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 . .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000320
2016-08-01
2024-12-09
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/8/1468.html?itemId=/content/journal/micro/10.1099/mic.0.000320&mimeType=html&fmt=ahah

References

  1. Anagnostopoulos C., Spizizen J. 1961; Requirements for transformation in Bacillus subtilis . J Bacteriol 81:741
    [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. Bioinformatics 17:509–519 [View Article][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 A 110:E1621E1630 [View Article]
    [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 A 98:11621–11626 [View Article]
    [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 Microbiol 59:1229–1238 [View Article][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 Microbiol 93:587–598 [View Article][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 Bacteriol 192:3406–3413 [View Article]
    [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 Bacteriol 143:971–980[PubMed]
    [Google Scholar]
  9. Charney J., Fisher W., Hegarty C. P. 1951; Managanese as an essential element for sporulation in the genus Bacillus. J Bacteriol 62:145[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 Microbiol 85:418–430 [View Article][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 . Microbiology 161:1092–1104 [View Article][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 Biol 2:e328 [View Article][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 Bacteriol 187:1357–1368 [View Article]
    [Google Scholar]
  14. González-Pastor J. E., Hobbs E. C., Losick R. 2003; Cannibalism by sporulating bacteria. Science 301:510–513 [View Article][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 . Biochemistry 37:1365–1375 [View Article][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 Microbiol 42:1199–1209[PubMed] [CrossRef]
    [Google Scholar]
  17. He K., Bauer C. E. 2014; Chemosensory signaling systems that control bacterial survival. Trends Microbiol 22:389–398 [View Article][PubMed]
    [Google Scholar]
  18. Helmann J. D. 2014; Specificity of metal sensing: iron and manganese homeostasis in Bacillus subtilis . J Biol Chem 289:28112–28120 [View Article][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 A 110:13600–13605 [View Article]
    [Google Scholar]
  20. Hoch J. A. 1993; Regulation of the phosphorelay and the initiation of sporulation in subtilis. Annu Rev Microbiol 47:441–465 [View Article]
    [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 Biol 427:3695–3708 [View Article][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 Bacteriol 192:3915–3924 [View Article][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 Bacteriol 176:5320–5329[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. Microbiology 147:1709–1718 [View Article][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 Microbiol 38:535–542[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 Microbiol 55:739–749 [View Article][PubMed]
    [Google Scholar]
  28. Kobayashi K. 2007; Bacillus subtilis pellicle formation proceeds through genetically defined morphological changes. J Bacteriol 189:4920–4931 [View Article][PubMed]
    [Google Scholar]
  29. Kobayashi K., Iwano M. 2012; BslA(YuaB) forms a hydrophobic layer on the surface of Bacillus subtilis biofilms. Mol Microbiol 85:51–66 [View Article][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 A 100:4678–4683 [View Article][PubMed]
    [Google Scholar]
  31. Kovács Á. T. 2016; Bacterial differentiation via gradual activation of global regulators. Curr Genet 62:125–128 [View Article][PubMed]
    [Google Scholar]
  32. Kovács . T., Kuipers O. P. 2011; Rok regulates yuaB expression during architecturally complex colony development of Bacillus subtilis 168. J Bacteriol 193:998–1002 [View Article][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 Microbiol 85:8–11 [View Article][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 Leeuwenhoek 82:113–122[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 . Nature 390:249–256 [View Article][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 Lett 242:51–57 [View Article][PubMed]
    [Google Scholar]
  37. López D. 2015; Connection of KinC to flotillins and potassium leakage in Bacillus subtilis . Microbiology 161:1180–1181 [View Article][PubMed]
    [Google Scholar]
  38. López D., Kolter R. 2010; Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis . FEMS Microbiol Rev 34:134–149 [View Article][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 A 106:280–285 [View Article]
    [Google Scholar]
  40. López D., Vlamakis H., Losick R., Kolter R. 2009b; Cannibalism enhances biofilm development in Bacillus subtilis . Mol Microbiol 74:609–618 [View Article]
    [Google Scholar]
  41. López D., Vlamakis H., Losick R., Kolter R. 2009c; Paracrine signaling in a bacterium. Genes Dev 23:1631–1638 [View Article]
    [Google Scholar]
  42. López D., Gontang E. A., Kolter R. 2010; Potassium sensing histidine kinase in Bacillus subtilis . Methods Enzymol 471:229–251 [View Article][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 Microbiol 54:616–632 [View Article][PubMed]
    [Google Scholar]
  44. Ng W. L., Bassler B. L. 2009; Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222 [View Article][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 Health 33:79–84 [View Article][PubMed]
    [Google Scholar]
  46. Resnekov O., Driks A., Losick R. 1995; Identification and characterization of sporulation gene spoVS from Bacillus subtilis . J Bacteriol 177:5628–5635[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 Bacteriol 192:6352–6356 [View Article][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 Bacteriol 195:2747–2754 [View Article][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 Microbiol 57:1143–1158 [View Article][PubMed]
    [Google Scholar]
  50. Traxler M. F., Kolter R. 2015; Natural products in soil microbe interactions and evolution. Nat Prod Rep 32:956–970 [View Article][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 J 8:2069–2079 [View Article][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 Bioinformatics 2:241–244[PubMed]
    [Google Scholar]
  53. Vasantha N., Freese E. 1979; The role of manganese in growth and sporulation of Bacillus subtilis . J Gen Microbiol 112: [View Article][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 Microbiol 56:1481–1494 [View Article][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 Bacteriol 188:3099–3109 [View Article]
    [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 Microbiol 101:531–541 [View Article]
    [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 Biol 4:184 [View Article][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 Dev 23:1959–1970 [View Article][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 Microbiol 11:157–168 [View Article][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 Bacteriol 185:4585–4592[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 Microbiol 133:475–481 [View Article][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 Bacteriol 181:7346–7355[PubMed]
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.000320
Loading
/content/journal/micro/10.1099/mic.0.000320
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
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