Incorporation of exogenous fatty acids protects Enterococcus faecalis from membrane-damaging agents

Applied and Environmental Microbiology

Volumn 80, Issue 20, 2014, Pages 6527-6538

  Saito, Holly E ^a   Harp, John R ^a   Fozo, Elizabeth M ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENTEROCOCCUS FAECALIS;

ADAPTATION; FATTY ACID; GROWTH RESPONSE; MEMBRANE; MICROBIAL COMMUNITY; SURVIVORSHIP; TEMPERATURE TOLERANCE;

ENTEROCOCCUS FAECALIS;

ANTIINFECTIVE AGENT; BILE ACID; DAPTOMYCIN; FATTY ACID; LINOLEIC ACID; OLEIC ACID;

ADAPTATION; ANTIBIOTIC RESISTANCE; BILE; CELL MEMBRANE; CHEMISTRY; DRUG EFFECTS; ENTEROCOCCUS FAECALIS; METABOLISM; PHYSIOLOGY;

ADAPTATION, BIOLOGICAL; ANTI-BACTERIAL AGENTS; BILE; BILE ACIDS AND SALTS; CELL MEMBRANE; DAPTOMYCIN; DRUG RESISTANCE, BACTERIAL; ENTEROCOCCUS FAECALIS; FATTY ACIDS; LINOLEIC ACID; OLEIC ACID;

EID: 84907279943     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02044-14     Document Type: Article

References (51)

1. Fisher K, Phillips C. 2009. The ecology, epidemiology and virulence of Enterococcus. Microbiology 155:1749-1757. http://dx.doi.org/10.1099/mic.0.026385-0.
2. Byappanahalli MN, Nevers MB, Korajkic A, Staley ZR, Harwood VJ. 2012. Enterococci in the environment. Microbiol. Mol. Biol. Rev. 76:685-706. http://dx.doi.org/10.1128/MMBR.00023-12.
3. Jonas BM, Murray BE, Weinstock GM. 2001. Characterization of emeA, a NorA homolog and multidrug resistance efflux pump, in Enterococcus faecalis. Antimicrob. Agents Chemother. 45:3574-3579. http://dx.doi.org/10.1128/AAC.45.12.3574-3579.2001.
4. Arias CA, Murray BE. 2012. The rise of the Enterococcus: beyond vancomycin resistance. Nat. Rev. Microbiol. 10:266-278. http://dx.doi.org/10.1038/nrmicro2761.
5. Coburn PS, Baghdayan AS, Dolan GT, Shankar N. 2007. Horizontal transfer of virulence genes encoded on the Enterococcus faecalis pathogenicity island. Mol. Microbiol. 63:530-544. http://dx.doi.org/10.1111/j.1365-2958.2006.05520.x.
6. Paulsen IT, Banerjei L, Myers GSA, Nelson KE, Seshadri R, Read TD, Fouts DE, Eisen JA, Gill SR, Heidelberg JF, Tettelin H, Dodson RJ, Umayam L, Brinkac L, Beanan M, Daugherty S, DeBoy RT, Durkin S, Kolonay J, Madupu R, Nelson W, Vamathevan J, Tran B, Upton J, Hansen T, Shetty J, Khouri H, Utterback T, Radune D, Ketchum KA, Dougherty BA, Fraser CM. 2003. Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299:2071-2074. http://dx.doi.org/10.1126/science.1080613.
7. Begley M, Gahan CG, Hill C. 2005. The interaction between bacteria and bile. FEMS Microbiol. Rev. 29:625-651. http://dx.doi.org/10.1016/j.femsre.2004.09.003.
8. Quillin SJ, Schwartz KT, Leber JH. 2011. The novel Listeria monocytogenes bile sensor BrtA controls expression of the cholic acid efflux pump MdrT. Mol. Microbiol. 81:129-142. http://dx.doi.org/10.1111/j.1365-2958.2011.07683.x.
9. Rosenberg EY, Bertenthal D, Nilles ML, Bertrand KP, Nikaido H. 2003. Bile salts and fatty acids induce the expression of Escherichia coli AcrAB multidrug efflux pump through their interaction with Rob regulatory protein. Mol. Microbiol. 48:1609-1619. http://dx.doi.org/10.1046/j.1365-2958.2003.03531.x.
10. Piddock LJ. 2006. Multidrug-resistance efflux pumps-not just for resistance. Nat. Rev. Microbiol. 4:629-636. http://dx.doi.org/10.1038/nrmicro1464.
11. Solheim M, Aakra A, Vebo H, Snipen L, Nes IF. 2007. Transcriptional responses of Enterococcus faecalis V583 to bovine bile and sodium dodecyl sulfate. Appl. Environ. Microbiol. 73:5767-5774. http://dx.doi.org/10.1128/AEM.00651-07.
12. Bohle LA, Faergestad EM, Veiseth-Kent E, Steinmoen H, Nes IF, Eijsink VG, Mathiesen G. 2010. Identification of proteins related to the stress response in Enterococcus faecalis V583 caused by bovine bile. Proteome Sci. 8:37. http://dx.doi.org/10.1186/1477-5956-8-37.
13. Rincé A, Le Breton Y, Verneuil N, Giard J-C, Hartke A, Auffray Y. 2003. Physiological and molecular aspects of bile salt response in Enterococcus faecalis. Int. J. Food Microbiol. 88:207-213. http://dx.doi.org/10.1016/S0168-1605(03)00182-X.
14. Zhang YM, Rock CO. 2008. Membrane lipid homeostasis in bacteria. Nat. Rev. Microbiol. 6:222-233. http://dx.doi.org/10.1038/nrmicro1839.
15. Shivaji S, Prakash JS. 2010. How do bacteria sense and respond to low temperature? Arch. Microbiol. 192:85-95. http://dx.doi.org/10.1007/s00203-009-0539-y.
16. Fozo EM, Quivey RG, Jr. 2004. Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl. Environ. Microbiol. 70:929-936. http://dx.doi.org/10.1128/AEM.70.2.929-936.2004.
17. Fozo EM, Quivey RG, Jr. 2004. The fabM gene product of Streptococcus mutans is responsible for the synthesis of monounsaturated fatty acids and is necessary for survival at low pH. J. Bacteriol. 186:4152-4158. http://dx.doi.org/10.1128/JB.186.13.4152-4158.2004.
18. Chang Y-Y, Cronan JE, Jr. 1999. Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol. Microbiol. 33:249-259. http://dx.doi.org/10.1046/j.1365-2958.1999.01456.x.
19. Jungkind DL, Wood RC. 1974. Physiological differences between cyclopropane fatty acid-deficient mutants and the parent strain of Streptococcus faecalis. Biochim. Biophys. Acta 337:298-310. http://dx.doi.org/10.1016/0005-2760(74)90211-2.
20. Bao Y, Sakinc T, Laverde D, Wobser D, Benachour A, Theilacker C, Hartke A, Huebner J. 2012. Role of mprF1 and mprF2 in the pathogenicity of Enterococcus faecalis. PLoS One 7:e38458. http://dx.doi.org/10.1371/journal.pone.0038458.
21. Roy H. 2009. Tuning the properties of the bacterial membrane with aminoacylated phosphatidylglycerol. IUBMB Life 61:940-953. http://dx.doi.org/10.1002/iub.240.
22. Fujita Y, Matsuoka H, Hirooka K. 2007. Regulation of fatty acid metabolism in bacteria. Mol. Microbiol. 66:829-839. http://dx.doi.org/10.1111/j.1365-2958.2007.05947.x.
23. Parsons JB, Yao J, Frank MW, Jackson P, Rock CO. 2012. Membrane disruption by antimicrobial fatty acids releases low-molecular-weight proteins from Staphylococcus aureus. J. Bacteriol. 194:5294-5304. http://dx.doi.org/10.1128/JB.00743-12.
24. Parsons JB, Frank MW, Subramanian C, Saenkham P, Rock CO. 2011. Metabolic basis for the differential susceptibility of Grampositive pathogens to fatty acid synthesis inhibitors. Proc. Natl. Acad. Sci. U. S. A. 108:15378-15383. http://dx.doi.org/10.1073/pnas.1109208108.
25. Sasser M, Kuntisky C, Jackoway G, Ezzell JW, Teska JD, Harper B, Parker S, Barden B, Blair H, Breezee J, Carpenter J, Cheek WV, DeMartino M, Evans B, Ezzell JW, Francesconi S, Franko E, Gardner W, Glazier M, Greth K, Harper T, Hart T, Hodel M, Holmes-Talbot K, Hopkins KL, Iqbal A, Johnson D, Madonna A, McDowell M, McKee ML, Park M, Parker S, Pentella M, Radosevic J, Robison RA, Rotzoll B, Scott K, Smith M, Syed N, Tang J, Teska JD, Trinh H, Williams LI, Wolcott M. 2005. Identification of Bacillus anthracis from culture using gas chromatographic analysis of fatty acid methyl esters. J. AOAC Int. 88:178-181.
26. Merritt ME, Donaldson JR. 2009. Effect of bile salts on the DNA and membrane integrity of enteric bacteria. J. Med. Microbiol. 58:1533-1541. http://dx.doi.org/10.1099/jmm.0.014092-0.
27. Trauner M, Boyer JL. 2003. Bile salt transporters: molecular characterization, function, and regulation. Physiol. Rev. 83:633-671.
28. Brinster S, Lamberet G, Staels B, Trieu-Cuot P, Gruss A, Poyart C. 2009. Type II fatty acid synthesis is not a suitable antibiotic target for Gram-positive pathogens. Nature 458:83-86. http://dx.doi.org/10.1038/nature07772.
29. Giles DK, Hankins JV, Guan Z, Trent MS. 2011. Remodelling of the Vibrio cholerae membrane by incorporation of exogenous fatty acids from host and aquatic environments. Mol. Microbiol. 79:716-728. http://dx.doi.org/10.1111/j.1365-2958.2010.07476.x.
30. Johnsson T, Nikkila P, Tolovonen L, Rosenqvist H, Laakso S. 1995. Cellular fatty acid profiles of Lactobacillus and Lactococcus strains in relation to the oleic acid content of the cultivation medium. Appl. Environ. Microbiol. 61:4497-4499.
31. Grogan DW, Cronan JE, Jr. 1997. Cyclopropane ring formation in membrane lipids of bacteria. Microbiol. Mol. Biol. Rev. 61:429-441.
32. Jungkind DL, Wood RC. 1974. Factors involved in the synthesis of cyclopropane fatty acids by Streptococcus faecalis. Biochim. Biophys. Acta 337:286-297. http://dx.doi.org/10.1016/0005-2760(74)90210-0.
33. Arias CA, Panesso D, McGrath DM, Qin X, Mojica MF, Miller C, Diaz L, Tran TT, Rincon S, Barbu EM, Reyes J, Roh JH, Lobos E, Sodergren E, Pasqualini R, Arap W, Quinn JP, Shamoo Y, Murray BE, Weinstock GM. 2011. Genetic basis for in vivo daptomycin resistance in enterococci. N. Engl. J. Med. 365:892-900. http://dx.doi.org/10.1056/NEJMoa1011138.
34. Alborn WE, Jr, Allen NE, Preston DA. 1991. Daptomycin disrupts membrane potential in growing Staphylococcus aureus. Antimicrob. Agents Chemother. 35:2282-2287. http://dx.doi.org/10.1128/AAC.35.11.2282.
35. Muraih JK, Pearson A, Silverman J, Palmer M. 2011. Oligomerization of daptomycin on membranes. Biochim. Biophys. Acta 1808:1154-1160. http://dx.doi.org/10.1016/j.bbamem.2011.01.001.
36. Silverman JA, Perlmutter NG, Shapiro HM. 2003. Correlation of daptomycin bactericidal activity and membrane depolarization in Staphylococcus aureus. Antimicrob. Agents Chemother. 47:2538-2544. http://dx.doi.org/10.1128/AAC.47.8.2538-2544.2003.
37. Straus SK, Hancock RE. 2006. Mode of action of the new antibiotic for Gram-positive pathogens daptomycin: comparison with cationic antimicrobial peptides and lipopeptides. Biochim. Biophys. Acta 1758:1215-1223. http://dx.doi.org/10.1016/j.bbamem.2006.02.009.
38. Bayer AS, Schneider T, Sahl HG. 2013. Mechanisms of daptomycin resistance in Staphylococcus aureus: role of the cell membrane and cell wall. Ann. N. Y. Acad. Sci. 1277:139-158. http://dx.doi.org/10.1111/j.1749-6632.2012.06819.x.
39. Mishra NN, Bayer AS, Tran TT, Shamoo Y, Mileykovskaya E, Dowhan W, Guan Z, Arias CA. 2012. Daptomycin resistance in enterococci is associated with distinct alterations of cell membrane phospholipid content. PLoS One 7:e43958. http://dx.doi.org/10.1371/journal.pone.0043958.
40. Tran TT, Panesso D, Mishra NN, Mileykovskaya E, Guan Z, Munita JM, Reyes J, Diaz L, Weinstock GM, Murray BE, Shamoo Y, Dowhan W, Bayer AS, Arias CA. 2013. Daptomycin-resistant Enterococcus faecalis diverts the antibiotic molecule from the division septum and remodels cell membrane phospholipids. mBio 4(4):e00281-13. http://dx.doi.org/10.1128/mBio.00281-13.
41. Palmer KL, Daniel A, Hardy C, Silverman J, Gilmore MS. 2011. Genetic basis for daptomycin resistance in enterococci. Antimicrob. Agents Chemother. 55:3345-3356. http://dx.doi.org/10.1128/AAC.00207-11.
42. Fozo EM, Kawano M, Fontaine F, Kaya Y, Mendieta KS, Jones KL, Ocampo A, Rudd KE, Storz G. 2008. Repression of small toxic protein synthesis by the Sib and OhsC small RNAs. Mol. Microbiol. 70:1076-1093. http://dx.doi.org/10.1111/j.1365-2958.2008.06394.x.
43. Wickens HJ, Pinney RJ, Mason DJ, Gant VA. 2000. Flow cytometric investigation of filamentation, membrane patency, and membrane potential in Escherichia coli following ciprofloxacin exposure. Antimicrob. Agents Chemother. 44:682-687. http://dx.doi.org/10.1128/AAC.44.3.682-687.2000.
44. Fozo EM, Kajfasz JK, Quivey RG, Jr. 2004. Low pH-induced membrane fatty acid alterations in oral bacteria. FEMS Microbiol. Lett. 238:291-295. http://dx.doi.org/10.1111/j.1574-6968.2004.tb09769.x.
45. Quivey RG, Jr, Faustoferri R, Monahan K, Marquis R. 2000. Shifts in membrane fatty acid profiles associated with adaptation of Streptococcus mutans. FEMS Microbiol. Lett. 189:89-92. http://dx.doi.org/10.1111/j.1574-6968.2000.tb09211.x.
46. Aguilar PS, Cronan JE, Jr, de Mendoza D. 1998. A Bacillus subtilis gene induced by cold shock encodes a membrane phospholipid desaturase. J. Bacteriol. 180:2194-2200.
47. Bourgogne A, Garsin DA, Qin X, Singh KV, Sillanpaa J, Yerrapragada S, Ding Y, Dugan-Rocha S, Buhay C, Shen H, Chen G, Williams G, Muzny D, Maadani A, Fox KA, Gioia J, Chen L, Shang Y, Arias CA, Nallapareddy SR, Zhao M, Prakash VP, Chowdhury S, Jiang H, Gibbs RA, Murray BE, Highlander SK, Weinstock GM. 2008. Large scale variation in Enterococcus faecalis illustrated by the genome analysis of strain OG1RF. Genome Biol. 9:R110. http://dx.doi.org/10.1186/gb-2008-9-7-r110.
48. Kubota N, Kuzumoto K, Hidaka E, Yoshizawa K, Oana K, Ogiso Y, Nakamura T, Kawakami Y. 2013. First isolation of oleate-dependent Enterococcus faecalis small-colony variants from the umbilical exudate of a paediatric patient with omphalitis. J. Med. Microbiol. 62:1883-1890. http://dx.doi.org/10.1099/jmm.0.062752-0.
49. Flahaut S, Frere J, Boutibonnes P, Auffray Y. 1996. Comparison of the bile salts and sodium dodecyl sulfate stress responses in Enterococcus faecalis. Appl. Environ. Microbiol. 62:2416-2420.
50. Wright HT, Reynolds KA. 2007. Antibacterial targets in fatty acid biosynthesis. Curr. Opin. Microbiol. 10:447-453. http://dx.doi.org/10.1016/j.mib.2007.07.001.
51. Parsons JB, Rock CO. 2011. Is bacterial fatty acid synthesis a valid target for antibacterial drug discovery? Curr. Opin. Microbiol. 14:544-549. http://dx.doi.org/10.1016/j.mib.2011.07.029.