The effect of skin fatty acids on Staphylococcus aureus

Archives of Microbiology

Volumn 197, Issue 2, 2015, Pages 245-267

  Neumann, Yvonne ^a,b,c   Ohlsen, Knut ^d   Donat, Stefanie ^d   Engelmann, Susanne ^c,e,f   Kusch, Harald ^e,g   Albrecht, Dirk ^e   Cartron, Michael ^a   Hurd, Alexander ^a   Foster, Simon J ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^d UNIVERSITY OF WÜRZBURG   (Germany)

^e UNIVERSITY OF GREIFSWALD   (Germany)

^f TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^g UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

C 6 H; Resistance; S. aureus; Skin fatty acid

Indexed keywords

6 HEXADECANOIC ACID; ABC TRANSPORTER; BACTERIAL TOXIN; BINDING PROTEIN; FATTY ACID; MONOVALENT CATION; TRANSCRIPTOME; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; HEXADECENOIC ACID; PALMITIC ACID DERIVATIVE; PROTEOME; VIRULENCE FACTOR;

ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL SECRETION SYSTEM; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; CELL MEMBRANE; CELL MEMBRANE FLUIDITY; CELL TRANSPORT; COLONY FORMING UNIT; CONTROLLED STUDY; EXTRACELLULAR TRAP; GENETIC TRANSCRIPTION; HOST RESISTANCE; INDUCED RESISTANCE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; OPERON; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN METABOLISM; PROTEOMICS; PURINE METABOLISM; PURINE SYNTHESIS; PYRIMIDINE METABOLISM; PYRIMIDINE SYNTHESIS; SKIN FLORA; STAPHYLOCOCCUS AUREUS; TRANSCRIPTOMICS; ANTIBIOTIC RESISTANCE; CELL WALL; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; SKIN;

BACTERIAL PROTEINS; CELL WALL; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MICROBIAL SENSITIVITY TESTS; PALMITIC ACIDS; PROTEOME; SKIN; STAPHYLOCOCCUS AUREUS; VIRULENCE FACTORS;

EID: 84925536333     PISSN: 03028933     EISSN: 1432072X     Source Type: Journal    
DOI: 10.1007/s00203-014-1048-1     Document Type: Article

References (86)

1. Adhikari RP, Novick RP (2008) Regulatory organization of the staphylococcal sae locus. Microbiology 154:949–959
2. Baldassarri L, Bertuccini L, Ammendolia MG, Arciola CR, Montanaro L (2001) Effect of iron limitation on slime production by Staphylococcus aureus. Eur J Clin Microbiol Infect Dis 20:343–345
3. Bayles KW (2003) Are the molecular strategies that control apoptosis conserved in bacteria? Trends Microbiol 11:306–311
4. Bayles KW (2007) The biological role of death and lysis in biofilm development. Nat Rev 5:721–726
5. Becker P, Hufnagle W, Peters G, Herrmann M (2001) Detection of differential gene expression in biofilm-forming versus planktonic populations of Staphylococcus aureus using micro-representational-difference analysis. Appl Environ Microbiol 67:2958–2965
6. Berends ET, Horswill AR, Haste NM, Monestier M, Nizet V, von Kockritz-Blickwede M (2010) Nuclease expression by Staphylococcus aureus facilitates escape from neutrophil extracellular traps. J Innate Immun 2(6):576–586
7. Bernhardt J, Büttner K, Scharf C, Hecker M (1999) Dual channel imaging of two-dimensional electropherograms in Bacillus subtilis. Electrophoresis 20(11):2225–2240
8. Bhakdi S, Tranum-Jensen J (1991) Alpha-toxin of Staphylococcus aureus. Microbiol Rev 55:733–751
9. Brunskill EW, Bayles KW (1996) Identification of LytSR-regulated genes from Staphylococcus aureus. J Bacteriol 178(19):5810–5812
10. Cartron ML, England SR, Chiriac AI, Josten M, Turner R, Rauter Y, Hurd A, Sahl H, Jones S, Foster SJ (2014) Bactericidal activity of the human skin fatty acid cis-6-hexadecanoic acid on Staphylococcus aureus. Antimicrob Agents Chemother 58(7):3599–3609
11. Chamberlain NR, Mehrtens BG, Xiong Z, Kapral FA, Boardman JL, Rearick JI (1991) Correlation of carotenoid production, decreased membrane fluidity, and resistance to oleic acid killing in Staphylococcus aureus 18Z. Infect Immun 59:4332–4337
12. Chan PF, Foster SJ (1998) The role of environmental factors in the regulation of virulence-determinant expression in Staphylococcus aureus 8325-4. Microbiology 144(9):2469–2479
13. Clarke SR (2010) Phenol-soluble modulins of Staphylococcus aureus lure neutrophils into battle. Cell Host Microbe 7(6):423–424
14. Clarke SR, Foster SJ (2008) IsdA protects Staphylococcus aureus against the bactericidal protease activity of apolactoferrin. Infect Immun 76(4):1518–1526
15. Clarke SR, Wiltshire MD, Foster SJ (2004) IsdA of Staphylococcus aureus is a broad spectrum, iron-regulated adhesion. Mol Microbiol 51(5):1509–1519
16. Clarke SR, Mohamed R, Bian L, Routh AF, Kokai-Kun JF, Mond JJ, Tarkowski A, Foster SJ (2007) The Staphylococcus aureus surface protein IsdA mediates resistance to innate defenses of human skin. Cell Host Microbe 1:1–14
17. Cosgrove K, Coutts G, Jonsson IM, Tarkowski A, Kokai-Kun JF, Mond JJ, Foster SJ (2007) Catalase (KatA) and alkyl hydroperoxide reductase (AhpC) have compensatory roles in peroxide stress resistance and are required for survival, persistence, and nasal colonization in Staphylococcus aureus. J Bacteriol 189:1025–1035
18. Duthie ES, Lorent LL (1952) Staphylococcal coagulase; mode of action and antigenicity. J Gen Microbiol 6(1–2):95–107
19. Eymann C, Dreisbach A, Albrecht D, Bernhardt J, Becher D, Gentner S, Tam LT, Büttner K, Buurman G, Scharf C, Venz S, Völker U, Hecker M (2004) A comprehensive proteome map of growing Bacillus subtilis cells. Proteomics 4(10):2849–2876
20. Frees D, Qazi SN, Hill PJ, Ingmer H (2003) Alternative roles of ClpX and ClpP in Staphylococcus aureus stress tolerance and virulence. Mol Microbiol 48:1565–1578
21. Geiger T, Goerke C, Mainiero M, Kraus D, Wolz C (2008) The virulence regulator Sae of Staphylococcus aureus: promoter activities and response to phagocytosis-related signals. J Bacteriol 190:3419–3428
22. Geiger T, Goerke C, Fritz M, Schäfer T, Ohlsen K, Liebeke M, Lalk M, Wolz C (2010) Role of the (p)ppGpp synthase RSH, a RelA/SpoT homolog, in stringent response and virulence of Staphylococcus aureus. Infect Immun 78(5):1873–1883
23. Giesbrecht P, Kersten T, Maidhof H, Wecke J (1998) Staphylococcal cell wall: morphogenesis and fatal variations in the presence of penicillin. Microbiol Mol Biol Rev 62(4):1371–1414
24. Giraudo AT, Raspanti CG, Calzolari A, Nagel R (1994) Characterization of a Tn551-mutant of Staphylococcus aureus defective in the production of several exoproteins. J Microbiol 40(8):677–681
25. Giraudo AT, Cheung AL, Nagel R (1997) The sae locus of Staphylococcus aureus controls exoprotein synthesis at the transcriptional level. Arch Microbiol 168(1):53–58
26. Giraudo AT, Calzolari A, Cataldi AA, Bogni C, Nagel R (1999) The sae locus of Staphylococcus aureus encodes a two-component regulatory system. FESM 177(1):15–22
27. Goerke C, Fluckiger U, Steinhuber A, Zimmerli W, Wolz C (2001) Impact of the regulatory loci agr, sarA and sae of Staphylococcus aureus on the induction of alpha-toxin during device-related infection resolved by direct quantitative transcript analysis. Mol Microbiol 40:1439–1447
28. Goerke C, Esser S, Kummel M, Wolz C (2005) Staphylococcus aureus strain designation by agr and cap polymorphism typing and delineation of agr diversification by sequence analysis. Int J Med Microbiol 295(2):67–75
29. Groicher KH, Firek BA, Fujimoto DF, Bayles KW (2000) The Staphylococcus aureus lrgAB operon modulates murein hydrolase activity and penicillin tolerance. J Bacteriol 182:1794–1801
30. Gründling A, Missiakas DM, Schneewind O (2006) Staphylococcus aureus mutants with increased lysostaphin resistance. J Bacteriol 188(17):6286–6297
31. Harraghy N, Kormanec J, Wolz C, Homerova D, Goerke C, Ohlsen K, Qazi S, Hill P, Herrmann M (2005) sae is essential for expression of the staphylococcal adhesins Eap and Emp. Microbiology 151(Pt 6):1789–1800
32. Heinrichs JH, Gatlin LE, Kunsch C, Choi GH, Hanson MS (1999) Identification and characterization of SirA, an iron-regulated protein from Staphylococcus aureus. J Bacteriol 181(5):1436–1443
33. Henze UU, Berger-Bachi B (1996) Penicillin-binding protein 4 overproduction increases beta-lactam resistance in Staphylococcus aureus. Antimicrob Agents Chemother 40(9):2121–2125
34. Holland KT, Taylor D, Farrell AM (1994) The effect of glycerol monolaurate on growth of, and production of toxic shock syndrome toxin-1 and lipase by, Staphylococcus aureus. J Antimicrob Chemother 33:41–55
35. Horsburgh MJ, Ingham E, Foster SJ (2001) In Staphylococcus aureus, fur is an interactive regulator with PerR, contributes to virulence, and is necessary for oxidative stress resistance through positive regulation of catalase and iron homeostasis. J Bacteriol 183(2):468–475
36. Kabara JJ, Swieczkowski DM, Conley AJ, Truant JP (1972) Fatty acids and derivatives as antimicrobial agents. Antimicrob Agents Chemother 2(1):23–28
37. Karakawa WW, Vann WF (1982) Capsular polysaccharides of Staphylococcus aureus. Semin Infect Dis 4:285–293
38. Kashiwagi K, Miyamoto S, Nukui E, Kobayashi H, Igarashi K (1993) Functions of potA and potD proteins in spermidine-preferential uptake system in Escherichia coli. J Biol Chem 268(26):19358–19363
39. Kenny JG, Ward D, Josefsson E, Jonsson IM, Hinds J, Rees HH, Lindsay JA, Tarkowski A, Horsburgh MJ (2009) The Staphylococcus aureus response to unsaturated long chain free fatty acids: survival mechanisms and virulence implications. PLoS One 4:e4344
40. Knapp HR, Melly MA (1986) Bactericidal effects of polyunsaturated fatty acids. J Infect Dis 154(1):84–94
41. Kobayashi M, Shimizu S (1999) Cobalt proteins. Eur J Biochem 261(1):1–9
42. Kohler T, Weidenmaier C, Peschel A (2009) Wall teichoic acid protects Staphylococcus aureus against antimicrobial fatty acids from human skin. J Bacteriol 191:4482–4484
43. Koprivnjak T, Mlakar V, Swanson L, Fournier B, Peschel A, Weiss JP (2006) Cation-induced transcriptional regulation of the dlt operon of Staphylococcus aureus. J Bacteriol 188(10):3622–3630
44. Kuroda M, Kuroda H, Oshima T, Takeuchi F, Mori H, Hiramatsu K (2003) Two-component system VraSR positively modulates the regulation of cell-wall biosynthesis pathway in Staphylococcus aureus. Mol Microbiol 49(3):807–821
45. Kusser WC, Ishiguro EE (1988) Effects of aminoglycosides and spectinomycin on the synthesis and release of lipopolysaccharide by Escherichia coli. Antimicrob Agents Chemother 32(8):1247–1250
46. MacMillan SV, Alexander DA, Culham DE, Kunte HJ, Marshall EV, Rochon D, Wood JM (1999) The ion coupling and organic substrate specificities of osmoregulatory transporter ProP in Escherichia coli. Biochim Biophys Acta 1420(1–2):30–44
47. McDevitt D, Francois P, Vaudaux P, Foster TJ (1994) Molecular characterization of the clumping factor (fibrinogen receptor) of Staphylococcus aureus. Mol Microbiol 11:237–248
48. McDevitt D, Nanavaty T, House-Pompeo K, Bell E, Turner N, McIntire L, Foster T, Hook M (1997) Characterization of the interaction between the Staphylococcus aureus clumping factor (ClfA) and fibrinogen. Eur J Biochem 247:416–424
49. Miller SJ, Aly R, Shinefield HR, Elias PM (1988) Antimicrobial activity of stratum corneum lipids from normal and essential fatty acid-deficient mice. Arch Dermatol 124:209–215
50. Mishra NN, Liu GY, Yeaman MR, Yang SJ, Bayer AS (2009) Carotenoid induced alteration of cell membrane (CM) fluidity impacts Staphylococcus aureus susceptibility to innate host defense peptides in vitro, abstr. C1-1362, p. 75. Abstract 49th Interscience conference Antimicrob. Agents Chemother. American Society for Microbiology, Washington, DC
51. Needham AJ, Kibart M, Crossley H, Ingham PW, Foster SJ (2004) Drosophila melanogaster as a model host for Staphylococcus aureus infection. Microbiology 150:2347–2355
52. Neuhaus FC, Baddiley J (2003) A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol Mol Biol Rev 67(4):686–723
53. Niyousaba F, Ogawa H (2005) Protective roles of the skin against infection: implication of naturally occurring human antimicrobial agents beta-defensins, cathelicidin LL-37 and lysozyme. J Dermatol Sci 40(3):157–168
54. Nolan T, Hands RE, Bustin SA (2006) Quantification of mRNA using real-time RT-PCR. Nat Protoc 1(3):1559–1582
55. Novick RP, Jiang D (2003) The staphylococcus saeRS system coordinates environmental signal with agr quorum sensing. Microbiology 149(10):2709–2717
56. Ong PY, Ohtake T, Brandt C, Strickland I, Boguniewicz M, Ganz T, Gallo RL, Leung DY (2002) Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med 347(15):1151–1160
57. O’Riordan K, Lee JC (2004) Staphylococcus aureus capsular polysaccharides. Clin Microbiol Rev 17:218–234
58. + circulation in cells. Biochim Biophys Acta 1187(2):206–210
59. Patton TG, Yang SJ, Bayles KW (2006) The role of proton motive force in expression of the Staphylococcus aureus cid and lrg operons. Mol Microbiol 59:1395–1404
60. Paulus TJ, McGarry TJ, Shekelle PG, Rosenzweig S, Switzer RL (1982) Coordinate synthesis of the enzymes of pyrimidine biosynthesis in Bacillus subtilis. J Bacteriol 149(2):775–778
61. Peacock SJ, Foster TJ, Cameron BJ, Berendt AR (1999) Bacterial fibronectin-binding proteins and endothelial cell surface fibronectin mediate adherence of Staphylococcus aureus to resting human endothelial cells. Microbiology 145(Pt 12):3477–3486
62. Peacock SJ, de Silva I, Lowy FD (2001) What determines nasal carriage of Staphylococcus aureus? Trends Microbiol 9(12):605–610
63. Peschel A (2002) How do bacteria resist human antimicrobial peptides? Trends Microbiol 10(4):179–186
64. Pohl K, Francois P, Stenz L, Schlink L, Geiger T, Herbert S, Goerke C, Schrenzel J, Wolz C (2009) CodY in Staphylococcus aureus: a regulatory link between metabolism and virulence gene expression. J Bacteriol 191(9):2953–2963
65. Projan SJ, Brown-Skrobot S, Schlievert PM, Vandenesch F, Novick RP (1994) Glycerol monolaurate inhibits the production of β-lactamase, toxic shock syndrome toxin-1, and other staphylococcal exoproteins by interfering with signal transduction. J Bacteriol 176:4204–4209
66. Proksch E, Brandner JM, Jensen JM (2008) The skin: an indispensable barrier. Exp Dermatol 17(12):1063–1072
67. Ramadurai L, Lockwood KJ, Nadakavukaren MJ, Jayaswal RK (1999) Characterization of a chromosomally encoded glycylglycine endopeptidase of Staphylococcus aureus. Microbiology 145(Pt 4):801–808
68. Rice KC, Firek BA, Nelson JB, Yang SJ, Patton TG, Bayles KW (2003) The Staphylococcus aureus cidAB operon: evaluation of its role in regulation of murein hydrolase activity and penicillin tolerance. J Bacteriol 185:2635–2643
69. Ruzin A, Novick RP (1998) Glycerol monolaurate inhibits induction of vancomycin resistance in Enterococcus faecalis. J Bacteriol 180:182–185
70. Schlievert PM, Deringer JR, Kim MH, Projan SJ, Novick RP (1992) Effect of glycerol monolaurate on bacterial growth and toxin production. Antimicrob Agents Chemother 36:621–626
71. Sebulsky MT, Hohnstein D, Hunter MD, Heinrichs DE (2000) Identification and characterization of a membrane permease involved in iron-hydroxamate transport in Staphylococcus aureus. J Bacteriol 182(16):4394–4400
72. Sebulsky MT, Shilton BH, Speziali CD, Heinrichs DE (2003) The role of FhuD2 in iron(III)-hydroxamate transport in Staphylococcus aureus demonstration that FhuD2 binds iron(III)-hydroxamates but with minimal conformational change and implication of mutations on transport. J Biol Chem 278(50):49890–49900
73. Sharma-Kuinkel BK, Mann EE, Ahn JS, Kuechenmeister LJ, Dunman PM, Bayles KW (2009) The Staphylococcus aureus LytSR two-component regulatory system affects biofilm formation. J Bacteriol 191(15):4767–4775
74. Shin SY, Bajpai VK, Kim HR, Kang SC (2007) Antibacterial activity of bioconverted eicosapentaenoic (EPA) and docosahexaenoic acid (DHA) against foodborne pathogenic bacteria. Int J Food Microbiol 113(2):233–236
75. Srivatsan A, Wang JD (2008) Control of bacterial transcription, translation and replication by (p)ppGpp. Curr Opin Microbiol 11:100–105
76. Takigawa H, Nakagawa H, Kuzukawa M, Mori H, Imokawa G (2005) Deficient production of hexadecanoic acid in the skin is associated in part with the vulnerability of atopic dermatitis patients to colonization by Staphylococcus aureus. Dermatology 211:240–248
77. Turnbough CL Jr, Switzer RL (2008) Regulation of pyrimidine biosynthetic gene expression in bacteria: repression without repressors. Microbiol Mol Biol Rev 72(2):266–300
78. Turner RJ, Lu Y, Switzer RL (1994) Regulation of the Bacillus subtilis pyrimidine biosynthetic (pyr) gene cluster by an autogenous transcriptional attenuation mechanism. J Bacteriol 176(12):3708–3722
79. Vetter SM, Schlievert PM (2005) Glycerol monolaurate inhibits virulence factor production in Bacillus anthracis. Antimicrob Agents Chemother 49:1302–1305
80. Watts A, Ke D, Wang Q, Pillay A, Nicholson-Weller A, Lee JC (2005) Staphylococcus aureus strains that express serotype 5 or serotype 8 capsular polysaccharides differ in virulence. Infect Immun 73:3502–3511
81. Weidenmaier C, Peschel A, Kempf VA, Lucindo N, Yeaman MR, Bayer AS (2005) DltABCD- and MprF-mediated cell envelope modifications of Staphylococcus aureus confer resistance to platelet microbicidal proteins and contribute to virulence in a rabbit endocarditis model. Infect Immun 73(12):8033–8038
82. Wille JJ, Kydonieus A (2003) Palmitoleic acid isomer (C16:1Δ6) in human skin sebum is effective against gram-positive bacteria. Skin Pharmacol Appl Skin Physiol 16:176–187
83. Wolf C, Hochgräfe F, Kusch H, Albrecht D, Hecker M, Engelmann S (2008) Proteomic analysis of antioxidant strategies of Staphylococcus aureus: diverse responses to different oxidants. Proteomics 8(15):3139–3153
84. Wolz C, Geiger T, Goerke C (2010) The synthesis and function of the alarmone (p)ppGpp in firmicutes. Int J Med Microbiol 300:142–147
85. Xu CP, Boks NP, de Vries J, Kaper HJ, Norde W, Busscher HJ, van der Mei HC (2008) Staphylococcus aureus-fibronectin interactions with and without fibronectin-binding proteins and their role in adhesion and desorption. Appl Environ Microbiol 74:7522–7528
86. Zhang L, Jacobsson K, Vasi J, Lindberg M, Frykberg L (1998) A second IgG-binding protein in Staphylococcus aureus. Microbiology (Reading, England) 144(Pt 4):985–991