Spo0A links de novo fatty acid synthesis to sporulation and biofilm development in Bacillus subtilis

Molecular Microbiology

Volumn 87, Issue 2, 2013, Pages 348-367

  Pedrido, María E ^a   de Oña, Paula ^a   Ramirez, Walter ^a   Leñini, Cecilia ^a   Goñi, Anibal ^a   Grau, Roberto ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; CARBOXYLASE; MALONYL COENZYME A; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SPOOA; UNCLASSIFIED DRUG;

ACCDA GENE; ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL SPORE; BIOFILM; CATALYSIS; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENZYME ACTIVITY; FATTY ACID SYNTHESIS; GENE ACTIVATION; NONHUMAN; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; REGULON; SPOROGENESIS; TRANSCRIPTION INITIATION;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; BIOFILMS; FATTY ACIDS; GENE EXPRESSION REGULATION, BACTERIAL; SPORES, BACTERIAL; TRANSCRIPTION FACTORS;

BACILLUS SUBTILIS;

EID: 84872382833     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12102     Document Type: Article

References (90)

1. Abanes-De Mello, A., Ya-Lin, S., Aung, S., and Pogliano, K. (2002) A cytoskeleton-like role for the bacterial cell wall during engulfment of the Bacillus subtilis forespore. Genes Dev 12: 3253-3264.
2. Abee, T., Kovács, A., Kuipers, O., and der Veen, S. (2011) Biofilm formation and dispersal in Gram positive bacteria. Curr Opin Biotechnol 22: 172-179.
3. Aguilar, C., Vlamakis, H., Losick, R., and Kolter, R. (2007) Thinking about Bacillus subtilis as a multicellular organism. Curr Opin Microbiol 10: 638-643.
4. Arabolaza, A., Nakamura, A., Pedrido, M.E., Martelotto, L., Orsaria, L., and Grau, R. (2003) Characterization of a novel inhibitory feedback of the anti-anti-sigma SpoIIAA on Spo0A activation during development in Bacillus subtilis. Mol Microbiol 47: 1251-1263.
5. Arigori, F.L., Guérout-Fleury, A., Barák, I., and Stragier, P. (1999) The SpoIIE phosphatase, the sporulation septum and the establishment of forespore-specific transcription in Bacillus subtilis: a reassessment. Mol Microbiol 31: 1407-1415.
6. Barák, I., Muchová, K., Wilkinson, A.J., O'Toole, P.J., and Pavlendová, N. (2008) Lipid spirals in Bacillus subtilis and their role in cell division. Mol Microbiol 68: 1315-1327.
7. Baud, S., Guyon, V., Kronenberger, J., Wuillème, S., Miquel, M., Caboche, M., etal. (2003) Multifunctioal acetyl-CoA carboxylase 1 is essential for very long chain fatty acid elongation and embryo development in Arabidopsis. Plant J 33: 75-86.
8. Bogdanov, M., Mileykovskaya, E., and Dowhan, W. (2008) Lipids in the assembly of membrane proteins and the organization of protein supercomplexes: implications for lipid-linked disorders. Subcell Biochem 49: 197-239.
9. Branda, S., González-Pastor, E., Ben-Yehuda, S., Losick, R., and Kolter, R. (2001) Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci USA 98: 11621-11626.
10. Branda, S., Chu, F., Kearns, D., Losick, R., and Kolter, R. (2006) A major protein component of the Bacillus biofilm matrix. Mol Microbiol 59: 1229-1238.
11. Broder, D., and Pogliano, K. (2006) Forespore engulfment mediated by a ratchet-like mechanism. Cell 26: 917-928.
12. Burton, B.M., Marquis, K.A., Sullivan, N.L., Rapoport, T.A., and Rudner, D.Z. (2007) The ATPase SpoIIIE transports DNA across fused septal membranes during sporulation in Bacillus subtilis. Cell 131: 1301-1312.
13. Campo, N., Marquis, K.A., and Rudner, D.Z. (2008) SpoIIQ anchors membrane proteins on both sides of the sporulation septum in Bacillus subtilis. J Biol Chem 283: 4975-4982.
14. Chary, V., Xenopoulos, P., Eldar, A., and Piggot, P. (2010) Loss of compartmentalization of Sigma E activity need not prevent formation of spores by Bacillus subtilis. J Bacteriol 192: 5616-5624.
15. Choard, T. (2008) Beyond the origin. Beneath the surface. Nature 456: 300-303.
16. Conrad, A., Suutari, M.K., Keinänen, M.M., Cadoret, A., Faure, P., Mansuy-Huault, L., and Block, J.C. (2003) Fatty acid lipidic fractions in extracellular polymeric substances of activated sludge flocks. Lipids 38: 1093-1105.
17. Cutting, S., Oke, V., Driks, A., Losick, R., and Kroos, L. (1990) A forespore checkpoint for mother cell gene expression during development in Bacillus subtilis. Cell 62: 239-250.
18. Davey, M., Cajazza, N., and O'Toole, G. (2003) Rhamnolipid surfactant production affects biofilm architectured in Pseudomonas aeruginosa PAO 1. J Bacteriol 185: 1027-1036.
19. Diez, V., Schujman, G., Gueiros-Filho, F., and De Mendoza, D. (2012) Vectorial signalling mechanism required for cell-cell communication during sporulation in Bacillus subtilis. Mol Microbiol 83: 261-274.
20. Dowhan, W., and Bogdanov, M. (2009) Lipid-dependent membrane protein topogenesis. Annu Rev Biochem 78: 515-540.
21. Dowhan, W., and Bogdanov, M. (2011) Lipid-proteins interactions as determinants of membrane protein structure and function. Biochem Soc Trans 39: 767-774.
22. Dworkin, J. (2003) Transient genetic asymmetry and cell fate in a bacterium. Trends Genet 19: 107-112.
23. Dworkin, J., and Losick, R. (2001) Differential gene expression governed by chromosomal spatial asymmetry. Cell 107: 339-346.
24. Emoto, K., and Umeda, M. (2001) Membrane lipid control of cytokinesis. Cell Struct Funct 26: 659-665.
25. Engelman, D.M. (2005) Membranes are more mosaic than fluid. Nature 438: 578-580.
26. Epstein, A., Pokroy, B., Saminara, A., and Aizenberg, J. (2011) Bacterial biofilm shows persistent resistance to liquid wetting and gas penetration. Proc Natl Acad Sci USA 108: 995-1000.
27. Errington, J. (2003) Regulation of endospore formation in Bacillus subtilis. Nat Rev Microbiol 1: 117-126.
28. Fairn, G.D., and Grinstein, S. (2008) A one-sided signal. Science 320: 458-460.
29. Fawcett, P., Melnikov, A., and Youngman, P. (1998) The Bacillus SpoIIGA protein is targeted to sites of spore septum formation in a SpoIIE-independent manner. Mol Microbiol 28: 931-943.
30. Flemming, H., and Wingender, J. (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
31. Frandsen, N., Barák, I., Karmazyn-Campelli, C., and Stragier, P. (1999) Transient gene asymmetry during sporulation and establishment of cell specificity in Bacillus subtilis. Genes Dev 13: 394-399.
32. E in Bacillus subtilis. Mol Microbiol 43: 27-38.
33. Fujita, M., and Losick, R. (2003) The master regulator Spo0A for entry into sporulation in Bacillus subtilis becomes a cell-specific transcription factor after asymmetric division. Genes Dev 17: 1166-1174.
34. Fujita, Y., Matsuoka, H., and Hirooka, K. (2007) Regulation of fatty acid metabolism in bacteria. Mol Microbiol 66: 829-839.
35. Golstein, B., and Macara, I.G. (2007) The PAR proteins: fundamentals players in animal cell polarization. Dev Cell 13: 609-622.
36. Gottig, N., Pedrido, M.E., Mendez, M., Lombardia, E., Rovetto, A., Philippe, V., etal. (2005) The Bacillus subtilis SinR and RapA developmental regulators are responsible for inhibition of spore development by alcohol. J Bacteriol 187: 2662-2672.
37. Grau, R., and De Mendoza, D. (1993) Regulation of the synthesis of unsaturated fatty acids by growth temperature in Bacillus subtilis. Mol Microbiol 8: 535-542.
38. Hamon, M., and Lazazzera, B. (2001) The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol Microbiol 42: 1199-1209.
39. Hamon, M., Stanley, N., Britton, R., Grossman, A., and Lazazzera, B. (2004) Identification of AbrB-regulated genes involved in biofilm formation by Bacillus subtilis. Mol Microbiol 52: 847-860.
40. Hartwell, L., and Weinert, T. (1989) Checkpoints: controls that ensure the order of cell cycle events. Science 246: 629-634.
41. Higgins, D., and Dworkin, J. (2012) Recent progress in Bacillus subtilis sporulation. FEMS Microbiol Rev 36: 131-148.
42. Hilbert, D.W., and Piggot, P.J. (2004) Compartmentalization of gene expression during Bacillus subtilis spore formation. Microbiol Mol Biol Rev 68: 234-262.
43. Imamura, D., Zhou, R., Feig, M., and Kroos, L. (2008) Evidences that the Bacillus subtilis SpoIIGA protein is a novel type of signal-transducing aspartic protease. J Biol Chem 283: 15287-15299.
44. Ireton, K., and Grossman, A. (1992) Coupling between gene expression and DNA synthesis early during development in Bacillus subtilis. Proc Natl Acad Sci USA 89: 8808-8812.
45. Iwamoto, K., Kobayashi, S., Fukuda, R., Umeda, M., Kobayashi, T., and Ohta, A. (2004) Local exposure of phosphatydylethanolamine on the yeast plasma membrane is implicated in cell polarity. Genes Cells 9: 891-903.
46. Jahn, R., Lang, T., and Südhof, T.C. (2003) Membrane fusion. Cell 112: 519-533.
47. F during sporulation in Bacillus subtilis. Proc Natl Acad Sci USA 92: 2012-2016.
48. Kearns, D., and Losick, R. (2005) Cell population heterogeneity during growth of Bacillus subtilis. Genes Dev 19: 3083-3094.
49. F during sporulation in Bacillus subtilis. Genes Dev 13: 1156-1167.
50. W-dependent stress response in Bacillus subtilis that reduces membrane fluidity. Mol Microbiol 81: 69-79.
51. Kobayashi, K., and Iwano, M. (2012) BslA (YuaB) forms a hydrophobic layer on the surface of Bacillus subtilis biofilms. Mol Microbiol 85: 51-56.
52. Kovács, Á., van Gestel, J., and Kuipers, O. (2012) The protective layer of a biofilm: a repellent function for a new class of amphiphilic proteins. Mol Microbiol 85: 8-11.
53. Lazarevic, V., Soldo, B., Médico, N., Pooley, H., Bron, S., and Karamata, D. (2005) Bacillus subtilis alpha-phosphoglucomutase is required for normal cell morphology and biofilm formation. Appl Environ Microbiol 71: 39-45.
54. Lazazzera, B. (2005) Lessons from DNA microarray analysis: the gene expression profile of biofilms. Curr Opin Microbiol 8: 222-227.
55. Lee, A. (2005) A greasy grip. Nature 438: 569-570.
56. Liu, J., Tan, K., and Stormo, G.D. (2003) Computational identification of the Spo0A-phosphate regulon that is essential for the cellular differentiation and development in Gram-positive spore-forming bacteria. Nucleic Acids Res 23: 6891-6903.
57. Lombardía, E., Rovetto, A., Arabolaza, A., and Grau, R. (2006) A LuxS-dependent cell to cell language regulates social behavior and development in Bacillus subtilis. J Bacteriol 188: 4442-4452.
58. Londoño-Vallejo, J., and Stragier, P. (1995) Cell-cell signaling pathway activating a developmental transcription factor in Bacillus subtilis. Genes Dev 9: 503-508.
59. López, D., and Kolter, R. (2010) Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis. FEMS Microbiol Rev 34: 134-149.
60. Losick, R., and Dworkin, J. (1999) Linking asymmetric division to cell fate: teaching an old microbe new tricks. Genes Dev 13: 377-381.
61. Losick, R., and Stragier, P. (1992) Crisscross regulation of cell-type-specific gene expression during development in Bacillus subtilis. Nature 355: 601-604.
62. Marini, P., Pérez, C., and De Mendoza, D. (2001) Growth-rate regulation of the Bacillus subtilis accBC operon encoding subunits of the acetyl-CoA carboxylase, the first enzyme of fatty acid synthesis. Arch Microbiol 175: 234-237.
63. Martínez, M., de Mendoza, D., and Schujman, G. (2010) Transcriptional and functional characterization of the gene encoding acyl carrier protein in Bacillus subtilis. Microbiology 156: 484-495.
64. Matsumoto, K., Kusaka, J., Nishibori, A., and Hara, H. (2006) Lipid domains in bacterial membranes. Mol Microbiol 61: 1110-1117.
65. Meyer, P., Gutierrez, J., Pogliano, K., and Dworkin, J. (2010) Cell wall synthesis is necessary for membrane dynamics during sporulation of Bacillus subtilis. Mol Microbiol 76: 956-970.
66. Mileykovskaya, E., and Dowhan, W. (2005) Role of membrane lipids in bacterial division-site selection. Curr Opin Microbiol 8: 135-142.
67. Mindich, L. (1970) Membrane synthesis in Bacillus subtilis. I. Isolation and properties of strains bearing mutations in glycerol metabolism. J Mol Biol 49: 415-432.
68. Molle, V., Fujita, M., Jensen, S.T., Eichenberger, P., González-Pastor, J.E., Liu, J.S., and Losick, R. (2003) The Spo0A regulon of Bacillus subtilis. Mol Microbiol 50: 1683-1701.
69. Morlot, C., Uehara, T., Marquis, K., Bernhardt, T., and Rudner, D. (2010) A highly coordinated cell wall degradation machine governs spore morphogenesis in Bacillus subtilis. Genes Dev 24: 411-422.
70. Neu, T., and Poralla, K. (1988) An amphiphilic polysaccharide from an adhesive Rhodococcus strain. FEMS Microbiol Lett 49: 389-392.
71. Neu, T.R., Dengler, T., Jann, B., and Poralla, K. (1992) Structural studies of an emulsion-stabilizing exopolysaccharide produced by an adhesive, hydrophobic Rhodococcus strain. J Gen Microbiol 138: 2531-2537.
72. Nishibori, A., Kusaka, J., Hara, H., Umeda, M., and Matsumoto, K. (2005) Phosphatydylethanolamine domains and localization of phospholipids synthases in Bacillus subtilis membranes. J Bacteriol 187: 2163-2174.
73. Ramamurthi, K., and Losick, R. (2005) Protein localization: reach out and touch the forespore. Curr Biol 15: 165-167.
74. Ramamurthi, K., and Losick, R. (2009) Negative membrane curvature as a cue for subcellular localization of a bacterial protein. Proc Natl Acad Sci USA 106: 13541-13545.
75. Rappleye, C.A., Tagawa, A., Le Bot, N., Ahringer, J., and Aroian, R.V. (2003) Involvement of fatty acid pathways and cortical interaction of the pronuclear complex in C. elegans embryonic polarity. BMC Dev Biol 3: 1-15.
76. Reder, A., Höper, D., Weinberg, C., Gerth, U., Fraunholzs, M., and Hecker, M. (2008) The Spx paralogue MgsR (YqgZ) controls a subregulon within the general stress response of Bacillus subtilis. Mol Microbiol 69: 1104-1120.
77. Romero, D., Aguilar, C., Losick, R., and Kolter, R. (2010) Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci USA 107: 2230-2234.
78. Rudner, D., Pan, Q., and Losick, R. (2002) Evidence that subcellular localization of a bacterial membrane protein is achieved by diffusion and capture. Proc Natl Acad Sci USA 99: 8701-8706.
79. Schneiter, R., and Kohlwein, S.D. (1997) Organelle structure, function, and inheritance in yeast: a role for fatty acid synthesis? Cell 88: 431-434.
80. Schujman, G.E., Grau, R., Gramajo, H., Ornella, L., and De Mendoza, D. (1998) De novo fatty acid synthesis is required for establishment of cell type specific gene transcription during sporulation in Bacillus subtilis. Mol Microbiol 29: 1215-1224.
81. Shank, E., and Kolter, R. (2011) Extracellular signaling and multicellularity in Bacillus subtilis. Curr Opin Microbiol 14: 741-747.
82. Singer, L., and Nicolson, G.L. (1972) The fluid mosaic model of the structure of cell membranes. Science 175: 720-732.
83. Stragier, P., and Losick, R. (1996) Molecular genetics of sporulation in Bacillus subtilis. Annu Rev Genet 30: 297-341.
84. Stragier, P., Bonamy, C., and Karmazyn-Campelli, C. (1998) Processing of a sporulation sigma factor in Bacillus subtilis: how morphological structure could control gene expression. Cell 52: 697-704.
85. Theilacker, C., Sanchez-Carballo, P., Toma, I., Fabretti, F., Sava, I., Kropec, A., etal. (2009) Glycolipids are involved in biofilm accumulation and prolongued bacteraemia in Enterococcus faecalis. Mol Microbiol 71: 1055-1069.
86. Vagner, V., Dervyn, E., and Ehrlich, S.D. (1998) A vector for systematic gene inactivation in Bacillus subtilis. Microbiology 144: 3097-3104.
87. Vanounou, S., Parola, A.H., and Fishov, I. (2003) Phosphatydylethanolamine and phosphatydylglycerol are segregated into different domains in bacterial membrane. A study with pyren-labelled phospholipids. Mol Microbiol 49: 1067-1079.
88. VidyaLaxme, B., Rovetto, A., Grau, R., and Agrawal, R. (2012) Synergistic effects of probiotic Leuconostoc mesenteroides and Bacillus subtilis in malted ragi food for antagonistic activity against V.cholerae and other beneficial properties. J Food Sci Technol doi: 10.1007/s13197-012-0834-5
89. Wach, A. (1996) PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S.cerevisiae. Yeast 12: 259-265.
90. Zhang, Y.-M., and Rock, C. (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6: 222-233.