Bacillus subtilis spore protein SpoVAC functions as a mechanosensitive channel

Molecular Microbiology

Volumn 92, Issue 4, 2014, Pages 813-823

  Velásquez, Jeanette ^a,b   Schuurman Wolters, Gea ^a   Birkner, Jan Peter ^a   Abee, Tjakko ^b,c   Poolman, Bert ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DODECYLAMINE; LYSOPHOSPHATIDYLCHOLINE; PROTEIN SPOVAC; UNCLASSIFIED DRUG; MEMBRANE PROTEIN;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENE; BACTERIAL SPORE; CHANNEL GATING; CONTROLLED STUDY; ESCHERICHIA COLI; GENE EXPRESSION; ION CONDUCTANCE; LACTOCOCCUS LACTIS; LIPID VESICLE; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SPHEROPLAST; SPOVAC GENE; GENETICS; MECHANICS; METABOLISM; PHYSIOLOGY;

BACILLUS SUBTILIS; ESCHERICHIA COLI;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CLONING, MOLECULAR; ESCHERICHIA COLI; GENE EXPRESSION; ION CHANNEL GATING; MECHANICAL PHENOMENA; MEMBRANE PROTEINS; SPORES, BACTERIAL;

EID: 84899902629     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12591     Document Type: Article

References (50)

1. Abhyankar, W., Hossain, A.H., Djajasaputra, A., Permpoonpattana, P., Ter Beek, A., Dekker, H.L., etal. (2013) In pursuit of protein targets: proteomic characterization of bacterial spore outer layers. J Proteome Res 12: 4507-4521.
2. Black, E.P., Koziol-Dube, K., Guan, D., Wei, J., Setlow, B., Cortezzo, D.E., etal. (2005) Factors influencing germination of Bacillus subtilis spores via activation of nutrient receptors by high pressure. Appl Environ Microbiol 71: 5879-5887.
3. Black, E.P., Wei, J., Atluri, S., Cortezzo, D.E., Koziol-Dube, K., Hoover, D.G., and Setlow, P. (2007) Analysis of factors influencing the rate of germination of spores of Bacillus subtilis by very high pressure. J Appl Microbiol 102: 65-76.
4. Blount, P., Sukharev, S.I., Moe, P.C., Martinac, B., and Kung, C. (1999) Mechanosensitive channels of bacteria. Methods Enzymol 294: 458-482.
5. Booth, I.R., and Blount, P. (2012) The MscS and MscL families of mechanosensitive channels act as microbial emergency release valves. J Bacteriol 194: 4802-4809.
6. Casadaban, M.J., and Cohen, S.N. (1980) Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol 138: 179-207.
7. Cowan, A.E., Olivastro, E.M., Koppel, D.E., Loshon, C.A., Setlow, B., and Setlow, P. (2004) Lipids in the inner membrane of dormant spores of Bacillus species are largely immobile. Proc Natl Acad Sci USA 101: 7733.
8. Daniel, R.A., and Errington, J. (1993) Cloning, DNA sequence, functional analysis and transcriptional regulation of the genes encoding dipicolinic acid synthetase required for sporulation in Bacillus subtilis. J Mol Biol 232: 468-483.
9. Edwards, M.D., Black, S., Rasmussen, T., Rasmussen, A., Stokes, N.R., Stephen, T.-L., etal. (2012) Characterization of three novel mechanosensitive channel activities in Escherichia coli. Channels 6: 272-281.
10. Errington, J. (1993) Bacillus subtilis sporulation: regulation of gene expression and control of morphogenesis. Microbiol Rev 57: 1-33.
11. Fort, P., and Errington, J. (1985) Nucleotide sequence and complementation analysis of a polycistronic sporulation operon, spoVA, in Bacillus subtilis. Microbiology 131: 1091-1105.
12. Geertsma, E.R., and Poolman, B. (2007) High-throughput cloning and expression in recalcitrant bacteria. Nat Methods 4: 705-707.
13. Geertsma, E.R., Nik Mahmood, N.A.B., Schuurman-Wolters, G.K., and Poolman, B. (2008) Membrane reconstitution of ABC transporters and assays of translocator function. Nat Protoc 3: 256-266.
14. Griffiths, K.K., and Setlow, P. (2009) Effects of modification of membrane lipid composition on Bacillus subtilis sporulation and spore properties. J Appl Microbiol 106: 2064-2078.
15. Griffiths, K.K., Zhang, J., Cowan, A.E., Yu, J., and Setlow, P. (2011) Germination proteins in the inner membrane of dormant Bacillus subtilis spores colocalize in a discrete cluster. Mol Microbiol 81: 1061-1077.
16. Guzman, L.M., Belin, D., Carson, M.J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
17. Haswell, E.S., Phillips, R., and Rees, D.C. (2011) Mechanosensitive channels: what can they do and how do they do it? Structure 19: 1356-1369.
18. Henriques, A.O., and Moran, C.P., Jr (2007) Structure, assembly, and function of the spore surface layers. Annu Rev Microbiol 61: 555-588.
19. Hille, B. (2001) Ion Channels of Excitable Membranes. Sunderland, MA: Sinauer Associates.
20. Koçer, A., Walko, M., and Feringa, B.L. (2006) Synthesis and utilization of reversible and irreversible light-activated nanovalves derived from the channel protein MscL. Nat Protoc 2: 1426-1437.
21. Korza, G., and Setlow, P. (2013) Topology and accessibility of germination proteins in the Bacillus subtilis spore inner membrane. J Bacteriol 195: 1484-1491.
22. Kung, C., Martinac, B., and Sukharev, S. (2010) Mechanosensitive channels in microbes. Annu Rev Microbiol 64: 313-329.
23. Levina, N., Totemeyer, S., Stokes, N., Louis, P., Jones, M., and Booth, I. (1999) Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J 18: 1730-1737.
24. Li, Y., Moe, P.C., Chandrasekaran, S., Booth, I.R., and Blount, P. (2002) Ionic regulation of MscK, a mechanosensitive channel from Escherichia coli. EMBO J 21: 5323-5330.
25. Li, Y., Davis, A., Korza, G., Zhang, P., Li, Y.-Q., Setlow, B., etal. (2012) Role of a SpoVA protein in dipicolinic acid uptake into developing spores of Bacillus subtilis. J Bacteriol 194: 1875-1884.
26. Martinac, B.B., Adler, J.J., and Kung, C.C. (1990) Mechanosensitive ion channels of E.coli activated by amphipaths. Nature 348: 261-263.
27. Mika, J.T., Birkner, J.P., Poolman, B., and Kocer, A. (2013) On the role of individual subunits in MscL gating: 'All for one, one for all?'. FASEB J 27: 882-892.
28. Moe, P.C.P., Blount, P.P., and Kung, C.C. (1998) Functional and structural conservation in the mechanosensitive channel MscL implicates elements crucial for mechanosensation. Mol Microbiol 28: 583-592.
29. Moir, A. (2006) How do spores germinate? J Appl Microbiol 101: 526-530.
30. Moir, A., Corfe, B., and Behravan, J. (2002) Spore germination. Cell Mol Life Sci 59: 403-409.
31. Nomura, T.T., Cranfield, C.G.C., Deplazes, E.E., Owen, D.M.D., Macmillan, A.A., Battle, A.R.A., etal. (2012) Differential effects of lipids and lyso-lipids on the mechanosensitivity of the mechanosensitive channels MscL and MscS. Proc Natl Acad Sci USA 109: 8770-8775.
32. Paredes-Sabja, D., Setlow, P., and Sarker, M.R. (2011) Germination of spores of Bacillales and Clostridiales species: mechanisms and proteins involved. Trends Microbiol 19: 85-94.
33. Perozo, E., Kloda, A., Cortes, D.M., and Martinac, B. (2002) Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat Struct Biol 9: 696-703.
34. Poolman, B., Spitzer, J.J., and Wood, J.M. (2004) Bacterial osmosensing: roles of membrane structure and electrostatics in lipid-protein and protein-protein interactions. Biochim Biophys Acta 1666: 88-104.
35. Schumann, U., Edwards, M.D., Rasmussen, T., Bartlett, W., Van West, P., and Booth, I.R. (2010) YbdG in Escherichia coli is a threshold-setting mechanosensitive channel with MscM activity. Proc Natl Acad Sci USA 107: 12664.
36. Setlow, B., Cowan, A.E., and Setlow, P. (2003) Germination of spores of Bacillus subtilis with dodecylamine. J Appl Microbiol 95: 637-648.
37. Setlow, B., Wahome, P.G., and Setlow, P. (2008) Release of small molecules during germination of spores of Bacillus species. J Bacteriol 190: 4759-4763.
38. Setlow, P. (2003) Spore germination. Curr Opin Microbiol 6: 550-556.
39. Setlow, P. (2006) Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J Appl Microbiol 101: 514-525.
40. Setlow, P. (2014) The germination of spores of Bacillus species: what we know and don't know. J Bacteriol. doi:10.1128/JB.01455-13
41. Stewart, K.A.V., and Setlow, P. (2013) Numbers of individual nutrient germinant receptors and other germination proteins in spores of Bacillus subtilis. J Bacteriol 195: 3575-3582.
42. Tovar-Rojo, F., Chander, M., Setlow, B., and Setlow, P. (2002) The products of the spoVA operon are involved in dipicolinic acid uptake into developing spores of Bacillus subtilis. J Bacteriol 184: 584-587.
43. Vepachedu, V.R., and Setlow, P. (2004) Analysis of the germination of spores of Bacillus subtilis with temperature sensitive spo mutations in the spoVA operon. FEMS Microbiol Lett 239: 71-77.
44. Vepachedu, V.R., and Setlow, P. (2005) Localization of SpoVAD to the inner membrane of spores of Bacillus subtilis. J Bacteriol 187: 5677-5682.
45. Vepachedu, V.R., and Setlow, P. (2007) Role of SpoVA proteins in release of dipicolinic acid during germination of Bacillus subtilis spores triggered by dodecylamine or lysozyme. J Bacteriol 189: 1565-1572.
46. Wahome, P.G., and Setlow, P. (2006) The synthesis and role of the mechanosensitive channel of large conductance in growth and differentiation of Bacillus subtilis. Arch Microbiol 186: 377-383.
47. Wahome, P.G., and Setlow, P. (2007) Growth, osmotic downshock resistance and differentiation of Bacillus subtilis strains lacking mechanosensitive channels. Arch Microbiol 189: 49-58.
48. Wahome, P.G., Cowan, A.E., Setlow, B., and Setlow, P. (2009) Levels and localization of mechanosensitive channel proteins in Bacillus subtilis. Arch Microbiol 191: 403-414.
49. Wang, G., Yi, X., Li, Y.-Q., and Setlow, P. (2011) Germination of individual Bacillus subtilis spores with alterations in the GerD and SpoVA proteins, which are important in spore germination. J Bacteriol 193: 2301-2311.
50. Wuytack, E.Y.E., Soons, J.J., Poschet, F.F., and Michiels, C.W.C. (1999) Comparative study of pressure- and nutrient-induced germination of Bacillus subtilis spores. Appl Environ Microbiol 66: 257-261.