis are required for production of the antilisterial bacteriocin subtilosin. J Bacteriol181:7346–7355[PubMed]
    [Google Scholar]
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