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Cell envelope related processes in Bacillus subtilis

van den Esker, Mariëlle Henriëtte

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van den Esker, M. H. (2018). Cell envelope related processes in Bacillus subtilis: Cell death, transport and

cold shock. Rijksuniversiteit Groningen.

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References

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1. Barbe, V. et al. From a consortium sequence to a unified sequence: the Bacillus subtilis 168 reference genome a decade later. Microbiology 155, 1758–1775 (2009).

2. Danhorn, T. & Fuqua, C. Biofilm formation by plant-associated bacteria. Annu. Rev. Microbiol. 61, 401–422 (2007).

3. Liu, B. et al. Biological control of take-all in wheat by endophytic Bacillus subtilis E1R-j and potential mode of action. Biol. Control 49, 277–285 (2009).

4. Huang, B., Lv, C., Zhuang, P., Zhang, H. & Fan, L. Endophytic colonisation of Bacillus subtilis in the roots of Robinia pseudoacacia L. Plant Biol. 13, 925–931 (2011).

5. Harshey, R. M. Bacterial motility on a surface: Many ways to a common goal. Annu. Rev. Microbiol. 57, 249–273 (2003).

6. Lopez, D., Vlamakis, H. & Kolter, R. Biofilms. Cold Spring Harb Perspect Biol 2, a000398 (2010). 7. Sá-Nogueira, I., Nogueira, T. V, Soares, S. & de Lencastre, H. The Bacillus subtilis L-arabinose

(ara) operon: nucleotide sequence, genetic organization and expression. Microbiology 143, 957–969 (1997).

8. Hirooka, K., Kodoi, Y., Satomura, T. & Fujita, Y. Regulation of the rhaEWRBMA operon involved in l-rhamnose catabolism through two transcriptional factors, RhaR and CcpA, in Bacillus subtilis. J. Bacteriol. 198, 830–845 (2015).

9. Wall, D. H. & Moore, J. C. Interactions underground. Bioscience 49, 109 (1999).

10. Keller, L. & Surette, M. G. Communication in bacteria: an ecological and evolutionary perspective. Nat. Rev. Microbiol. 4, 249–258 (2006).

11. van Overbeek, L. S. et al. Impact of bacterial–fungal interactions on the colonization of the endosphere. Trends Plant Sci. 21, 230–242 (2016).

12. Kunst, F. et al. The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390, 249–256 (1997).

13. Kobayashi, K. et al. Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. U. S. A. 100, 4678–4683 (2003).

14. Commichau, F. M., Pietack, N. & Stülke, J. Essential genes in Bacillus subtilis: a re-evaluation after ten years. Mol. BioSyst. Mol. BioSyst 9, 1068–1075 (2013).

15. Zeigler, D. R. et al. The origins of 168, W23, and other Bacillus subtilis legacy strains. J. Bacteriol. 190, 6983–6995 (2008).

16. Zeigler, D. R. Bacillus Genetic Stock Center. at <http://www.bgsc.org/>

17. Matias, V. R. F. & Beveridge, T. J. Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space. Mol. Microbiol. 56, 240–251 (2005).

18. Matias, V. R. F. & Beveridge, T. J. Native cell wall organization shown by cryo-electron microscopy confirms the existence of a periplasmic space in Staphylococcus aureus. J. Bacteriol. 188, 1011–1021 (2006).

19. Silhavy, T. J., Kahne, D. & Walker, S. The bacterial cell envelope. Cold Spring Harb. Perspect. Biol. 2, a000414 (2010).

20. Leaver, M., Domínguez-Cuevas, P., Coxhead, J. M., Daniel, R. A. & Errington, J. Life without a wall or division machine in Bacillus subtilis. Nature 457, 849–853 (2009).

21. Dufresne, K. & Paradis-Bleau, C. Biology and assembly of the bacterial envelope. Adv. Exp. Med. Biol. 883, 41–76 (2015).

(4)

521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker Processed on: 25-7-2018 Processed on: 25-7-2018 Processed on: 25-7-2018

Processed on: 25-7-2018 PDF page: 117PDF page: 117PDF page: 117PDF page: 117

117 23. Mitrophanov, A. Y. & Groisman, E. A. Signal integration in bacterial two-component

regulatory systems. Genes Dev. 22, 2601–2611 (2008).

24. Vollmer, W. et al. Peptidoglycan structure and architecture. FEMS Microbiol. Rev. 32, 149–167 (2008).

25. Bhavsar, A. P. & Brown, E. D. Cell wall assembly in Bacillus subtilis: how spirals and spaces challenge paradigms. Mol. Microbiol. 60, 1077–1090 (2006).

26. Boylen, C. W. & Ensign, J. C. Ratio of teichoic acid and peptidoglycan in cell walls of Bacillus subtilis following spore germination and during vegetative growth. J. Bacteriol. 96, 421–427 (1968).

27. Ellwood, D. C. The wall content and composition of Bacillus substilis var. niger grown in a chemostat. Biochem. J. 118, 367–373 (1970).

28. Brown, S., Santa Maria, J. P. & Walker, S. Wall teichoic acids of gram-positive bacteria. Annu. Rev. Microbiol. 67, 313–336 (2013).

29. Biswas, R. et al. Proton-binding capacity of Staphylococcus aureus wall teichoic acid and its role in controlling autolysin activity. PLoS One 7, e41415 (2012).

30. Neuhaus, F. C. & Baddiley, J. A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol. Mol. Biol. Rev. 67, 686–723 (2003). 31. Ward, J. B. Teichoic and teichuronic acids: biosynthesis, assembly, and location. Microbiol. Rev.

45, 211–243 (1981).

32. Bhavsar, A. P., Erdman, L. K., Schertzer, J. W. & Brown, E. D. Teichoic acid is an essential polymer in Bacillus subtilis that is functionally distinct from teichuronic acid. J. Bacteriol. 186, 7865–7873 (2004).

33. D’Elia, M. A., Millar, K. E., Beveridge, T. J. & Brown, E. D. Wall teichoic acid polymers are dispensable for cell viability in Bacillus subtilis. J. Bacteriol. 188, 8313–8316 (2006).

34. Schirner, K., Marles-Wright, J., Lewis, R. J. & Errington, J. Distinct and essential morphogenic functions for wall- and lipo-teichoic acids in Bacillus subtilis. EMBO J. 28, 830–842 (2009). 35. Demoling, F., Figueroa, D. & Bååth, E. Comparison of factors limiting bacterial growth in

different soils. Soil Biol. Biochem. 39, 2485–2495 (2007).

36. Koch, A. L. Microbial physiology and ecology of slow growth. Microbiol. Mol. Biol. Rev. 61, 305–318 (1997).

37. Coleman, D. C., Cole, C. V., Hunt, H. W. & Klein, D. A. Trophic interactions in soils as they affect energy and nutrient dynamics. Microb. Ecol. 4, 345–349 (1978).

38. Buchanan, M. & King, L. D. Seasonal fluctuations in soil microbial biomass carbon, phosphorus, and activity in no-till and reduced-chemical-input maize agroecosystems. Biol. Fertil. Soils 13, 211–217 (1992).

39. Dills, S. S., Apperson, A., Schmidt, M. R. & Saier, M. H. Carbohydrate transport in bacteria. Microbiol. Rev. 44, 385–418 (1980).

40. Willey, J. M., Sherwood, L. & Woolverton, C. J. in Prescott’s microbiology (McGraw-Hill Higher Education, 2013).

41. Golby, P., Davies, S., Kelly, D. J., Guest, J. R. & Andrews, S. C. Identification and characterization of a two-component sensor-kinase and response-regulator system (DcuS-DcuR) controlling gene expression in response to C4-dicarboxylates in Escherichia coli. J. Bacteriol. 181, 1238–1248 (1999).

(5)

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Processed on: 25-7-2018 PDF page: 118PDF page: 118PDF page: 118PDF page: 118

118

42. Tanaka, K., Kobayashi, K. & Ogasawara, N. The Bacillus subtilis YufLM two-component system regulates the expression of the malate transporters MaeN (YufR) and YflS, and is essential for utilization of malate in minimal medium. Microbiology 149, 2317–2329 (2003).

43. Graf, S., Schmieden, D., Tschauner, K., Hunke, S. & Unden, G. The sensor kinase DctS forms a tripartite sensor unit with DctB and DctA for Sensing C4-dicarboxylates in Bacillus subtilis. J. Bacteriol. 196, 1084–1093 (2013).

44. Sonenshein, A. L. Control of key metabolic intersections in Bacillus subtilis. Nat. Rev. Microbiol. 5, 917–927 (2007).

45. Kleijn, R. J. et al. Metabolic fluxes during strong carbon catabolite repression by malate in Bacillus subtilis. J. Biol. Chem. 285, 1587–1596 (2010).

46. Meyer, F. M. et al. Malate-mediated carbon catabolite repression in Bacillus subtilis involves the HPrK/CcpA pathway. J. Bacteriol. 193, 6939–6949 (2011).

47. Fujita, Y. Carbon catabolite control of the metabolic network in Bacillus subtilis. Biosci. Biotechnol. Biochem. 73, 245–259 (2009).

48. Marciniak, B. C. et al. High- and low-affinity cre boxes for CcpA binding in Bacillus subtilis revealed by genome-wide analysis. BMC Genomics 13, 401 (2012).

49. Vollmer, W., Joris, B., Charlier, P. & Foster, S. Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol. Rev. 32, 259–286 (2008).

50. Schlag, M. et al. Role of staphylococcal wall teichoic acid in targeting the major autolysin Atl. Mol. Microbiol. 75, 864–873 (2010).

51. Fedtke, I. et al. A Staphylococcus aureus ypfP mutant with strongly reduced lipoteichoic acid (LTA) content: LTA governs bacterial surface properties and autolysin activity. Mol. Microbiol. 65, 1078–1091 (2007).

52. Wecke, J., Madela, K. & Fischer, W. The absence of D-alanine from lipoteichoic acid and wall teichoic acid alters surface charge, enhances autolysis and increases susceptibility to methicillin in Bacillus subtilis. Microbiology 143, 2953–2960 (1997).

53. Peschel, A., Vuong, C., Otto, M. & Götz, F. The D-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolytic enzymes. Antimicrob. Agents Chemother. 44, 2845–2847 (2000).

54. Yamamoto, H., Miyake, Y., Hisaoka, M., Kurosawa, S.-I. & Sekiguchi, J. The major and minor wall teichoic acids prevent the sidewall localization of vegetative DL-endopeptidase LytF in Bacillus subtilis. Mol. Microbiol. 70, 297–310 (2008).

55. Lewis, K. Programmed death in bacteria. Microbiol. Mol. Biol. Rev. 64, 503–514 (2000). 56. Branda, S. S., Vik, S., Friedman, L. & Kolter, R. Biofilms: the matrix revisited. Trends Microbiol.

13, 20–26 (2005).

57. Bayles, K. W. The biological role of death and lysis in biofilm development. Nat. Rev. Microbiol. 5, 721–726 (2007).

58. Groicher, K. H., Firek, B. a, Fujimoto, D. F. & Bayles, K. W. The Staphylococcus aureus lrgAB operon modulates murein hydrolase activity and penicillin tolerance. J. Bacteriol. 182, 1794–1801 (2000).

59. Yang, S. et al. A LysR-type regulator, CidR, is required for induction of the Staphylococcus aureus cidABC operon. J. Bacteriol. 187, 5893–5900 (2005).

60. Ranjit, D. K., Endres, J. L. & Bayles, K. W. Staphylococcus aureus CidA and LrgA proteins exhibit holin-like properties. J. Bacteriol. 193, 2468–2476 (2011).

(6)

521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker Processed on: 25-7-2018 Processed on: 25-7-2018 Processed on: 25-7-2018

Processed on: 25-7-2018 PDF page: 119PDF page: 119PDF page: 119PDF page: 119

119 61. Rice, K. C. & Bayles, K. W. Molecular control of bacterial death and lysis. Microbiol. Mol. Biol.

Rev. 72, 85–109 (2008).

62. Rice, K. C. et al. The Staphylococcus aureus cidAB operon : Evaluation of its role in regulation of murein hydrolase activity and penicillin tolerance. J. Bacteriol. 185, 2635–2643 (2003). 63. Lehman, M. K. et al. Identification of the amino acids essential for LytSR-mediated signal

transduction in Staphylococcus aureus and their roles in biofilm-specific gene expression. Mol. Microbiol. 95, 723–737 (2015).

64. Sharma-Kuinkel, B. K. et al. The Staphylococcus aureus LytSR two-component regulatory system affects biofilm formation. J. Bacteriol. 191, 4767–4775 (2009).

65. Yang, S.-J., Dunman, P. M., Projan, S. J. & Bayles, K. W. Characterization of the Staphylococcus aureus CidR regulon: elucidation of a novel role for acetoin metabolism in cell death and lysis. Mol. Microbiol. 60, 458–468 (2006).

66. Chaudhari, S. S. et al. The LysR-type transcriptional regulator, CidR, regulates stationary phase cell death in Staphylococcus aureus. Mol. Microbiol. 101, 942–953 (2016).

67. Ahn, S.-J., Qu, M.-D., Roberts, E., Burne, R. a & Rice, K. C. Identification of the Streptococcus mutans LytST two-component regulon reveals its contribution to oxidative stress tolerance. BMC Microbiol. 12, 187 (2012).

68. Chandramohan, L., Ahn, J.-S., Weaver, K. E. & Bayles, K. W. An overlap between the control of programmed cell death in Bacillus anthracis and sporulation. J. Bacteriol. 191, 4103–4110 (2009). 69. Zhu, T. et al. Impact of the Staphylococcus epidermidis LytSR two-component regulatory system

on murein hydrolase activity, pyruvate utilization and global transcriptional profile. BMC Microbiol. 10, 287 (2010).

70. Weber, M. H. W. & Marahiel, M. A. Coping with the cold: the cold shock response in the Gram-positive soil bacterium Bacillus subtilis. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 357, 895–907 (2002).

71. Barria, C., Malecki, M. & Arraiano, C. M. Bacterial adaptation to cold. Microbiology 159, 2437–2443 (2013).

72. Schumann, W. Regulation of bacterial heat shock stimulons. Cell Stress Chaperones 21, 959 (2016).

73. Ermolenko, D. N. & Makhatadze, G. I. Bacterial cold-shock proteins. Cell. Mol. Life Sci. 59, 1902–1913 (2002).

74. Beranová, J., Jemioła-Rzeminska, M., Elhottová, D., Strzałka, K. & Konopásek, I. Metabolic control of the membrane fluidity in Bacillus subtilis during cold adaptation. Biochim. Biophys. Acta 1778, 445–453 (2008).

75. Bierhanzl, V. M., Riesová, M., Taraba, L., Cabala, R. & Seydlová, G. Analysis of phosphate and phosphate containing headgroups enzymatically cleaved from phospholipids of Bacillus subtilis by capillary electrophoresis. Anal. Bioanal. Chem. 407, 7215–7220 (2015).

76. Kaneda, T. Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol. Rev. 55, 288–302 (1991).

77. Weber, M. H. W., Klein, W., Müller, L., Niess, U. M. & Marahiel, M. A. Role of the Bacillus subtilis fatty acid desaturase in membrane adaptation during cold shock. Mol. Microbiol. 39, 1321–1329 (2001).

(7)

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Processed on: 25-7-2018 PDF page: 120PDF page: 120PDF page: 120PDF page: 120

120

78. Beckering, C. L., Steil, L., Weber, M. H. W., Völker, U. & Marahiel, M. A. Genomewide transcriptional analysis of the cold shock response in Bacillus subtilis. J. Bacteriol. 184, 6395–6402 (2002).

79. Wiegeshoff, F., Beckering, C. L., Debarbouille, M. & Marahiel, M. A. Sigma L is important for cold shock adaptation of Bacillus subtilis. J. Bacteriol. 188, 3130–3133 (2006).

80. Brunskill, E. W. & Bayles, K. W. Identification of LytSR-regulated genes from Staphylococcus aureus. J. Bacteriol. 178, 5810–2 (1996).

81. Patton, T. G., Yang, S. & Bayles, K. W. The role of proton motive force in expression of the Staphylococcus aureus cid and lrg operons. Mol. Microbiol. 59, 1395–1404 (2006).

82. Rice, K. C., Nelson, J. B., Patton, T. G., Bayles, K. W. & Yang, S. Acetic acid induces expression of the Staphylococcus aureus cidABC and lrgAB murein hydrolase regulator operons. J. Bacteriol. 187, 813–821 (2005).

83. Thomas, V. C. et al. A central role for carbon-overflow pathways in the modulation of bacterial cell death. PLoS Pathog. 10, e1004205 (2014).

84. Kobayashi, K. et al. Comprehensive DNA microarray analysis of Bacillus subtilis two-component regulatory systems. J. Bacteriol. 183, 7365–7370 (2001).

85. Moreno, M. S., Schneider, B. L., Maile, R. R., Weyler, W. & Saier, M. H. Catabolite repression mediated by the CcpA protein in Bacillus subtilis: novel modes of regulation revealed by whole-genome analyses. Mol. Microbiol. 39, 1366–1381 (2004).

86. Detert Oude Weme, R., Seidel, G. & Kuipers, O. P. Probing the regulatory effects of specific mutations in three major binding domains of the pleiotropic regulator CcpA of Bacillus subtilis. Front. Microbiol. 6, 1051 (2015).

87. Lehnik-Habrink, M. et al. DEAD-Box RNA helicases in Bacillus subtilis have multiple functions and act independently from each other. J. Bacteriol. 195, 534–44 (2013).

88. Chen, Y., Gozzi, K., Yan, F. & Chai, Y. Acetic acid acts as a volatile signal to stimulate bacterial biofilm formation. MBio 6, e00392 (2015).

89. Krogh, A., Larsson, B., von Heijne, G. & Sonnhammer, E. L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567–80 (2001).

90. Biasini, M. et al. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 42, W252-8 (2014).

91. Nicolas, P. et al. Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science (80-. ). 335, 1103–6 (2012).

92. Patton, T. G., Rice, K. C., Foster, M. K. & Bayles, K. W. The Staphylococcus aureus cidC gene encodes a pyruvate oxidase that affects acetate metabolism and cell death in stationary phase. Mol. Microbiol. 56, 1664–74 (2005).

93. Brunskill, E. W. & Bayles, K. W. Identification and molecular characterization of a putative regulatory locus that affects autolysis in Staphylococcus aureus. J. Bacteriol. 178, 611–8 (1996). 94. Sierro, N., Makita, Y., de Hoon, M. & Nakai, K. DBTBS: a database of transcriptional regulation

in Bacillus subtilis containing upstream intergenic conservation information. Nucleic Acids Res. 36, D93–D96 (2008).

95. Kleijn, R. J. et al. Metabolic fluxes during strong carbon catabolite repression by malate in Bacillus subtilis. J. Biol. Chem. 285, 1587–1596 (2010).

(8)

521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker Processed on: 25-7-2018 Processed on: 25-7-2018 Processed on: 25-7-2018

Processed on: 25-7-2018 PDF page: 121PDF page: 121PDF page: 121PDF page: 121

121 96. Sonenshein, A. L. Control of key metabolic intersections in Bacillus subtilis. Nat. Rev. Microbiol.

5, 917–927 (2007).

97. Jolkver, E. et al. Identification and Characterization of a bacterial transport system for the uptake of pyruvate, propionate, and acetate in Corynebacterium glutamicum. J. Bacteriol. 191, 940–948 (2009).

98. Kreth, J., Lengeler, J. W. & Jahreis, K. Characterization of pyruvate uptake in Escherichia coli K-12. PLoS One 8, e67125 (2013).

99. Woodrow. Plants in Action: Adaptation in Nature, Performance in Cultivation. (Macmillan Education Australia, 1999).

100. Sargent, M. G. Control of cell length in Bacillus subtilis. J. Bacteriol. 123, 7–19 (1975).

101. Weart, R. B. et al. A metabolic sensor governing cell size in bacteria. Cell 130, 335–47 (2007). 102. Chien, A.-C., Hill, N. S. & Levin, P. A. Cell size control in bacteria. Curr. Biol. 22, R340–R349

(2012).

103. Tomlinson, G. A. & Hochstein, L. I. Studies on acid production during carbohydrate metabolism by extremely halophilic bacteria. Can. J. Microbiol. 18, 1973–1976 (1972).

104. Ruby, E. G. & Nealson, K. H. Pyruvate production and excretion by the luminous marine bacteria. Appl. Envir. Microbiol. 34, 164–169 (1977).

105. Nakata, H. M. Effect of pH on intermediates produced during growth and sporulation of Bacillus cereus. J. Bacteriol. 86, 577–581 (1963).

106. Kodaki, T., Murakami, H., Taguchi, M., Izui, K. & Katsuki, H. Stringent control of intermediary metabolism in Escherichia coli: pyruvate excretion by cells grown on succinate. J. Biochem. 90, 1437–44 (1981).

107. Sanchez, M. A. Molecular identification and characterization of an essential pyruvate transporter from Trypanosoma brucei. J. Biol. Chem. 288, 14428–37 (2013).

108. Kovács, A. T. & Kuipers, O. P. Rok regulates yuaB expression during architecturally complex colony development of Bacillus subtilis 168. J. Bacteriol. 193, 998–1002 (2011).

109. Harwood, C. R. & Cutting, S. M. Molecular biological methods for Bacillus. (Wiley, 1990). 110. Sambrook, J., Fritsch, E. F. & Maniatis, T. Molecular cloning: A laboratory manual. (Cold Spring

Harbor Laboratory Press, 1989).

111. Konkol, M. A., Blair, K. M. & Kearns, D. B. Plasmid-encoded ComI inhibits competence in the ancestral 3610 strain of Bacillus subtilis. J. Bacteriol. 195, 4085–4093 (2013).

112. Wertman, K. F., Wyman, A. R. & Botstein, D. Host/vector interactions which affect the viability of recombinant phage lambda clones. Gene 49, 253–262 (1986).

113. Hahn, J., Luttinger, A. & Dubnau, D. Regulatory inputs for the synthesis of ComK, the competence transcription factor of Bacillus subtilis. Mol. Microbiol. 21, 763–75 (1996).

114. Scholz, O., Thiel, A., Hillen, W. & Niederweis, M. Quantitative analysis of gene expression with an improved green fluorescent protein. Eur. J. Biochem. 267, 1565–70 (2000).

115. Veening, J.-W., Murray, H. & Errington, J. A mechanism for cell cycle regulation of sporulation initiation in Bacillus subtilis. Genes Dev. 23, 1959–70 (2009).

116. Itaya, M. Construction of a novel tetracycline resistance gene cassette useful as a marker on the Bacillus subtilis chromosome. Biosci. Biotechnol. Biochem. 56, 685–686 (1992).

117. Kim, L., Mogk, A. & Schumann, W. A xylose-inducible Bacillus subtilis integration vector and its application. Gene 181, 71–76 (1996).

(9)

521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker Processed on: 25-7-2018 Processed on: 25-7-2018 Processed on: 25-7-2018

Processed on: 25-7-2018 PDF page: 122PDF page: 122PDF page: 122PDF page: 122

122

118. Tomita, S. et al. Comparison of components and synthesis genes of cell wall teichoic acid among Lactobacillus plantarum strains. Biosci. Biotechnol. Biochem. 74, 928–933 (2010).

119. Wecke, J., Madela, K. & Fischer, W. The absence of D-alanine from lipoteichoic acid and wall teichoic acid alters surface charge, enhances autolysis and increases susceptibility to methicillin in Bacillus subtilis. Microbiology 143, 2953–2960 (1997).

120. Wickham, J. R., Halye, J. L., Kashtanov, S., Khandogin, J. & Rice, C. V. Revisiting magnesium chelation by teichoic acid with phosphorus solid-state NMR and theoretical calculations. J. Phys. Chem. B 113, 2177–2183 (2009).

121. Smith, T. J., Blackman, S. A. & Foster, S. J. Autolysins of Bacillus subtilis : multiple enzymes with multiple functions. Microbiology 146, 249–262 (2000).

122. Kasahara, J. et al. Teichoic acid polymers affect expression and localization of dl-endopeptidase LytE required for lateral cell wall hydrolysis in Bacillus subtilis. J. Bacteriol. 198, 1585–1594 (2016). 123. Wecke, J., Perego, M. & Fischer, W. D-alanine deprivation of Bacillus subtilis teichoic acids is without effect on cell growth and morphology but affects the autolytic activity. Microb. drug Resist. 2, 123–129 (1996).

124. Wecke, J., Madela, K. & Fischer, W. The absence of D-alanine from lipoteichoic acid and wall teichoic acid alters surface charge, enhances autolysis and increases susceptibility to methicillin in Bacillus subtilis. Microbiology 143, 2953–2960 (1997).

125. Kiriyama, Y. et al. Localization and expression of the Bacillus subtilis DL-endopeptidase LytF are influenced by mutations in LTA synthases and glycolipid anchor synthetic enzymes. Microbiology 160, 2639–2649 (2014).

126. Soldo, B., Lazarevic, V. & Karamata, D. tagO is involved in the synthesis of all anionic cell-wall polymers in Bacillus subtilis 168. Microbiology 148, 2079–2087 (2002).

127. Bisicchia, P. et al. The essential YycFG two-component system controls cell wall metabolism in Bacillus subtilis. Mol. Microbiol. 65, 180–200 (2007).

128. Uehara, T. & Bernhardt, T. G. More than just lysins: peptidoglycan hydrolases tailor the cell wall. Curr. Opin. Microbiol. 14, 698–703 (2011).

129. Kasahara, J. et al. Teichoic acid polymers affect expression and localization of dl-endopeptidase LytE required for lateral cell wall hydrolysis in Bacillus subtilis. J. Bacteriol. 198, 1585–1594 (2016). 130. Koch, A. L. The pH in the neighborhood of membranes generating a protonmotive force. J.

Theor. Biol. 120, 73–84 (1986).

131. Kemper, M. A., Urrutia, M. M., Beveridge, T. J., Koch, A. L. & Doyl, A. R. J. Proton motive force may regulate cell wall-associated enzymes of Bacillus subtilis. J. Bacteriol. 175, 5690–5696 (1993).

132. Calamita, H. G. et al. Evidence that the cell wall of Bacillus subtilis is protonated during respiration. Proc. Natl. Acad. Sci. U. S. A. 98, 15260–15263 (2001).

133. Yamada, S. et al. An autolysin ring associated with cell separation of Staphylococcus aureus. J. Bacteriol. 178, 1565–1571 (1996).

134. Baba, T. et al. Targeting of muralytic enzymes to the cell division site of Gram-positive bacteria: repeat domains direct autolysin to the equatorial surface ring of Staphylococcus aureus. EMBO J. 17, 4639–4646 (1998).

135. Westers, H. et al. Genome engineering reveals large dispensable regions in Bacillus subtilis. Mol. Biol. Evol. 20, 2076–2090 (2003).

(10)

521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker Processed on: 25-7-2018 Processed on: 25-7-2018 Processed on: 25-7-2018

Processed on: 25-7-2018 PDF page: 123PDF page: 123PDF page: 123PDF page: 123

123 136. Swoboda, J. G., Campbell, J., Meredith, T. C. & Walker, S. Wall teichoic acid function,

biosynthesis, and inhibition. Chembiochem 11, 35–45 (2010).

137. Müller, J. P. et al. Interaction of Bacillus subtilis CsaA with SecA and precursor proteins. Biochem. J. 348 Pt 2, 367–373 (2000).

138. Fukushima, T. et al. A new D,L-endopeptidase gene product, YojL (renamed CwlS), plays a role in cell separation with LytE and LytF in Bacillus subtilis. J. Bacteriol. 188, 5541–5550 (2006). 139. Moore, C. M., Gaballa, A., Hui, M., Ye, R. W. & Helmann, J. D. Genetic and physiological

responses of Bacillus subtilis to metal ion stress. Mol. Microbiol. 57, 27–40 (2005).

140. Vieira, J. & Messing, J. New pUC-derived cloning vectors with different selectable markers and DNA replication origins. Gene 100, 189–194 (1991).

141. Itaya, M., Kondo, K. & Tanaka, T. A neomycin resistance gene cassette selectable in a single copy state in the Bacillus subtilis chromosome. Nucleic Acids Res. 17, 4410 (1989).

142. de Jong, I. G., Beilharz, K., Kuipers, O. P. & Veening, J.-W. Live cell imaging of Bacillus subtilis and Streptococcus pneumoniae using automated time-lapse microscopy. J. Vis. Exp. 53, e3145, doi: 10.3791/3145 (2011).

143. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).

144. Aranda, P. S., LaJoie, D. M. & Jorcyk, C. L. Bleach gel: a simple agarose gel for analyzing RNA quality. Electrophoresis 33, 366–369 (2012).

145. Skinner, M. E., Uzilov, A. V., Stein, L. D., Mungall, C. J. & Holmes, I. H. JBrowse: A next-generation genome browser. Genome Res. 19, 1630–1638 (2009).

146. de Jong, A., van der Meulen, S., Kuipers, O. P. & Kok, J. T-REx: Transcriptome analysis webserver for RNA-seq expression data. BMC Genomics 16, 663 (2015).

147. Aguilar, P. S., Cronan, J. E. & de Mendoza, D. A Bacillus subtilis gene induced by cold shock encodes a membrane phospholipid desaturase. J. Bacteriol. 180, 2194–2200 (1998).

148. Aguilar, P. S., Hernandez-Arriaga, A. M., Cybulski, L. E., Erazo, A. C. & de Mendoza, D. Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO J. 20, 1681–1691 (2001).

149. Svobodová, J., Julák, J., Pilar, J. & Svoboda, P. Membrane fluidity in Bacillus subtilis. Validity of homeoviscous adaptation. Folia Microbiol. (Praha). 33, 170–177 (1988).

150. Suutari, M. & Laakso, S. Unsaturated and branched chain-fatty acids in temperature adaptation of Bacillus subtilis and Bacillus megaterium. Biochim. Biophys. Acta - Lipids Lipid Metab. 1126, 119–124 (1992).

151. Klein, W., Weber, M. H. W. & Marahiel, M. A. Cold shock response of Bacillus subtilis: Isoleucine-dependent switch in the fatty acid branching pattern for membrane adaptation to low temperatures. J. Bacteriol. 181, 5341–5349 (1999).

152. Hunger, K., Beckering, C. L. & Marahiel, M. A. Genetic evidence for the temperature-sensing ability of the membrane domain of the Bacillus subtilis histidine kinase DesK. FEMS Microbiol. Lett. 230, 41–46 (2004).

153. Graumann, P., Schröder, K., Schmid, R. & Marahiel, M. A. Cold shock stress-induced proteins in Bacillus subtilis. J. Bacteriol. 178, 4611–4619 (1996).

154. Kaan, T., Homuth, G., Mäder, U., Bandow, J. & Schweder, T. Genome-wide transcriptional profiling of the Bacillus subtilis cold-shock response. Microbiology 148, 3441–3455 (2002).

(11)

521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker Processed on: 25-7-2018 Processed on: 25-7-2018 Processed on: 25-7-2018

Processed on: 25-7-2018 PDF page: 124PDF page: 124PDF page: 124PDF page: 124

124

155. Brigulla, M. et al. Chill induction of the SigB-dependent general stress response in Bacillus subtilis and its contribution to low-temperature adaptation. J. Bacteriol. 185, 4305–4314 (2003). 156. Budde, I., Steil, L., Scharf, C., Völker, U. & Bremer, E. Adaptation of Bacillus subtilis to growth at low temperature: a combined transcriptomic and proteomic appraisal. Microbiology 152, 831–853 (2006).

157. Débarbouillé, M., Martin-Verstraete, I., Kunst, F. & Rapoport, G. The Bacillus subtilis sigL gene encodes an equivalent of sigma 54 from gram-negative bacteria. Proc. Natl. Acad. Sci. U. S. A. 88, 9092–9096 (1991).

158. Merrick, M. J. In a class of its own--the RNA polymerase sigma factor sigma 54 (sigma N). Mol. Microbiol. 10, 903–909 (1993).

159. Studholme, D. J. & Buck, M. The biology of enhancer-dependent transcriptional regulation in bacteria: insights from genome sequences. FEMS Microbiol. Lett. 186, 1–9 (2000).

160. Debarbouille, M., Gardan, R., Arnaud, M. & Rapoport, G. Role of BkdR, a transcriptional activator of the sigL-dependent isoleucine and valine degradation pathway in Bacillus subtilis. J. Bacteriol. 181, 2059–2066 (1999).

161. Michna, R. H., Commichau, F. M., Tödter, D., Zschiedrich, C. P. & Stülke, J. SubtiWiki–a database for the model organism Bacillus subtilis that links pathway, interaction and expression information. Nucleic Acids Res. 42, D692–D698 (2014).

162. Grau, R., Gardiol, D., Glikin, G. C. & Mendoza, D. DNA supercoiling and thermal regulation of unsaturated fatty acid synthesis in Bacillus subtilis. Mol. Microbiol. 11, 933–941 (1994). 163. Lenhart, J. S., Schroeder, J. W., Walsh, B. W. & Simmons, L. A. DNA repair and genome

maintenance in Bacillus subtilis. Microbiol. Mol. Biol. Rev. 76, 530–564 (2012).

164. van den Esker, M. H., Kovács, Á. T. & Kuipers, O. P. YsbA and LytST are essential for pyruvate utilization in Bacillus subtilis. Environ. Microbiol. 19, 83–94 (2017).

165. Charbonnier T, Le Coq D, McGovern S, Calabre M, Delumeau O, Aymerich S, J. M. Molecular and physiological logics of the pyruvate-induced response of a novel transporter in Bacillus subtilis. MBio 8, e00976-17 (2017).

166. Fan, G. & Li, J. Regions identity between the genome of vertebrates and non-retroviral families of insect viruses. Virol. J. 8, 1–11 (2011).

167. Ali, N. O., Bignon, J., Rapoport, G. & Debarbouille, M. Regulation of the acetoin catabolic pathway is controlled by sigma L in Bacillus subtilis. J. Bacteriol. 183, 2497–2504 (2001). 168. Martin, I., Debarbouille, M., Klier, A. & Rapoport, G. Induction and metabolite regulation

of levanase synthesis in Bacillus subtilis. J. Bacteriol. 171, 1885–1892 (1989).

169. Débarbouillé, M., Martin-Verstraete, I., Klier, A. & Rapoport, G. The transcriptional regulator LevR of Bacillus subtilis has domains homologous to both sigma 54- and phosphotransferase system-dependent regulators. Proc. Natl. Acad. Sci. U. S. A. 88, 2212–2216 (1991).

170. Calogero, S. et al. RocR, a novel regulatory protein controlling arginine utilization in Bacillus subtilis, belongs to the NtrC/NifA family of transcriptional activators. J. Bacteriol. 176, 1234–1241 (1994).

171. Gardan, R., Rapoport, G. & Débarbouillé, M. Expression of the rocDEF operon involved in arginine catabolism in Bacillus subtilis. J. Mol. Biol. 249, 843–856 (1995).

172. Belitsky, B. R. & Sonenshein, A. L. An enhancer element located downstream of the major glutamate dehydrogenase gene of Bacillus subtilis. Proc. Natl. Acad. Sci. U. S. A. 96, 10290–10295 (1999).

(12)

521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker Processed on: 25-7-2018 Processed on: 25-7-2018 Processed on: 25-7-2018

Processed on: 25-7-2018 PDF page: 125PDF page: 125PDF page: 125PDF page: 125

125 173. Jamalli, A., Hébert, A., Zig, L. & Putzer, H. Control of expression of the RNases J1 and J2 in

Bacillus subtilis. J. Bacteriol. 196, 318–324 (2014).

174. Czaplewski, L. G., North, A. K., Smith, M. C., Baumberg, S. & Stockley, P. G. Purification and initial characterization of AhrC: the regulator of arginine metabolism genes in Bacillus subtilis. Mol. Microbiol. 6, 267–275 (1992).

175. O’Reilly, M., Woodson, K., Dowds, B. C. & Devine, K. M. The citrulline biosynthetic operon, argC-F, and a ribose transport operon, rbs, from Bacillus subtilis are negatively regulated by Spo0A. Mol. Microbiol. 11, 87–98 (1994).

176. Brinsmade, S. R. et al. Hierarchical expression of genes controlled by the Bacillus subtilis global regulatory protein CodY. Proc. Natl. Acad. Sci. U. S. A. 111, 8227–8232 (2014).

177. Asadishad, B., Olsson, A. L. J., Dusane, D. H., Ghoshal, S. & Tufenkji, N. Transport, motility, biofilm forming potential and survival of Bacillus subtilis exposed to cold temperature and freeze–thaw. Water Res. 58, 239–247 (2014).

178. Lahooti, M. & Harwood, C. R. Transcriptional analysis of the Bacillus subtilis teichuronic acid operon. Microbiology 145, 3409–3417 (1999).

179. Allenby, N. E. E. et al. Post-transcriptional regulation of the Bacillus subtilis pst operon encoding a phosphate-specific ABC transporter. Microbiology 150, 2619–2628 (2004).

180. Muller, J. P., An, Z., Merad, T., Hancock, I. C. & Harwood, C. R. Influence of Bacillus subtilis phoR on cell wall anionic polymers. Microbiology 47, 43947–43956 (2016).

181. Lide, D. Aqueous solubility of inorganic compounds at various temperatures. 8, 112–117 182. Prayitno, N. R. & Archibald, A. R. The effects of growth conditions on cell wall composition

and cell morphology in a temperature-sensitive tag-B mutant of Bacillus subtilis. World J. Microbiol. Biotechnol. 13, 207–217 (1997).

183. Liu, B., Zhang, Y. & Zhang, W. RNA-Seq-based analysis of cold shock response in Thermoanaerobacter tengcongensis, a bacterium harboring a single cold shock protein encoding gene. PLoS One 9, e93289 (2014).

184. Graumann, P. & Marahiel, M. A. Some like it cold: response of microorganisms to cold shock. Arch. Microbiol. 166, 293–300 (1996).

185. Jones, P. G., Cashel, M., Glaser, G. & Neidhardt, F. C. Function of a relaxed-like state following temperature downshifts in Escherichia coli. J. Bacteriol. 174, 3903–3914 (1992).

186. Umbarger, H. E. Amino acid biosynthesis and its regulation. Annu. Rev. Biochem. 47, 533–606 (1978).

187. Oku, H. & Kaneda, T. Biosynthesis of branched-chain fatty acids in Bacillus subtilis. A decarboxylase is essential for branched-chain fatty acid synthetase. J. Biol. Chem. 263, 18386– 18396 (1988).

188. Schujman, G. E., Paoletti, L., Grossman, A. D. & de Mendoza, D. FapR, a bacterial transcription factor involved in global regulation of membrane lipid biosynthesis. Dev. Cell 4, 663–672 (2003). 189. Fujita, Y., Matsuoka, H. & Hirooka, K. Regulation of fatty acid metabolism in bacteria. Mol.

Microbiol. 66, 829–839 (2007).

190. Zhang, X., St Leger, R. J. & Fang, W. Pyruvate accumulation is the first line of cell defense against heat stress in a fungus. MBio 8, e01284-17 (2017).

191. García-Ríos, E., Ramos-Alonso, L. & Guillamón, J. M. Correlation between low temperature adaptation and oxidative stress in Saccharomyces cerevisiae. Front. Microbiol. 7, 1199 (2016).

(13)

521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker Processed on: 25-7-2018 Processed on: 25-7-2018 Processed on: 25-7-2018

Processed on: 25-7-2018 PDF page: 126PDF page: 126PDF page: 126PDF page: 126

126

192. Sinetova, M. A. & Los, D. A. New insights in cyanobacterial cold stress responses: Genes, sensors, and molecular triggers. Biochim. Biophys. Acta - Gen. Subj. 1860, 2391–2403 (2016). 193. Karami-Moalem, S., Maali-Amiri, R. & Kazemi-Shahandashti, S.-S. Effect of cold stress on

oxidative damage and mitochondrial respiratory properties in chickpea. Plant Physiol. Biochem. 122, 31–39 (2018).

194. Hoch, J. A. & Mathews, J. L. Chromosomal location of pleiotropic negative sporulation mutations in Bacillus subtilis. Genetics 73, 215–228 (1973).

195. Baerends, R. J. S. et al. Genome2D: a visualization tool for the rapid analysis of bacterial transcriptome data. Genome Biol. 5, R37 (2004).

196. Nazir, R., Warmink, J. A., Boersma, H. & van Elsas, J. D. Mechanisms that promote bacterial fitness in fungal-affected soil microhabitats. FEMS Microbiol. Ecol. 71, 169–185 (2010). 197. Tarkka, M. T., Sarniguet, A. & Frey-Klett, P. Inter-kingdom encounters: recent advances in

molecular bacterium-fungus interactions. Curr. Genet. 55, 233–43 (2009).

198. Frey-Klett, P. et al. Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol. Mol. Biol. Rev. 75, 583–609 (2011). 199. Kluge, M. A fungus eats a cyanobacterium: The story of the Geosiphon pyriformis endocyanosis.

Biology and Environment: Proceedings of the Royal Irish Academy 102, 11–14 (2002).

200. Partida-Martinez, L. P. & Hertweck, C. Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437, 884–888 (2005).

201. Hogan, D. A. & Kolter, R. Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296, 2229–2232 (2002).

202. Peters, B. M. et al. Microbial interactions and differential protein expression in Staphylococcus aureus -Candida albicans dual-species biofilms. FEMS Immunol. Med. Microbiol. 59, 493–503 (2010). 203. Gibson, J., Sood, A. & Hogan, D. A. Pseudomonas aeruginosa-Candida albicans interactions:

localization and fungal toxicity of a phenazine derivative. Appl. Environ. Microbiol. 75, 504–513 (2009).

204. Morales, D. K. et al. Antifungal mechanisms by which a novel Pseudomonas aeruginosa phenazine toxin kills Candida albicans in biofilms. Mol. Microbiol. 78, 1379–1392 (2010).

205. Holcombe, L. J. et al. Pseudomonas aeruginosa secreted factors impair biofilm development in Candida albicans. Microbiology 156, 1476–1486 (2010).

206. Peters, B. M. et al. Staphylococcus aureus adherence to Candida albicans hyphae is mediated by the hyphal adhesin Als3p. Microbiology 158, 2975–2986 (2012).

207. Scherlach, K., Graupner, K. & Hertweck, C. Molecular bacteria-fungi interactions: effects on environment, food, and medicine. Annu. Rev. Biochem. 67, 375–397 (2013).

208. Nützmann, H.-W. et al. Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation. Proc. Natl. Acad. Sci. U. S. A. 108, 14282–7 (2011).

209. König, C. C. et al. Bacterium induces cryptic meroterpenoid pathway in the pathogenic fungus Aspergillus fumigatus. Chembiochem 14, 938–42 (2013).

210. Nützmann, H.-W., Fischer, J., Scherlach, K., Hertweck, C. & Brakhage, A. A. Distinct amino acids of histone H3 control secondary metabolism in Aspergillus nidulans. Appl. Environ. Microbiol. 79, 6102–6109 (2013).

(14)

521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker Processed on: 25-7-2018 Processed on: 25-7-2018 Processed on: 25-7-2018

Processed on: 25-7-2018 PDF page: 127PDF page: 127PDF page: 127PDF page: 127

127 211. Ingham, C. J., Kalisman, O., Finkelshtein, A. & Ben-Jacob, E. Mutually facilitated dispersal

between the nonmotile fungus Aspergillus fumigatus and the swarming bacterium Paenibacillus vortex. Proc. Natl. Acad. Sci. U. S. A. 108, 19731–19736 (2011).

212. Nurmiaho-Lassila, E.-L., Timonen, S., Haahtela, K. & Sen, R. Bacterial colonization patterns of intact Pinus sylvestris mycorrhizospheres in dry pine forest soil: an electron microscopy study. Can. J. Microbiol. 43, 1017–1035 (1997).

213. Kawarai, T., Furukawa, S., Ogihara, H. & Yamasaki, M. Mixed-species biofilm formation by lactic acid bacteria and rice wine yeasts. Appl. Environ. Microbiol. 73, 4673–4676 (2007). 214. Artursson, V. & Jansson, J. K. Use of bromodeoxyuridine immunocapture to identify active

bacteria associated with arbuscular mycorrhizal hyphae. Appl. Environ. Microbiol. 69, 6208–6215 (2003).

215. Papagianni, M. Advances in citric acid fermentation by Aspergillus niger: biochemical aspects, membrane transport and modeling. Biotechnol. Adv. 25, 244–263 (2007).

216. Kwon, M. J. et al. The transcriptomic fingerprint of glucoamylase over-expression in Aspergillus niger. BMC Genomics 13, 701 (2012).

217. Westers, L., Westers, H. & Quax, W. J. Bacillus subtilis as cell factory for pharmaceutical proteins: a biotechnological approach to optimize the host organism. Biochim. Biophys. Acta 1694, 299–310 (2004).

218. Antelmann, H., Van Dijl, J. M., Bron, S. & Hecker, M. Proteomic survey through secretome of Bacillus subtilis. Methods Biochem. Anal. 49, 179–208 (2006).

219. Branda, S. S., González-Pastor, J. E., Ben-Yehuda, S., Losick, R. & Kolter, R. Fruiting body formation by Bacillus subtilis. Proc. Natl. Acad. Sci. U. S. A. 98, 11621–11626 (2001).

220. Kearns, D. B. & Losick, R. Swarming motility in undomesticated Bacillus subtilis. Mol. Microbiol. 49, 581–590 (2003).

221. Mhatre, E., Monterrosa, R. G. & Kovács, A. T. From environmental signals to regulators: modulation of biofilm development in Gram-positive bacteria. J. Basic Microbiol. 54, 616–632 (2014).

222. Chen, Y. et al. A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants. Mol. Microbiol. 85, 418–430 (2012).

223. Beauregard, P. B., Chai, Y., Vlamakis, H., Losick, R. & Kolter, R. Bacillus subtilis biofilm induction by plant polysaccharides. Proc. Natl. Acad. Sci. 110, 1621–1630 (2013).

224. Chen, Y. et al. Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ. Microbiol. 15, 848–864 (2013).

225. Ruepp, A. et al. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 32, 5539–5545 (2004).

226. Andersen, M. R., Nielsen, M. L. & Nielsen, J. Metabolic model integration of the bibliome, genome, metabolome and reactome of Aspergillus niger. Mol. Syst. Biol. 4, 178 (2008).

227. Arnaud, M. B. et al. The Aspergillus Genome Database, a curated comparative genomics resource for gene, protein and sequence information for the Aspergillus research community. Nucleic Acids Res. 38, 420–427 (2010).

228. Lee, B. N. & Adams, T. H. The Aspergillus nidulans fluG gene is required for production of an extracellular developmental signal and is related to prokaryotic glutamine synthetase I. Genes Dev. 8, 641–651 (1994).

(15)

521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker Processed on: 25-7-2018 Processed on: 25-7-2018 Processed on: 25-7-2018

Processed on: 25-7-2018 PDF page: 128PDF page: 128PDF page: 128PDF page: 128

128

229. Breakspear, A. & Momany, M. Aspergillus nidulans conidiation genes dewA, fluG, and stuA are differentially regulated in early vegetative growth. Eukaryot. Cell 6, 1697–1700 (2007). 230. Daboussi, M. J. et al. Heterologous expression of the Aspergillus nidulans regulatory gene nirA in

Fusarium oxysporum. Gene 109, 155–160 (1991).

231. Narendja, F., Goller, S. P., Wolschek, M. & Strauss, J. Nitrate and the GATA factor AreA are necessary for in vivo binding of NirA, the pathway-specific transcriptional activator of Aspergillus nidulans. Mol. Microbiol. 44, 573–583 (2002).

232. Schinko, T., Gallmetzer, A., Amillis, S. & Strauss, J. Pseudo-constitutivity of nitrate-responsive genes in nitrate reductase mutants. Fungal Genet. Biol. 54, 34–41 (2013).

233. Keller & Hohn. Metabolic pathway gene clusters in filamentous fungi. Fungal Genet. Biol. 21, 17–29 (1997).

234. Khaldi, N. et al. SMURF: Genomic mapping of fungal secondary metabolite clusters. Fungal Genet. Biol. 47, 736–741 (2010).

235. Metzger, U. et al. The structure of dimethylallyl tryptophan synthase reveals a common architecture of aromatic prenyltransferases in fungi and bacteria. Proc. Natl. Acad. Sci. U. S. A. 106, 14309–14314 (2009).

236. Inglis, D. O. et al. Comprehensive annotation of secondary metabolite biosynthetic genes and gene clusters of Aspergillus nidulans, A. fumigatus, A. niger and A. oryzae. BMC Microbiol. 13, 91 (2013). 237. Andersen, M. R. et al. Accurate prediction of secondary metabolite gene clusters in filamentous

fungi. Proc. Natl. Acad. Sci. U. S. A. 110, E99-107 (2013).

238. Eichenberger, P. et al. The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis. PLoS Biol. 2, e328 (2004).

239. Cangiano, G. et al. Direct and indirect control of late sporulation genes by GerR of Bacillus subtilis. J. Bacteriol. 192, 3406–3413 (2010).

240. Ramirez-Peralta, A. et al. Effects of the SpoVT regulatory protein on the germination and germination protein levels of spores of Bacillus subtilis. J. Bacteriol. 194, 3417–3425 (2012). 241. Vishnoi, M. et al. Triggering sporulation in Bacillus subtilis with artificial two-component

systems reveals the importance of proper Spo0A activation dynamics. Mol. Microbiol. 90, 181–194 (2013).

242. Nakano, M., Dailly, Y., Zuber, P. & Clark, D. Characterization of anaerobic fermentative growth of Bacillus subtilis: identification of fermentation end products and genes required for growth. J. Bacteriol. 179, 6749–6755 (1997).

243. Derré, I., Rapoport, G. & Msadek, T. CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in gram-positive bacteria. Mol. Microbiol. 31, 117–131 (1999).

244. Helmann, J. D. Deciphering a complex genetic regulatory network: the Bacillus subtilis sigmaW protein and intrinsic resistance to antimicrobial compounds. Sci. Prog. 89, 243–266 (2006). 245. Nakano, M. M. et al. srfA is an operon required for surfactin production, competence

development, and efficient sporulation in Bacillus subtilis. J. Bacteriol. 173, 1770–1778 (1991). 246. Grangemard, I., Wallach, J., Maget-Dana, R. & Peypoux, F. Lichenysin: a more efficient cation

chelator than surfactin. Appl. Biochem. Biotechnol. 90, 199–210 (2001).

247. Singh, P. & Cameotra, S. S. Potential applications of microbial surfactants in biomedical sciences. Trends Biotechnol. 22, 142–146 (2004).

(16)

521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker Processed on: 25-7-2018 Processed on: 25-7-2018 Processed on: 25-7-2018

Processed on: 25-7-2018 PDF page: 129PDF page: 129PDF page: 129PDF page: 129

129 248. Lopez, D., Vlamakis, H., Losick, R. & Kolter, R. Paracrine signaling in a bacterium. Genes Dev.

23, 1631–1638 (2009).

249. Mohammadipour, M., Mousivand, M., Salehi Jouzani, G. & Abbasalizadeh, S. Molecular and biochemical characterization of Iranian surfactin-producing Bacillus subtilis isolates and evaluation of their biocontrol potential against Aspergillus flavus and Colletotrichum gloeosporioides. Can. J. Microbiol. 55, 395–404 (2009).

250. Velho, R. V, Medina, L. F. C., Segalin, J. & Brandelli, A. Production of lipopeptides among Bacillus strains showing growth inhibition of phytopathogenic fungi. Folia Microbiol. (Praha). 56, 297–303 (2011).

251. López, D., Fischbach, M. a, Chu, F., Losick, R. & Kolter, R. Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. Proc. Natl. Acad. Sci. U. S. A. 106, 280–285 (2009).

252. Brandl, M. T. et al. Salmonella biofilm formation on Aspergillus niger involves cellulose--chitin interactions. PLoS One 6, e25553 (2011).

253. Dijksterhuis, J., Sanders, M., Gorris, L. G. & Smid, E. J. Antibiosis plays a role in the context of direct interaction during antagonism of Paenibacillus polymyxa towards Fusarium oxysporum. J. Appl. Microbiol. 86, 13–21 (1999).

254. Vinck, A. et al. Hyphal differentiation in the exploring mycelium of Aspergillus niger. Mol. Microbiol. 58, 693–699 (2005).

255. Schrey, S. D., Schellhammer, M., Ecke, M., Hampp, R. & Tarkka, M. T. Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol. 168, 205–216 (2005).

256. Deveau, A. et al. The mycorrhiza helper Pseudomonas fluorescens BBc6R8 has a specific priming effect on the growth, morphology and gene expression of the ectomycorrhizal fungus Laccaria bicolor S238N. New Phytol. 175, 743–755 (2007).

257. Maligoy, M., Mercade, M., Cocaign-Bousquet, M. & Loubiere, P. Transcriptome analysis of Lactococcus lactis in coculture with Saccharomyces cerevisiae. Appl. Environ. Microbiol. 74, 485–494 (2008).

258. Schroeckh, V. et al. Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc. Natl. Acad. Sci. U. S. A. 106, 14558–14563 (2009). 259. Moretti, M. et al. A proteomics approach to study synergistic and antagonistic interactions of

the fungal-bacterial consortium Fusarium oxysporum wild-type MSA 35. Proteomics 10, 3292– 3320 (2010).

260. Mela, F. et al. Dual transcriptional profiling of a bacterial/fungal confrontation: Collimonas fungivorans versus Aspergillus niger. ISME J. 5, 1494–1504 (2011).

261. Ekblad, A., Wallander, H. & Nasholm, T. Chitin and ergosterol combined to measure total and living fungal biomass in ectomycorrhizas. New Phytol. 138, 143–149 (1998).

262. Vlamakis, H., Chai, Y., Beauregard, P., Losick, R. & Kolter, R. Sticking together: building a biofilm the Bacillus subtilis way. Nat. Rev. Microbiol. 11, 157–168 (2013).

263. Ren, D. et al. Gene expression in Bacillus subtilis surface biofilms with and without sporulation and the importance of yveR for biofilm maintenance. Biotechnol. Bioeng. 86, 344–364 (2004). 264. Sieuwerts, S. et al. Mixed-culture transcriptome analysis reveals the molecular basis of

mixed-culture growth in Streptococcus thermophilus and Lactobacillus bulgaricus. Appl. Environ. Microbiol. 76, 7775–7784 (2010).

(17)

521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker Processed on: 25-7-2018 Processed on: 25-7-2018 Processed on: 25-7-2018

Processed on: 25-7-2018 PDF page: 130PDF page: 130PDF page: 130PDF page: 130

130

265. Kearns, D. B. & Losick, R. Cell population heterogeneity during growth of Bacillus subtilis. Genes Dev. 19, 3083–3094 (2005).

266. de Bekker, C., Bruning, O., Jonker, M. J., Breit, T. M. & Wösten, H. A. B. Single cell transcriptomics of neighboring hyphae of Aspergillus niger. Genome Biol. 12, R71 (2011). 267. Kayala, M. A. & Baldi, P. Cyber-T web server: differential analysis of high-throughput data.

Nucleic Acids Res. 40, W553-559 (2012).

268. Gruben, B. S., Zhou, M. & de Vries, R. P. GalX regulates the D-galactose oxido-reductive pathway in Aspergillus niger. FEBS Lett. 586, 3980–3985 (2012).

269. Medema, M. H. et al. antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res. 39, W339-346 (2011).

270. Shelest, E. Transcription factors in fungi. FEMS Microbiol. Lett. 286, 145–151 (2008).

271. van Hijum, S. A. F. T. et al. A generally applicable validation scheme for the assessment of factors involved in reproducibility and quality of DNA-microarray data. BMC Genomics 6, 77 (2005).

272. Mironczuk, A. M., Manu, A., Kuipers, O. P. & Kovács, A. T. Distinct roles of ComK1 and ComK2 in gene regulation in Bacillus cereus. PLoS One 6, e21859 (2011).

273. Pfaffl, M. W., Horgan, G. W. & Dempfle, L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36 (2002).

274. Van Leeuwen, M. R., Smant, W., de Boer, W. & Dijksterhuis, J. Filipin is a reliable in situ marker of ergosterol in the plasma membrane of germinating conidia (spores) of Penicillium discolor and stains intensively at the site of germ tube formation. J. Microbiol. Methods 74, 64–73 (2008).

275. Bayles, K. W. Are the molecular strategies that control apoptosis conserved in bacteria? Trends Microbiol. 11, 306–311 (2003).

276. van den Esker, M. H., Kovács, Á. T. & Kuipers, O. P. From cell death to metabolism: holin-antiholin homologues with new functions. MBio 8, e01963-17 (2017).

277. Andersen, J. L. & Kornbluth, S. The tangled circuitry of metabolism and apoptosis. Mol. Cell 49, 399–410 (2013).

278. Lobritz, M. A. et al. Antibiotic efficacy is linked to bacterial cellular respiration. Proc. Natl. Acad. Sci. 112, 8173–8180 (2015).

279. Briehl, M., Pooley, H.M., Karamata, D. Mutants of Bacillus subtilis 168 thermosensitive for growth and wall teichoic acid synthesis. J. Gen. Microbiol. 135, 1325–1334 (1989).

280. Mauël, C., Young, M., Margot, P. & Karamata, D. The essential nature of teichoic acids in Bacillus subtilis as revealed by insertional mutagenesis. Mol Gen Genet 215, 388–394 (1989). 281. D’Elia, M. A. et al. Lesions in teichoic acid biosynthesis in Staphylococcus aureus lead to a lethal

gain of function in the otherwise dispensable pathway. J. Bacteriol. 188, 4183–4189 (2006). 282. Weidenmaier, C. et al. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major

risk factor in nosocomial infections. Nat. Med. 10, 243–245 (2004).

283. Gualerzi, C. O., Giuliodori, A. M. & Pon, C. L. Transcriptional and post-transcriptional control of cold-shock genes. J. Mol. Biol. 331, 527–539 (2003).

284. Cacace, G. et al. Proteomics for the elucidation of cold adaptation mechanisms in Listeria monocytogenes. J. Proteomics 73, 2021–2030 (2010).

(18)

521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker 521545-L-bw-vdEsker Processed on: 25-7-2018 Processed on: 25-7-2018 Processed on: 25-7-2018

Processed on: 25-7-2018 PDF page: 131PDF page: 131PDF page: 131PDF page: 131

131 285. Yamanaka, K. Cold shock response in Escherichia coli. J. Mol. Microbiol. Biotechnol 1, 193–202 (1999). 286. Wiebe, W. J., Sheldon, W. M. & Pomeroy, L. R. Bacterial growth in the cold: Evidence for an

enhanced substrate requirement. Appl. Environ. Microbiol. 58, 359–364 (1992).

287. Scherer, S. & Neuhaus, K. in The Prokaryotes (eds. Falkow, S., Rosenberg, E., Schleifer, K.-H. & Stackebrandt, E.) 210–262 (Springer New York, 2006). doi:10.1007/0-387-30742-7_8 288. Earl, A. M., Losick, R. & Kolter, R. Ecology and genomics of Bacillus subtilis. Trends Microbiol.

16, 269–275 (2008).

289. Palková, Z. Multicellular microorganisms: laboratory versus nature. EMBO Rep. 5, 470–476 (2004).

290. Grundmann, G. L. Spatial scales of soil bacterial diversity - the size of a clone. FEMS Microbiol. Ecol. 48, 119–127 (2004).

291. Stefanic, P. & Mandic-Mulec, I. Social interactions and distribution of Bacillus subtilis pherotypes at microscale. J. Bacteriol. 191, 1756–1764 (2009).

292. Vignati, D. A. L., Ferrari, B. J. D. & Dominik, J. Laboratory-to-field extrapolation in aquatic sciences. Environ. Sci. Technol. 41, 1067–73 (2007).

293. Requena, N., Jimenez, I., Toro, M. & Barea, J. M. Interactions between plant-growth-promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi and Rhizobium spp. in the rhizosphere of Anthyllis cytisoides, a model legume for revegetation in mediterranean semi-arid ecosystems. New Phytol. 136, 667–677 (1997).

294. Toro, M., Azc N, R. & Barea, J.-M. Improvement of arbuscular mycorrhiza development by inoculation of soil with phosphate-solubilizing Rhizobacteria to improve rock phosphate bioavailability (32P) and nutrient cycling. Appl. Environ. Microbiol. 63, 4408–4412 (1997). 295. Swain, M. R. & Ray, R. C. Biocontrol and other beneficial activities of Bacillus subtilis isolated

from cowdung microflora. Microbiol. Res. 164, 121–130 (2009).

296. Yánez-Mendizábal, V. et al. Biological control of peach brown rot (Monilinia spp.) by Bacillus subtilis CPA-8 is based on production of fengycin-like lipopeptides. Eur. J. Plant Pathol. 132, 609–619 (2012).

297. Shafi, J., Tian, H. & Ji, M. Bacillus species as versatile weapons for plant pathogens: a review. Biotechnol. Biotechnol. Equip. 31, 446–459 (2017).

298. van der Heijden, M. Fundamenteel onderzoek is allesbehalve spielerei. NRC (2016). 299. Sewell, E. W. C. & Brown, E. D. Taking aim at wall teichoic acid synthesis: new biology and

new leads for antibiotics. J. Antibiot. (Tokyo). 67, 43–51 (2014).

300. Sadykov, M. R. & Bayles, K. W. The control of death and lysis in staphylococcal biofilms: a coordination of physiological signals. Curr. Opin. Microbiol. 15, 211–215 (2012).

301. Overmars, L., Kerkhoven, R., Siezen, R. J. & Francke, C. MGcV: the microbial genomic context viewer for comparative genome analysis. BMC Genomics 14, 209 (2013).

302. Celler, K., Koning, R. I., Koster, A. J. & van Wezel, G. P. Multidimensional view of the bacterial cytoskeleton. J. Bacteriol. 195, 1627–36 (2013).

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