Chapter 35 : Respiration and Small-Colony Variants of Staphylococcus aureus

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respiration and carbohydrate metabolism follow patterns very similar to those in , with glycolysis in staphylococci following the nearly universal patterns found in all biological systems. Reactions that are favored in respiratory-deficient small-colony variants (SCVs) are shown in a table, and it is apparent that these variants are optimizing reactions that produce ATP and oxidize NADH by non-oxygen-dependent mechanisms. Although mutations in any essential gene can cause slow growth and small colonies, this chapter considers a subset of these mutants that was first observed in patients who had unusually persistent infections and were later found to have defects in oxidative metabolism and electron transport. This chapter focuses on multiple phenotypic changes associated with interrupted electron transport. It was also found that bacterial electron transport inhibitors Z69 and Z90 are able to reproduce the SCV phenotype. JB-1 is a menadione auxotrophic SCV that was selected with gentamicin from its parent, 6850. Some hemin auxotrophs selected by resistance to gentamicin have also been characterized in detail. Although many different mutations might produce slow growth, menadione and hemin auxotrophs predominate among clinical SCV isolates. Finally, the chapter talks about instability of the SCV phenotype, SCVs and antibiotic resistance, and electron transport, respiration, and toxin production in .

Citation: Proctor R. 2006. Respiration and Small-Colony Variants of Staphylococcus aureus, p 434-442. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch35

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Electron Transport System
Cell Wall Biosynthesis
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Fatty Acid Biosynthesis
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Relationship between electron transport and the small-colony variant phenotype in .

Citation: Proctor R. 2006. Respiration and Small-Colony Variants of Staphylococcus aureus, p 434-442. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch35
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1. Abele-Horn, M.,, B. Schupfner,, P. Emmerling,, H. Waldner,, and H. Goring. 2000. Persistent wound infection after herniotomy associated with small-colony variants of Staphylococcus aureus. Infection 28:5354.
2. Baddour, L. M.,, and G. D. Christensen. 1987. Prosthetic valve endocarditis due to small-colony staphylococcal variants. Rev. Infect. Dis. 9:11681174.
3. Baldwin, J. E.,, and H. Krebs. 1981. The evolution of metabolic cycles. Nature 291:381382.
4. Balwit, J. M.,, P. van Langevelde,, J. M. Vann,, and R. A. Proctor. 1994. Gentamicin-resistant, menadione and hemin auxotrophic Staphylococcus aureus persist within cultured endothelial cells. J. Infect. Dis. 170:10331037.
5. Barbour, R. G. H. 1950. Small colony variants (“G” forms) produced by Staphylococcus pyogenes during the development of resistance to streptomycin. Aust. J. Exp. Biol. Med. Sci. 28:411421.
6. Bates, D.,, C. von Eiff,, G. Peters,, A. Bayer,, and R. A. Proctor. 2003. A menD, but not hemB, mutant persists within the kidney in the rabbit endocarditis model. J. Infect. Dis. 187:16541661.
7. Baumert, N.,, C. von Eiff,, F. Schaaff,, G. Peters,, R. A. Proctor,, and H. G. Sahl. 2002. Physiology and antibiotic susceptibility of Staphylococcus aureus small colony variants. Microb. Drug Resist. 8:253260.
8. Bentley, R.,, and R. Meganathan. 1982. Biosynthesis of vitamin K (menaquinone) in bacteria. Microbiol. Rev. 46:241280.
9. Bishop, D. H. L.,, K. D. Pandya,, and H. K. King. 1962. Ubiquinone and vitamin K in bacteria. Biochem. J. 83:606614.
10. Brown, M. R.,, P. J. Collier,, and P. Gilbert. 1990. Influence of growth rate on susceptibility to antimicrobial agents: modification of the cell envelope and batch and continuous culture studies. Antimicrob. Agents Chemother. 34:16231628.
11. Chinn, B. D. 1936. Characteristics of small colony variants with special reference to Shigella paradysenteriae sonne. J. Infect. Dis. 59:137157.
12. Chuard, C.,, P. E. Vaudaux,, R. A. Proctor,, and D. P. Lew. 1997. Decreased susceptibility to antibiotic killing of small colony variants of Staphylococcus aureus in fluid phase and on fibronectin-coated surfaces. J. Antimicrob. Chemother. 39:603608.
13. Clements, M. O.,, S. P. Watson,, R. K. Poole,, and S. J. Foster. 1999. CtaA of Staphylococcus aureus is required for starvation survival, recovery, and cytochrome biosynthesis. J. Bacteriol. 181:501507.
14. Clerch, B.,, E. Rivera,, and M. Llagostera. 1996. Identification of a pKM101 region which confers a slow growth rate and interferes with susceptibility to quinonolone in Escherichia coli AB1157. J. Bacteriol. 178:55685572.
15. Collins, M. D.,, and D. Jones. 1981. Distribution of isoprenoid quinone structure types in bacteria and their taxonomic implications. Microbiol. Rev. 45:316354.
16. Darouiche, R. O.,, and R. J. Hamill. 1994. Antibiotic penetration of and bactericidal activity within endothelial cells. Antimicrob. Agents Chemother. 38:10591064.
17. de la Fuente, R.,, K. H. Schleifer,, F. Götz,, and H.-P. Köst. 1986. Accumulation of porphyrins and pyrrole pigments by Staphylococcus aureus ssp. anaerobius and its aerobic mutant. FEMS Microbiol. Lett. 45:183188.
18. Eisenberg, E. S.,, L. J. Mandel,, H. R. Kaback,, and M. H. Miller. 1984. Quantitative association between electrical potential across the cytoplasmic membrane and early gentamicin uptake and killing in Staphylococcus aureus. J. Bacteriol. 157:863867.
19. Eisenberg, P. 1910. Untersuchungen über die variablen Typhusstamm (Bacterium typhi mutabile), sowie über eine eigentumliche hemmende Wirkung des gewöhnlichen Agar, verursacht durch Autoklavierung, abstr. 56. Zentbl. Bakteriol. Abt., 1:208.
20. Eng, R. H. K.,, F. T. Padberg,, S. M. Smith,, E. N. Tan,, and C. E. Cherubin. 1991. Bactericidal effects of antibiotics on slowly and nongrowing bacteria. Antimicrob. Agents Chemother. 35:18241828.
21. Evans, D. J.,, D. G. Allison,, M. R. W. Brown,, and P. Gilbert. 1991. Susceptibility of Pseudomonas aeruginosa and Escherichia coli biofilms toward ciprofloxacin: effect of specific growth rate. J. Antimicrob. Chemother. 27:177184.
22. Fillingame, R. H. 1997. Coupling H+ transport and ATP synthesis in F0F1 ATP synthases: glimpses of interacting parts in a dynamic molecular machine. J. Exp. Biol. 200:217224.
23. Fillingame, R. H.,, P. C. Jones,, W. Jiang,, F. I. Valiyaveetil,, and O. Y. Dmitriev. 1998. Subunit organization and structure in the F0 sector of Escherichia coli F0F1 ATP synthase. Biochim. Biophys. Acta 1365:135142.
24. Frerman, F. E.,, and D. C. White. 1967. Membrane lipid changes during formation of a functional electron transport system in Staphylococcus aureus. J. Bacteriol.94:18681874.
25. Gilman, S.,, and V. Saunders. 1986. Accumulation of gentamicin by Staphylococcus aureus: the role of transmembrane electrical potential. J. Antimicrob. Chemother. 17:3744.
26. Goldenbaum, P. E.,, and D. C. White. 1974. Role of lipid in the formation and function of the respiratory system of Staphylococcus aureus. Ann. N.Y. Acad. Sci. 236:115123.
27. Hale, J. H. 1947. Studies on staphylococcal mutation: characteristics of the “G” (gonidial) variant and factors concerned in its production. Br. J. Exp. Pathol. 28:202210.
28. Huang, C. T.,, F. P. Yu,, G. A. McFeters,, and P. S. Stewart. 1995. Nonuniform spatial patterns of respiratory activity within biofilms during disinfection. Appl. Environ. Microbiol. 61:22522256.
29. Jensen, P. R.,, and O. Michelsen. 1992. Carbon and energy metabolism of atp mutants of Escherichia coli. J. Bacteriol. 174:76357641.
30. Jonsson, I.-M.,, C. von Eiff,, R. A. Proctor,, G. Peters,, C. Ryden,, and A. Tarkowski. 2003. Virulence of a hemB mutant Staphylococcus aureus small colony variant in a murine model of septic arthritis. Microbial Pathog. 34:7379.
31. Joyce, G. H.,, and D. C. White. 1971. Effect of benso(a) pyrene and piperonyl butoxide on formation of respiratory system, phospholipids, and carotenoids of Staphylococcus aureus. J. Bacteriol. 106:403411.
32. Kafala, B.,, and A. Sasarman. 1994. Cloning and sequence analysis of the hemB gene of Staphylococcus aureus. Can. J. Microbiol. 40:651657.
33. Kahl, B,, A. Duebbers,, G. Lubritz,, J. Haeberle,, H. G. Koch,, B. Ritzerfeld,, M. Reilly,, E. Harms,, R. A. Proctor,, M. Herrmann,, and G. Peters. 2003. Population dynamics and persistence of Staphylococcus aureus infection in cystic fibrosis patients. J. Clin. Microbiol. 41:44244427.
34. Kahl, B.,, R. A. Proctor,, A. Schulze-Everding,, M. Herrmann,, H. G. Koch,, I. Harms,, and G. Peters. 1998. Persistent infection with small colony variant strains of Staphylococcus aureus in patients with cystic fibrosis. J. Infect. Dis. 177:10231029.
35. Kahl, B.,, C. von Eiff,, M. Herrmann,, G. Peters,, and R. A. Proctor. 1996. Staphylococcal small colony variants present a challenge to clinicians and clinical microbiologists. Antimicrob. Infect. Dis. Newsl. 15:5963.
36. Kaplan, M. W.,, and W. E. Dye. 1976. Growth requirements of some small-colony-forming variants of Staphylococcus aureus. J. Clin. Microbiol. 4:343348.
37. Kipp, F.,, W. Ziebuhr,, K. Becker,, V. Krimmer,, N. Hobeta,, G. Peters,, and C. von Eiff. 2003. Detection of Staphylococcus aureus by 16S rRNA directed in situ hybridisation in a patient with a brain abscess caused by small colony variants. J. Neurol. Neurosurg. Psychiatry 74:10001002.
38. Kohler, C.,, C. von Eiff,, G. Peters,, R. A. Proctor,, M. Hecker,, and S. Engelmann. 2003. Physiological characterization of a heme-deficient mutant of Staphylococcus aureus by a proteomic approach. J. Bacteriol. 185:69286937.
39. Koo, S. P.,, A. S. Bayer,, H.-G. Sahl,, R. A. Proctor,, and M. R. Yeaman. 1996. Staphylocidal action of thrombin-induced platelet microbicidal protein (tPMP) is not solely dependent on transmembrane potential (Δψ). Infect. Immun. 64:10701074.
40. Lewis, L. A.,, K. Li,, M. Bharosay,, M. Cannella,, V. Jorgenson,, R. Thomas,, D. Pena,, M. Velez,, B. Pereira,, and A. Sassine. 1990. Characterization of gentamicin-resistant respiratory-deficient (Res) variant strains of Staphylococcus aureus. Microbiol. Immunol. 34:587605.
41. Massey, R. C.,, A. Buckling,, and S. J. Peacock. 2001. Phenotypic switching of antibiotic resistance circumvents permanent costs in Staphylococcus aureus. Curr. Biol. 11:18101814.
42. Massey, R. C.,, and S. J. Peacock. 2002. Antibiotic-resistant sub-populations of the pathogenic bacterium Staphylococcus aureus confer population-wide resistance. Curr. Biol. 12:R686R687.
43. Musher, D. M.,, R. E. Baughn,, G. B. Templeton,, and J. N. Minuth. 1977. Emergence of variant forms of Staphylococcus aureus after exposure to gentamicin and infectivity of the variants in experimental animals. J. Infect. Dis. 136:360369.
44. Neumann, S.,, U. Matthey,, G. Kaim,, and P. Dimroth. 1998. Purification and properties of the F0F1 ATPase of Ilyobacter tartaricus, a sodium ion pump. J. Bacteriol. 180:33123316.
45. Novick, R., 1993. Staphylococcus, p. 1733. In A. L. Sonenshein,, J. A. Hoch,, and R. Losick (ed.), Bacillus subtilis and Other Gram-Positive Bacteria. American Society for Microbiology, Washington, D.C.
46. Novick, R. P. 2003. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol. Microbiol. 48:14291449.
47. Nydahl, B. C.,, and W. L. Hall. 1965. The treatment of staphylococcal infection with nafcillin with a discussion of staphylococcal nephritis. Ann. Intern. Med. 63:2743.
48. Pan, X. S.,, P. J. Hamlyn,, R. Talens-Visconti,, F. L. Alovero,, R. H. Manzo,, and L. M. Fisher. 2002. Small-colony mutants of Staphylococcus aureus allow selection of gyrase-mediated resistance to dual-target fluoroquinolones. Antimicrob. Agents Chemother. 46:24982506.
49. Proctor, R. A., 1994. Microbial pathogenic factors: small colony variants, p. 7790. In A. L. Bisno, and F. A. Waldvogel (ed.), Infections Associated with Indwelling Medical Devices, 2nd ed. American Society for Microbiology, Washington, D.C.
50. Proctor, R. A. 1998. Bacterial energetics and antimicrobial resistance. Drug Resist. Updates 1:227235.
51. Proctor, R. A.,, D. M. Bates,, and P. J. McNamara,. 2001. Electron transport-deficient Staphylococcus aureus small-colony variants as emerging pathogens, p. 95110. In W. Craig (ed.), Emerging Infections, vol. 5. ASM Press, Washington, D.C.
52. Proctor, R. A.,, S. Dalal,, B. Kahl,, D. Brar,, G. Peters,, and W. W. Nichols. 2002. Two diarylurea electron transport inhibitors reduce Staphylococcus aureus hemolytic activity and protect cultured endothelial cells from lysis. Antimicrob. Agents Chemother. 46:23332336.
53. Proctor, R. A.,, J. M. Balwit,, and O. Vesga. 1994. Variant subpopulations of Staphylococcus aureus can cause persistent and recurrent infections. Infect. Agents Dis. 3:302312.
54. Proctor, R. A.,, and G. Peters. 1998. Small colony variants in staphylococcal infections: diagnostic and therapeutic implications. Clin. Infect. Dis. 27:419423.
55. Proctor, R. A.,, P. van Langevelde,, M. Kristjansson,, J. N. Maslow,, and R. D. Arbeit. 1995. Persistent and relapsing infections associated with small colony variants of Staphylococcus aureus. Clin. Infect. Dis. 20:95102.
56. Proctor, R. A.,, O. Vesga,, M. F. Otten,, S.-P. Koo,, M. R. Yeaman,, H.-G. Sahl,, and A. S. Bayer. 1996. Staphylococcus aureus small colony variants cause persistent and resistant infections. Chemotherapy (Basel) 42(Suppl. 2):4752.
57. Ray, S. C.,, R. Schulick,, D. Flayhart,, and J. Dick. 1997. First report of infection with Staphylococcus aureus subspecies anaerobius, abstr. 567. In Proc. 35th Infect. Dis. Soc. Am. Meet. Infectious Disease Society of America, Alexandria, Va.
58. Regassa, L. B.,, R. P. Novick,, and M. J. Betley. 1992. Glucose and nonmaintained pH decrease expression of the accessory gene regulator (agr) in Staphylococcus aureus. Infect. Immun. 60:33813388.
59. Reizere, J.,, M. H. Saier, Jr.,, J. Deutscher,, F. Grenier,, J. Thompson,, and W. Hengstenberg. 1988. The phosphoenolpyruvate:sugar phosphotransferase system in gram-positive bacteria: properties, mechanism, and regulation. Crit. Rev. Microbiol. 15:297338.
60. Sadowska, B.,, A. Bonar,, C. von Eiff,, R. A. Proctor,, M. Chmiela,, W. Rudnicka,, and B. Rozalska. 2002. Characteristics of Staphylococcus aureus, isolated from airways of cystic fibrosis patients, and their small colony variants. FEMS Immunol. Med. Microbiol. 32:191197.
61. Salgado, D. R.,, F. A. Boza,, M. Pinto,, and J. Sampaio. 2001. Outbreak with small colony variants of methicillin-resistant Staphylococcus aureus in an ICU, abstr. K-1226. In Proc. 41st Intersci. Conf. Antimicrob. Agents Chemother. American Society for Microbiology, Washington, D.C.
62. Santana, M.,, M. S. Ionescu,, A. Vertes,, R. Longin,, F. Kunst,, A. Danchin,, and P. Glaser. 1994. Bacillus subtilis F0F1 ATPase: DNA sequence of the atp operon and characterization of atp mutants. J. Bacteriol. 176:68026811.
63. Schlievert, P. M.,, J. R. Dringer,, M. H. Kim,, S. J. Projan,, and R. P. Novick. 1992. Effect of glycerol monolaurate on bacterial growth and toxin production. Antimicrob. Agents Chemother. 36:626631.
64. Schnitzer, R. J.,, L. J. Camagni,, and M. Buck. 1943. Resistance of small colony variants (G forms) of a staphylococcus toward the bacteriostatic activity of penicillin. Proc. Soc. Exp. Biol. Med. 53:7589.
65. Seifert, H.,, C. von Eiff,, and G. Fatkenheuer. 1999. Fatal case due to methicillin-resistant Staphylococcus aureus small colony variants in an AIDS patient. Emerg. Infect. Dis. 5:450453.
66. Seifert, H.,, H. Wisplinghoff,, P. Schnabel,, and C. von Eiff. 2003. Small colony variants of Staphylococcus aureus and pacemaker-related infection. Emerg. Infect. Dis. 9:13161318.
67. Silverman, J. A.,, N. G. Perlmutter,, and H. M. Shapiro. 2003. Correlation of daptomycin bactericidal activity and membrane depolarization in Staphylococcus aureus. Antimicrob. Agents Chemother. 47:25382544.
68. Somerville, G. A.,, M. S. Chaussee,, C. I. Morgan,, J. R. Fitzgerald,, D. W. Dorward,, L. J. Reitzer,, and J. M. Musser. 2002. Staphylococcus aureus aconitase inactivation unexpectedly inhibits post-exponential-phase growth and enhances stationary-phase survival. Infect. Immun. 70:63736382.
69. Somerville, G. A.,, B. Said-Salim,, J. M. Wickman,, S. J. Raffel,, B. N. Kreiswirth,, and J. M. Musser. 2003. Correlation of acetate catabolism and growth yield in Staphylococcus aureus: implications for host-pathogen interactions. Infect. Immun. 71:47244732.
70. Spearman, P.,, D. Lakey,, S. Jotte,, A. Chernowitz,, S. Claycomb,, and C. Stratton. 1996. Sternoclavicular joint septic arthritis with small-colony variant Staphylococcus aureus. Diagn. Microbiol. Infect. Dis. 26:1315.
71. Taber, H. W., 1993. Respiratory chains, p. 199212. In A. L. Sonenshein,, J. A. Hoch,, and R. Losick (ed.), Bacillus subtilis and Other Gram-Positive Bacteria. American Society for Microbiology, Washington, D.C.
72. Tien, W.,, and D. C. White. 1968. Linear sequential arrangement of genes for the biosynthetic pathway of heme in Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 61:13921398.
73. Vaudaux, P.,, P. Francois,, C. Bisognano,, W. L. Kelley,, D. P. Lew,, J. Schrenzel,, R. A. Proctor,, P. J. McNamara,, G. Peters,, and C. von Eiff. 2002. Increased expression of clumping factor and fibronectin-binding proteins by small colony variants of Staphylococcus aureus. Infect. Immun. 70:54285437.
74. Vesga, O.,, J. M. Vann,, D. Brar,, and R. A. Proctor. 1996. Staphylococcus aureus small colony variants are induced by the endothelial cell intracellular milieu. J. Infect. Dis. 173:739742.
75. von Eiff, C.,, P. McNamara,, D. Bates,, K. Becker,, X. Lei,, M. Ziman,, B. Bochner,, G. Peters,, and R. A. Proctor. Phenotype MicroArray of S. aureus menD and hemB mutants with small colony variant (SCV) phenotype. In Proc. 11th Int. Symp. Staphylococci Staphylococcal Infect., Charleston, S.C.
76. von Eiff, C.,, K. Becker,, D. Metze,, G. Lubritz,, J. Hockmann,, T. Schwarz,, and G. Peters. 2001. Intracellular persistence of Staphylococcus aureus small-colony variants within keratinocytes: a cause for antibiotic treatment failure in a patient with Darier’s disease. Clin. Infect. Dis. 32:16431647.
77. von Eiff, C.,, D. Bettin,, R. A. Proctor,, B. Rolauffs,, N. Lindner,, W. Winkelmann,, and G. Peters. 1997. Recovery of small colony variants of Staphylococcus aureus following gentamicin bead placement for osteomyelitis. Clin. Infect. Dis. 25:12501251.
78. von Eiff, C.,, C. Heilmann,, R. A. Proctor,, C. Woltz,, G. Peters,, and F. Götz. 1997. A site-directed Staphylococcus aureus hemB mutant is a small-colony variant which persists intracellularly. J. Bacteriol. 179:47064712.
79. von Eiff, C.,, P. Vaudaux,, B. C. Kahl,, D. Lew,, S. Emler,, A. Schmidt,, G. Peters,, and R. A. Proctor. 1999. Bloodstream infections caused by small-colony variants of coagulase-negative staphylococci following pacemaker implantation. Clin. Infect. Dis. 29:932934.
80. Widmer, A. F.,, A. Wiestner,, R. Frei,, and W. Zimmerli. 1991. Killing of nongrowing and adherent Escherichia coli determines drug efficacy in device-related infections. Antimicrob. Agents Chemother. 35:741746.
81. Wise, R. I.,, and W. W. Spink. 1954. The influence of antibiotics on the origin of small colonies (G variants) of Micrococcus pyogenes var. aureus. J. Clin. Invest. 33:16111622.
82. Xu, K.,, J. Delling,, and T. Elliott. 1992. The genes required for heme synthesis in Salmonella typhimurium include those encoding alternative functions for aerobic and anaerobic coproporphyrinogen oxidation. J. Bacteriol. 174:39533963.
83. Youmans, G. P.,, and E. Delves. 1942. The effect of inorganic salts on the production of small colony variants by Staphylococcus aureus. J. Bacteriol. 44:127136.


Generic image for table

Redox and ATP-producing reactions in SCVs

Abbreviations: ADH, alcohol dehydrogenase; ArcA = arginine deiminase; ArcB = ornithine transcarbamolyase; ArcC = carbamoylate kinase; CitB = aconitase; FadB = 3-hydroxyacyl-CoA dehydrogenase: HMP, hydroxymonocarboxylic acid phosphatase (flavohemoprotein or pyruvate/nitrite reductase); LDH =lactate dehydrogenase; MltD = mannitol-1-phosphate 5-dehydrogenase; Mqo2 - malate:quinone oxidoreductase; PycA = pyruvate carboxylase; PdhB = pyruvate dehydrogenase El component beta subunit; PflB = pyruvate formate lyase.

SA0182 and SA0224 refer to gene numbers in the N315 genome.

Citation: Proctor R. 2006. Respiration and Small-Colony Variants of Staphylococcus aureus, p 434-442. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch35

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