Spore Structural Proteins

Peter Setlow

doi:10.1128/9781555818388.ch55

Chapter 55 : Spore Structural Proteins

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Department of Biochemistry, University of Connecticut Health Center, Farmington, Connecticut 06030-3305

Content Type: Monograph

Publication Year: 1993

Category: Bacterial Pathogenesis; Microbial Genetics and Molecular Biology

Book DOI: 10.1128/9781555818388

Chapter DOI: 10.1128/9781555818388.ch55

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Spore Structural Proteins, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555818388/9781555810535_Chap55-1.gif /docserver/preview/fulltext/10.1128/9781555818388/9781555810535_Chap55-2.gif

Abstract:

Each spore coat and nucleoid structure contains a large amount of protein, with spore coats comprising ~50% and spore nucleoid proteins greater than are equal to 5% of total Bacillus subtilis spore protein; spores of other Bacillus species have comparable amounts of protein in these two structures. Thus, both spore coat and spore nucleoid components are major spore structural proteins; both types of proteins consist of multiple species coded for by monocistronic genes scattered around the B. subtilis chromosome. Understanding the structure and function of their individual protein components can give insight into spore coat and nucleoid structures. The majority of the B. subtilis spore coat appears to be composed of protein (~50% of total spore protein), although small amounts of lipid should be present in spore coat preparations, since the outer forespore membrane is often extracted with spore coat proteins. The proteins associated with the spore coat and nucleoid are unique both to the spore stage of the B. subtilis life cycle and also to this group of organisms. A number of the spore coat proteins have highly unusual amino acid compositions that may be important in their specific functions in the complex spore coat. α/ β-Type small acid-soluble spore proteins (SASP), on the other hand, do not have unusual amino acid compositions but have properties in vitro that clearly indicate how these proteins function in determining forespore nucleoid structure and properties in vivo.

Citation: Setlow P. 1993. Spore Structural Proteins, p 801-809. In Sonenshein A, Hoch J, Losick R (ed), Bacillus subtilis and Other Gram-Positive Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555818388.ch55

Highlighted Text: Show | Hide

Full text loading...

Figures

Spore Structural Proteins

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818388.chap55-1,webId=/content/author/10.1128/9781555818388.chap55-1,properties={foaf_givenname=Peter, foaf_name=Peter Setlow, foaf_surname=Setlow, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818388.chap55-aff1]]}]]

/content/10.1128/9781555818388.chap55.fig55-1

Figure 1

Electron micrograph of a dormant spore of B. subtilis PY79. Sporulation was caused by nutrient exhaustion, and spores were taken at t20 for fixation. Methods for fixation and staining were as described in reference 9 . The outer spore coat (oc), inner spore coat (ic), and spore cortex (cx) layers are noted. Bar for entire spore, 100 nm; bar for enlargement of the coat region, 50 nm.

10.1128/9781555818388/fig55-1_thmb.gif

10.1128/9781555818388/fig55-1.gif

Figure 1

/content/10.1128/9781555818388.chap55.fig55-2

Figure 2

Primary sequence of B. subtilis α/β-type SASP. Known amino acid sequences of α/β-type SASP from B. subtilis and the protein specified by the sspF gene (previously 0.3 kb) are shown in one-letter code and are taken from references 49 and 51 . The N-terminal methionine in the coding gene is included but is undoubtedly removed posttranslationally. The sspA gene codes for SASP-α, sspB codes for SASP-β, sspC codes for SspC, and sspD codes for SspD ( 49 ). For the proteins specified by the sspABCD genes, residues conserved in all known α/β-type SASP from the Bacillus line of sporeformers are in boldface type; residues that are similar in these SASP are underlined. A gap has been introduced in these sequences to maximize the alignment with SspF. The large downward-pointing arrow indicates the site of cleavage by the SASP-specific protease ( 49 ). The two upward-pointing arrowheads indicate residues whose alteration in SspC (Gly→Ala or Lys→GIn) reduces or abolishes the ability of this protein to bind DNA in vivo or in vitro ( 57 ). For the protein specified by the sspF gene, residues identical to those conserved in other α/β-type SASP are in boldface; residues similar to those in other α/β-type SASP are underlined.

10.1128/9781555818388/fig55-2_thmb.gif

10.1128/9781555818388/fig55-2.gif

Figure 2

References

/content/book/10.1128/9781555818388.chap55

1. Aronson, A. I.,, and P. C. Fitz-James. 1976. Structure and morphogenesis of the bacterial spore coat. Bacteriol. Rev. 40: 360– 402.

2. Aronson, A. I.,, H.-Y. Song,, and N. Bourne. 1989. Gene structure and precursor processing of a novel Bacillus subtilis spore coat protein. Mol. Microbiol. 3: 437– 444.

3. Bailie, E.,, G. R. Germaine,, W. G. Murrell,, and D. F. Ohye. 1974. Photoreactivation, photoproduct formation, and deoxyribonucleic acid state in ultraviolet-irradiated sporulating cultures of Bacillus cereus. J. Bacteriol. 120: 516– 523.

4. Bourne, N.,, P. C. FitzJames,, and A. I. Aronson. 1991. Structural and germination defects of Bacillus subtilis spores with altered contents of a spore coat protein. J. Bacteriol. 173: 6618– 6625.

5. Bourne, N.,, T.-S. Huang,, and A. I. Aronson,. 1990. Properties of Bacillus subtilis spores with alterations in spore coat structure, p. 329– 338. In M. M. Zukowski,, A. T. Ganesan,, and J. A. Hoch (ed.), Genetics and Biotechnology of Bacilli, vol. 3. Academic Press, Inc., New York.

6. Cabrera-Martinez, R.,, J. M. Mason,, B. Setlow,, W. M. Waites,, and P. Setlow. 1989. Purification and amino acid sequence of two small, acid-soluble proteins from Clostridium bifermentans spores. FEMS Microbiol. Lett. 61: 139– 144.

7. Cabrera-Martinez, R. M.,, and P. Setlow. 1991. Cloning and nucleotide sequence of three genes coding for small, acid-soluble proteins of Clostridium perfringens spores. FEMS Microbiol. Lett. 77: 127– 132.

8. Carillo, Y.,, and P. Setlow. Unpublished results.

9. Cutting, S.. Personal communication.

10. Cutting, S.,, A. Driks,, R. Schmidt,, B. Kunkel,, and R. Losick. 1991. Forespore-specific transcription of a gene in the signal transduction pathway that governs Pro-�� k processing in Bacillus subtilis. Genes Dev. 5: 456– 466.

11. Cutting, S.,, S. Panzer,, and R. Losick. 1989. Regulatory studies on the promoter for a gene governing synthesis and assembly of the spore coat in Bacillus subtilis. J. Mol. Biol. 207: 393– 404.

12. Cutting, S.,, L. Zheng,, and R. Losick. 1991. Gene encoding two alkali-soluble components of the spore coat from Bacillus subtilis. J. Bacteriol. 173: 2915– 2919.

13. Deits, T.. Personal communication.

14. Donovan, W.,, L. Zheng,, K. Sandman,, and R. Losick. 1987. Genes encoding spore coat polypeptides from Bacillus subtilis. J. Mol. Biol. 196: 1– 10.

15. Fairhead, H.,, and P. Setlow. 1992. Binding of DNA to a/B-type small, acid-soluble proteins from spores of Bacillus or Clostridium species prevents formation of cy-tosine dimers, cytosine-thymine dimers, and bipyrimi-dine photoadducts after UV irradiation. J. Bacteriol. 174: 2874– 2880.

16. Feng, P.,, and A. I. Aronson. 1986. Characterization of a Bacillus subtilis germination mutant with pleiotropic alterations in spore coat structure. Curr. Microbiol. 13: 221– 226.

17. Francesconi, S. C.,, T. J. MacAlister,, B. Setlow,, and P. Setlow. 1988. Immunoelectron microscopic localization of small, acid-soluble spore proteins in sporulating cells of Bacillus subtilis. J. Bacteriol. 170: 5963– 5967.

18. Gerhardt, P.,, and R. E. Marquis,. 1989. Spore thermoresistance mechanisms, p. 43– 63. In I. Smith,, R. A. Slepecky,, and P. Setlow (ed.), Regulation of Prokaryotic Development. American Society for Microbiology, Washington, D.C.

19. Goldman, R. C.,, and D. J. Tipper. 1978. Bacillus subtilis spore coats: complexity and purification of a unique polypeptide component. J. Bacteriol. 135: 1091– 1106.

20. Goldman, R. C.,, and D. J. Tipper. 1981. Coat protein synthesis during sporulation of Bacillus subtilis: immunological detection of soluble precursors to the 12,200-dalton spore coat protein. J. Bacteriol. 147: 1040– 1048.

21. Gould, G. W., 1983. Mechanisms of resistance and dormancy, p. 173– 209. In A. Hurst, and G. W. Gould (ed.), The Bacterial Spore, vol. 2. Academic Press, Inc., London.

22. James, W.,, and J. Mandelstam. 1985. spoVIC, a new sporulation locus in Bacillus subtilis affecting spore coats, germination and the rate of sporulation. J. Gen. Microbiol. 131: 2409– 2419.

23. Jenkinson, H. F. 1981. Germination and resistance defects in spores of a Bacillus subtilis mutant lacking a coat polypeptide. J. Gen. Microbiol. 127: 81– 91.

24. Jenkinson, H. F. 1983. Altered arrangement of proteins in the spore coat of a germination mutant of Bacillus subtilis. J. Gen. Microbiol. 129: 1945– 1958.

25. Jenkinson, H. F.,, and H. Lord. 1983. Protease deficiency and its association with defects in spore coat structure, germination and resistance properties in a mutant of Bacillus subtilis. J. Gen. Microbiol. 129: 2727– 2737.

26. Jenkinson, H. F.,, W. D. Sawyer,, and J. Mandelstam. 1981. Synthesis and order of assembly of spore coat proteins in Bacillus subtilis. J. Gen. Microbiol. 123: 1– 16.

27. Johnson, W. C.,, and D. J. Tipper. 1981. Acid-soluble spore proteins of Bacillus subtilis. J. Bacteriol. 146: 972– 982.

28. Kadota, H.,, K. Iijima,, and A. Uchida. 1965. The presence of keratin-like substance in spore coat of Bacillus subtilis. Agric. Biol. Chem. 29: 870– 875.

29. Maglll, N. G.,, C. A. Loshon,, and P. Setlow. 1990. Small, acid-soluble, spore proteins and their genes from two species of Sporosarcina. FEMS Microbiol. Lett. 72: 293– 298.

30. Margolis, P. Personal communication.

31. Mohr, S.,, B. Setlow,, and P. Setlow. Unpublished results.

32. Mohr, S. C.,, N. V. H. A. Sokolov,, C. He,, and P. Setlow. 1991. Binding of small acid-soluble spore proteins from Bacillus subtilis changes the conformation of DNA from B to A. Proc. Natl. Acad. Sci. USA 88: 77– 81.

33. Moir, A. 1981. Germination properties of a spore coat-defective mutant of Bacillus subtilis. J. Bacteriol. 146: 1106– 1116.

34. Nicholson, W. L.,, B. Setlow,, and P. Setlow. 1990. Binding of DNA in vitro by a small, acid-soluble spore protein and its effect on DNA topology. J. Bacterid. 172: 6900– 6906.

35. Nicholson, W. L.,, B. Setlow,, and P. Setlow. 1991. Ultraviolet irradiation of DNA complexed with α/β-type small, acid-soluble proteins from spores of Bacillus or Clostridium species makes spore photoproduct but not thymine dimers. Proc. Natl. Acad. Sci. USA 88: 8288– 8292.

36. Nicholson, W. L.,, and P. Setlow. 1990. Dramatic increase in the negative superhelicity of plasmid DNA in the forespore compartment of sporulating cells of Bacillus subtilis. J. Bacterid. 172: 7– 14.

37. Nicholson, W. L.,, D. Sun,, B. Setlow,, and P. Setlow. 1989. Promoter specificity of sigma-G-containing RNA polymerase from sporulating cells of Bacillus subtilis: identification of a group of forespore-specific promoters. J. Bacterid. 171: 2708– 2718.

38. Ollington, J. F.,, and R. Loslck. 1981. A cloned gene that is turned on at an intermediate stage of spore formation in Bacillus subtilis. J. Bacteriol. 147: 443– 451.

39. Pandey, N. K.,, and A. I. Aronson. 1979. Properties of the Bacillus subtilis spore coat. J. Bacteriol. 137: 1208– 1218.

40. Panzer, S.,, R. Losick,, D. Sun,, and P. Setlow. 1989. Evidence for an additional temporal class of gene expression in the forespore compartment of sporulating Bacillus subtilis. J. Bacteriol. 171: 561– 564.

41. Roels, S.,, A. Driks,, and R. Losick. 1992. Characterization of spoTVA, a sporulation gene involved in coat morphogenesis in Bacillus subtilis. J. Bacteriol. 174: 575– 585.

42. Sandman, K.,, L. Kroos,, S. Cutting,, P. Youngman,, and R. Losick. 1988. Identification of the promoter for a spore coat protein gene in Bacillus subtilis and studies on the regulation of its induction at a late stage of sporulation. J. Mol. Biol. 200: 461– 473.

43. Setlow, B.,, A. R. Hand,, and P. Setlow. 1991. Synthesis of a Bacillus subtilis small, acid-soluble spore protein in Escherichia coli causes cell DNA to assume some characteristics of spore DNA. J. Bacteriol. 173: 1642– 1653.

44. Setlow, B.,, N. Magill,, P. Febbroriello,, L. Nakhimovsky,, D. E. Koppel,, and P. Setlow. 1991. Condensation of the forespore nucleoid early in sporulation of Bacillus species. J. Bacteriol. 173: 6270– 6278.

45. Setlow, B.,, and P. Setlow. Unpublished results.

46. Setlow, B.,, D. Sun,., and P. Setlow. 1992. Interaction between DNA and α/β-type small, acid-soluble spore proteins: a new class of DNA-binding protein. J. Bacteriol. 174: 2312– 2322.

47. Setlow, P. 1978. Purification and characterization of additional low-molecular-weight basic proteins degraded during germination of Bacillus megaterium spores. J. Bacteriol. 136: 331– 340.

48. Setlow, P. 1988. Resistance of bacterial spores to ultraviolet light. Comments Mol. Cell. Biophys. 5: 253– 264.

49. Setlow, P. 1988. Small acid-soluble, spore proteins of Bacillus species: structure, synthesis, genetics, function and degradation. Annu. Rev. Microbiol. 42: 319– 338.

50. Setlow, P. 1992. DNA in dormant spores of Bacillus species is in an A-like conformation. Mol. Microbiol. 6: 563– 567.

51. Stephens, M. A.,, N. Lang,, K. Sandman,, and R. Losick. 1984. A promoter whose utilization is temporally regulated during sporulation in Bacillus subtilis. J. Mol. Biol. 176: 333– 348.

52. Stevens, C. M.,, R. Daniel,, N. Ming,, and J. Errington. 1992. Characterization of a sporulation gene, spoIVA, involved in spore coat morphogenesis in Bacillus subtilis. J. Bacteriol. 174: 586– 594.

53. Stragier, P., 1989. Temporal and spatial control of gene expression during sporulation: from facts to speculation, p. 243– 254. In I. Smith,, R. A. Slepecky,, and P. Setlow (ed.), Regulation of Procaryotic Development. American Society for Microbiology, Washington, D.C.

54. Sun, D.,, P. Stragier,, and P. Setlow. 1989. Identification of a new ��-factor involved in compartmentalized gene expression during sporulation of Bacillus subtilis. Genes Dev. 3: 141– 149.

55. Sussman, M. D.,, and P. Setlow. 1991. Cloning, nucleotide sequence, and regulation of the Bacillus subtilis gpr gene which codes for the protease that initiates degradation of small, acid-soluble, proteins during spore germination. J. Bacteriol. 173: 293– 300.

56. Tipper, D. J.,, and J. J. Gauthier,. 1972. Structure of the bacterial endospore, p. 3– 12. In H. O. Halvorson,, R. Hanson,, and L. L. Campbell (ed.), Spores V. American Society for Microbiology, Washington, D.C.

57. Tovar-Rojo, F.,, and P. Setlow. 1991. Analysis of the effects of mutant small, acid-soluble spore proteins from Bacillus subtilis on DNA in vivo and in vitro. J. Bacteriol. 173: 4827– 4835.

58. Zheng, L.,, W. P. Donovan,, P. C. Fitz-James,, and R. Losick. 1988. Gene encoding a morphogenic protein required in the assembly of the outer coat of the Bacillus subtilis endospore. Genes Dev. 2: 1047– 1054.

59. Zheng, L.,, and R. Losick. 1990. Cascade regulation of spore coat gene expression in Bacillus subtilis. J. Mol. Biol. 212: 645– 660.

Tables

Spore Structural Proteins

/content/10.1128/9781555818388.chap55.tab55-1

Table 1

Properties of spore coat proteins a

10.1128/9781555818388/tab55-1_thmb.gif

10.1128/9781555818388/tab55-1.gif

Table 1

Properties of spore coat proteins a

/content/10.1128/9781555818388.chap55.tab55-2

Table 2

Properties of B. subtilis SASPa

10.1128/9781555818388/tab55-2_thmb.gif

10.1128/9781555818388/tab55-2.gif

Table 2

Properties of B. subtilis SASPa