Friend turned foe: Evolution of enterococcal virulence and antibiotic resistance

Annual Review of Microbiology

Volumn 68, Issue , 2014, Pages 337-356

  Van Tyne, Daria ^a   Gilmore, Michael S ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Enterococcus; Genomics; Human associated microbial flora

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; AVOPARCIN; CHLORAMPHENICOL; GENTAMICIN; TETRACYCLINE; ANTIINFECTIVE AGENT;

ANTIBIOTIC RESISTANCE; BACTERIAL VIRULENCE; DISEASE EXACERBATION; ENTEROCOCCAL INFECTION; HOSPITAL INFECTION; HUMAN; MOLECULAR EVOLUTION; NONHUMAN; REVIEW; ANIMAL; DRUG EFFECTS; ENTEROCOCCUS; EVOLUTION; GENETICS; GRAM-POSITIVE BACTERIAL INFECTIONS; MICROBIOLOGY; PATHOGENICITY; VIRULENCE;

ANIMALS; ANTI-BACTERIAL AGENTS; BIOLOGICAL EVOLUTION; DRUG RESISTANCE, BACTERIAL; ENTEROCOCCUS; GRAM-POSITIVE BACTERIAL INFECTIONS; HUMANS; VIRULENCE;

EID: 84907500590     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-091213-113003     Document Type: Review

References (135)

1. Acar J, Casewell M, Freeman J, Friis C, Goossens H. 2000. Avoparcin and virginiamycin as animal growth promoters: a plea for science in decision-making. Clin. Microbiol. Infect. 6:477-82
2. Arias CA, Murray BE. 2012. The rise of the Enterococcus: beyond vancomycin resistance. Nat. Rev. Microbiol. 10:266-78
3. Bager F, Aarestrup FM, MadsenM,Wegener HC. 1999. Glycopeptide resistance in Enterococcus faecium from broilers and pigs following discontinued use of avoparcin. Microb. Drug Resist. 5:53-56
4. Bates J. 1997. Epidemiology of vancomycin-resistant enterococci in the community and the relevance of farm animals to human infection. J. Hosp. Infect. 37:89-101
5. Benveniste R, Davies J. 1973. Aminoglycoside antibiotic-inactivating enzymes in actinomycetes similar to those present in clinical isolates of antibiotic-resistant bacteria. Proc. Natl. Acad. Sci. USA 70:2276-80
6. Bleiweis AS, Zimmerman LN. 1964. Properties of proteinase from Streptococcus faecalis var. Liquefaciens. J. Bacteriol. 88:653-59
7. Brock TD, Peacher B, Pierson D. 1963. Survey of the bacteriocines of enterococci. J. Bacteriol. 86:702-7
8. Broderick NA, Raffa KF, Goodman RM, Handelsman J. 2004. Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl. Environ.Microbiol. 70:293-300
9. Brown SP, Cornforth DM, Mideo N. 2012. Evolution of virulence in opportunistic pathogens: generalism, plasticity, and control. Trends Microbiol. 20:336-42
10. Byappanahalli MN, NeversMB, Korajkic A, Staley ZR, Harwood VJ. 2012. Enterococci in the environment. Microbiol. Mol. Biol. Rev. 76:685-706
11. Casadevall A, Pirofski L. 2001. Host-pathogen interactions: the attributes of virulence. J. Infect. Dis. 184:337-44
12. Cattoir V, Leclercq R. 2013. Twenty-five years of shared life with vancomycin-resistant enterococci: Is it time to divorce? J. Antimicrob. Chemother. 68:731-42
13. Chang S, Sievert DM, Hageman JC, BoultonML, Tenover FC, et al. 2003. Infection with vancomycinresistant Staphylococcus aureus containing the vanA resistance gene. N. Engl. J. Med. 348:1342-47
14. Chow JW, Thal LA, Perri MB, Vazquez JA, Donabedian SM, et al. 1993. Plasmid-associated hemolysin and aggregation substance production contribute to virulence in experimental enterococcal endocarditis. Antimicrob. Agents Chemother. 37:2474-77
15. Chuang ON, Schlievert PM, Wells CL, Manias DA, Tripp TJ, Dunny GM. 2009. Multiple functional domains of Enterococcus faecalis aggregation substance Asc10 contribute to endocarditis virulence. Infect. Immun. 77:539-48
16. Chuang-Smith ON, Wells CL,Henry-Stanley MJ,Dunny GM. 2010. Acceleration of Enterococcus faecalis biofilm formation by aggregation substance expression in an ex vivo model of cardiac valve colonization. PLoS ONE 5:e15798
17. Clewell DB, Weaver KE. 1989. Sex pheromones and plasmid transfer in Enterococcus faecalis. Plasmid 21:175-84
18. Coque TM, Tomayko JF,Ricke SC, Okhyusen PC,Murray BE. 1996. Vancomycin-resistant enterococci from nosocomial, community, and animal sources in the United States. Antimicrob. Agents Chemother. 40:2605-9
19. Cox CR, Coburn PS, GilmoreMS. 2005. Enterococcal cytolysin: a novel two component peptide system that serves as a bacterial defense against eukaryotic and prokaryotic cells. Curr. Protein Pept. Sci. 6:77-84
20. Cox CR, Gilmore MS. 2007. Native microbial colonization of Drosophila melanogaster and its use as a model of Enterococcus faecalis pathogenesis. Infect. Immun. 75:1565-76
21. Creti R, Imperi M, Bertuccini L, Fabretti F, Orefici G, et al. 2004. Survey for virulence determinants among Enterococcus faecalis isolated from different sources. J. Med. Microbiol. 53:13-20
22. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, et al. 2013. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559-63
23. Davies J. 1990. What are antibiotics? Archaic functions for modern activities. Mol. Microbiol. 4:1227-32
24. Davies J, Davies D. 2010. Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 74:417-33
25. DCosta VM, King CE, Kalan L, Morar M, Sung WW, et al. 2011. Antibiotic resistance is ancient. Nature 477:457-61
26. DCosta VM, McGrannKM, Hughes DW, Wright GD. 2006. Sampling the antibiotic resistome. Science 311:374-77
27. Desmarais TR, Solo-Gabriele HM, Palmer CJ. 2002. Influence of soil on fecal indicator organisms in a tidally influenced subtropical environment. Appl. Environ. Microbiol. 68:1165-72
28. Devriese LA, Ieven M, Goossens H, Vandamme P, Pot B, et al. 1996. Presence of vancomycin-resistant enterococci in farm and pet animals. Antimicrob. Agents Chemother. 40:2285-87
29. Drummond AJ, Suchard MA, Xie D, Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29:1969-73
30. Dunny GM. 1990. Genetic functions and cell-cell interactions in the pheromone-inducible plasmid transfer system of Enterococcus faecalis. Mol. Microbiol. 4:689-96
31. Dunny GM, Leonard BA, Hedberg PJ. 1995. Pheromone-inducible conjugation in Enterococcus faecalis: interbacterial and host-parasite chemical communication. J. Bacteriol. 177:871-76
32. Edwards EJ, Osborne CP, Stromberg CA, Smith SA, BondWJ, et al. 2010. The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328:587-91
33. Fisher K, Phillips C. 2009. The ecology, epidemiology and virulence of Enterococcus. Microbiology 155:1749-57
34. Foucault ML, Courvalin P, Grillot-Courvalin C. 2009. Fitness cost of VanA-type vancomycin resistance in methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 53:2354-59
35. Frieden TR, Munsiff SS, Low DE, Willey BM, Williams G, et al. 1993. Emergence of vancomycinresistant enterococci in New York City. Lancet 342:76-79
36. Garsin DA, Sifri CD, Mylonakis E, Qin X, Singh KV, et al. 2001. A simple model host for identifying gram-positive virulence factors. Proc. Natl. Acad. Sci. USA 98:10892-97
37. Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, et al. 2006. Metagenomic analysis of the human distal gut microbiome. Science 312:1355-59
38. Gilmore MS. 2002. The molecular basis of antibiotic resistance: where Newton meets Darwin. Int. J. Med. Microbiol. 292:65
39. GilmoreMS, Lebreton F, van Schaik W. 2013. Genomic transition of enterococci from gut commensals to leading causes of multidrug-resistant hospital infection in the antibiotic era. Curr. Opin. Microbiol. 16:10-16
40. Giraffa G. 2003. Functionality of enterococci in dairy products. Int. J. Food Microbiol. 88:215-22
41. Greenfield TJ, Ehli E, Kirshenmann T, Franch T, Gerdes K, Weaver KE. 2000. The antisense RNA of the par locus of pAD1regulates the expression of a 33-amino-acid toxic peptide by an unusual mechanism. Mol. Microbiol. 37:652-60
42. Hancock LE, GilmoreMS. 2002. The capsular polysaccharide of Enterococcus faecalis and its relationship to other polysaccharides in the cell wall. Proc. Natl. Acad. Sci. USA 99:1574-79
43. Hartke A, Giard JC, Laplace JM, Auffray Y. 1998. Survival of Enterococcus faecalis in an oligotrophic microcosm: changes in morphology, development of general stress resistance, and analysis of protein synthesis. Appl. Environ. Microbiol. 64:4238-45
44. Hartke A, Lemarinier S, Pichereau V, Auffray Y. 2002. Survival of Enterococcus faecalis in seawater microcosms is limited in the presence of bacterivorous zooflagellates. Curr. Microbiol. 44:329-35
45. Ike Y, Clewell DB. 1984. Genetic analysis of the pAD1 pheromone response in Streptococcus faecalis, using transposon Tn917 as an insertional mutagen. J. Bacteriol. 158:777-83
46. Ike Y, Hashimoto H, Clewell DB. 1984. Hemolysin of Streptococcus faecalis subspecies zymogenes contributes to virulence in mice. Infect. Immun. 45:528-30
47. Ike Y, Hashimoto H, Clewell DB. 1987. High incidence of hemolysin production by Enterococcus (Streptococcus) faecalis strains associated with human parenteral infections. J. Clin. Microbiol. 25:1524-28
48. Inst. Med. 2010. Antibiotic Resistance: Implications for Global Health and Novel Intervention Strategies: Workshop Summary. Washington, DC: Natl. Acad.
49. Jett BD, Huycke MM, Gilmore MS. 1994. Virulence of enterococci. Clin. Microbiol. Rev. 7:462-78
50. Jett BD, Jensen HG, Nordquist RE, Gilmore MS. 1992. Contribution of the pAD1-encoded cytolysin to the severity of experimental Enterococcus faecalis endophthalmitis. Infect. Immun. 60:2445-52
51. Jt. Expert Advis. Comm. Antibiot. Resist. ( JETACAR). 1999. The Use of Antibiotics in Food-Producing Animals: Antibiotic-Resistant Bacteria in Animals and Humans. Canberra, Aust.: Commonw. Aust.
52. Kaplan H, Hill K, Lancaster J, Hurtado AM. 2000. A theory of human life history evolution: diet, intelligence, and longevity. Evol. Anthropol. 9:156-85
53. Kempf I, HellardG, Perrin-Guyomard A, Gicquel-BruneauM, Sanders P, Leclercq R. 2008. Prevalence of high-level vancomycin-resistant enterococci in French broilers and pigs. Int. J. Antimicrob. Agents 32:463-64
54. KimEB, MarcoML. 2014. Nonclinical and clinical Enterococcus faecium strains, but not Enterococcus faecalis strains, have distinct structural and functional genomic features. Appl. Environ. Microbiol. 80:154-65
55. Kos VN, Desjardins CA, Griggs A, Cerqueira G, van Tonder A, et al. 2012. Comparative genomics of vancomycin-resistant Staphylococcus aureus strains and their positions within the clade most commonly associated with methicillin-resistant S. aureus hospital-acquired infection in the United States. mBio 3:e00112
56. Kreft B, Marre R, Schramm U, Wirth R. 1992. Aggregation substance of Enterococcus faecalis mediates adhesion to cultured renal tubular cells. Infect. Immun. 60:25-30
57. Kubinak JL, Potts WK. 2013. Host resistance influences patterns of experimental viral adaptation and virulence evolution. Virulence 4:410-18
58. Lawley TD, Walker AW. 2013. Intestinal colonization resistance. Immunology 138:1-11
59. Leavis H, TopJ, Shankar N, Borgen K, Bonten M,et al. 2004.Anovel putative enterococcal pathogenicity island linked to the esp virulence gene of Enterococcus faecium and associated with epidemicity. J. Bacteriol. 186:672-82
60. Leavis HL, Bonten MJ, Willems RJ. 2006. Identification of high-risk enterococcal clonal complexes: global dispersion and antibiotic resistance. Curr. Opin. Microbiol. 9:454-60
61. Lebreton F, van Schaik W, McGuire AM, Godfrey P, Griggs A, et al. 2013. Emergence of epidemic multidrug-resistant Enterococcus faecium from animal and commensal strains. mBio 4:e00534
62. Leclercq R, Derlot E, Duval J, Courvalin P. 1988. Plasmid-mediated resistance to vancomycin and teicoplanin in Enterococcus faecium. N. Engl. J. Med. 319:157-61
63. Levy SB. 2002. The Antibiotic Paradox: How the Misuse of Antibiotics Destroys Their Curative Power. Cambridge, MA: Perseus
64. Levy SB, Marshall B. 2004. Antibacterial resistance worldwide: causes, challenges and responses. Nat. Med. 10:S122-29
65. Ludwig W, Seewaldt E, Kilpper-Balz R, SchleiferKH, Magrum L, et al. 1985. The phylogenetic position of Streptococcus and Enterococcus. J. Gen. Microbiol. 131:543-51
66. MacCallumWG, Hastings TW. 1899. A case of acute endocarditis caused by Micrococcus zymogenes (Nov. spec.), with a description of the microorganism. J. Exp. Med. 4:521-34
67. Makinen PL, Clewell DB, An F, Makinen KK. 1989. Purification and substrate specificity of a strongly hydrophobic extracellular metalloendopeptidase ("gelatinase") from Streptococcus faecalis (strain 0G1-10). J. Biol. Chem. 264:3325-34
68. Manson JM, Hancock LE, Gilmore MS. 2010. Mechanism of chromosomal transfer of Enterococcus faecalis pathogenicity island, capsule, antimicrobial resistance, and other traits. Proc. Natl. Acad. Sci. USA 107:12269-74
69. Manson JM, Rauch M, Gilmore MS. 2008. The commensal microbiology of the gastrointestinal tract. Adv. Exp. Med. Biol. 635:15-28
70. Maraccini PA, Ferguson DM, Boehm AB. 2012. Diurnal variation in Enterococcus species composition in polluted ocean water and a potential role for the enterococcal carotenoid in protection against photoinactivation. Appl. Environ. Microbiol. 78:305-10
71. Martin JD, Mundt JO. 1972. Enterococci in insects. Appl. Microbiol. 24:575-80
72. Mason KL, Stepien TA, Blum JE, Holt JF, Labbe NH, et al. 2011. From commensal to pathogen: translocation of Enterococcus faecalis from the midgut to the hemocoel of Manduca sexta. mBio 2:e00065- 11
73. Mayr E. 1947. Ecological factors in speciation. Evolution 1:263-88
74. McBride SM, Fischetti VA, Leblanc DJ, Moellering RC Jr, GilmoreMS. 2007. Genetic diversity among Enterococcus faecalis. PLoS ONE 2:e582
75. McGavinMH, Krajewska-Pietrasik D, Ryden C, Höok M. 1993. Identification of a Staphylococcus aureus extracellular matrix-binding protein with broad specificity. Infect. Immun. 61:2479-85
76. Michaux C, Martini C, Shioya K, Ahmed Lecheheb S, Budin-Verneuil A, et al. 2012. CspR, a cold shock RNA-binding protein involved in the long-term survival and the virulence of Enterococcus faecalis. J. Bacteriol. 194:6900-8
77. Mundt JO. 1963. Occurrence of enterococci in animals in a wild environment. Appl.Microbiol. 11:136-40
78. Mundt JO. 1963. Occurrence of enterococci on plants in a wild environment. Appl.Microbiol. 11:141-44
79. Mundy LM, Sahm DF, GilmoreM. 2000. Relationships between enterococcal virulence and antimicrobial resistance. Clin. Microbiol. Rev. 13:513-22
80. Murray BE. 1990. The life and times of the enterococcus. Clin. Microbiol. Rev. 3:46-65
81. Murray BE. 1998. Diversity among multidrug-resistant enterococci. Emerg. Infect. Dis. 4:37-47
82. Nallapareddy SR, Qin X, Weinstock GM, Hook M, Murray BE. 2000. Enterococcus faecalis adhesin, Ace, mediates attachment to extracellular matrix proteins collagen type IV and laminin as well as collagen type I. Infect. Immun. 68:5218-24
83. Nallapareddy SR, Singh KV, Duh RW, Weinstock GM, Murray BE. 2000. Diversity of ace, a gene encoding amicrobial surface component recognizing adhesivematrixmolecules, from different strains of Enterococcus faecalis and evidence for production of Ace during human infections. Infect. Immun. 68:5210-7
84. Niven CF, Sherman JM. 1944. Nutrition of the enterococci. J. Bacteriol. 47:335-42
85. Noble CJ. 1978. Carriage of group D streptococci in the human bowel. J. Clin. Pathol. 31:1182-86
86. Olmsted SB, Dunny GM, Erlandsen SL, Wells CL. 1994. A plasmid-encoded surface protein on Enterococcus faecalis augments its internalization by cultured intestinal epithelial cells. J. Infect. Dis. 170:1549-56
87. Palmer KL, Gilmore MS. 2010. Multidrug-resistant enterococci lack CRISPR-cas. mBio 1:e00227-10
88. Palmer KL, Godfrey P, Griggs A, Kos VN, Zucker J, et al. 2012. Comparative genomics of enterococci: variation in Enterococcus faecalis, clade structure in E. faecium, and defining characteristics of E. gallinarum and E. casseliflavus. mBio 3:e00318-11
89. Palmer KL, Kos VN, Gilmore MS. 2010. Horizontal gene transfer and the genomics of enterococcal antibiotic resistance. Curr. Opin. Microbiol. 13:632-39
90. Parte AC. 2014. LPSN-list of prokaryotic names with standing in nomenclature. Nucleic Acids Res. 42:D613-16
91. Paulsen IT, Banerjei L, Myers GS, Nelson KE, Seshadri R, et al. 2003. Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299:2071-74
92. Pinkston KL, Gao P, Diaz-Garcia D, Sillanpää J, Nallapareddy SR, et al. 2011. The Fsr quorum-sensing system of Enterococcus faecalis modulates surface display of the collagen-bindingMSCRAMMAce through regulation of gelE. J. Bacteriol. 193:4317-25
93. Purnell SE, Ebdon JE, Taylor HD. 2011. Bacteriophage lysis of Enterococcus host strains: a tool for microbial source tracking? Environ. Sci. Technol. 45:10699-705
94. Rana NF, Sauvageot N, Laplace JM, Bao Y, Nes I, et al. 2013. Redox balance via lactate dehydrogenase is important for multiple stress resistance and virulence in Enterococcus faecalis. Infect. Immun. 81:2662-68
95. RenduW, Beauval C, Crevecoeur I, Bayle P, Balzeau A, et al. 2013. Evidence supporting an intentional Neandertal burial at La Chapelle-aux-Saints. Proc. Natl. Acad. Sci. USA 111:81-86
96. Rich RL, Kreikemeyer B, Owens RT, LaBrenz S, Narayana SV, et al. 1999. Ace is a collagen-binding MSCRAMM from Enterococcus faecalis. J. Biol. Chem. 274:26939-45
97. Rigottier-Gois L, Alberti A, Houel A, Taly JF, Palcy P, et al. 2011. Large-scale screening of a targeted Enterococcus faecalis mutant library identifies envelope fitness factors. PLoS ONE 6:e29023
98. Rippere K, Patel R, Uhl JR, Piper KE, Steckelberg JM, et al. 1998. DNA sequence resembling vanA and vanB in the vancomycin-resistant biopesticide Bacillus popilliae. J. Infect. Dis. 178:584-88
99. Roux A, Payne SM, Gilmore MS. 2009. Microbial telesensing: probing the environment for friends, foes, and food. Cell Host Microbe 6:115-24
100. Ruiz-Garbajosa P, BontenMJ, Robinson DA, Top J, Nallapareddy SR, et al. 2006. Multilocus sequence typing scheme for Enterococcus faecalis reveals hospital-adapted genetic complexes in a background of high rates of recombination. J. Clin. Microbiol. 44:2220-28
101. Sahm DF, Kissinger J, Gilmore MS, Murray PR, Mulder R, et al. 1989. In vitro susceptibility studies of vancomycin-resistant Enterococcus faecalis. Antimicrob. Agents Chemother. 33:1588-91
102. Schleifer KH, Kilpper-Balz R. 1984. Transfer of Streptococcus faecalis and Streptococcus faecium to the genus Enterococcus nom. rev. as Enterococcus faecalis comb. nov. and Enterococcus faecium comb. nov. Int. J. Syst. Bacteriol. 34:31-34
103. Seipke RF, KaltenpothM, Hutchings MI. 2012. Streptomyces as symbionts: an emerging and widespread theme? FEMS Microbiol. Rev. 36:862-76
104. Shankar N, Baghdayan AS, Gilmore MS. 2002. Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis. Nature 417:746-50
105. Shankar V, Baghdayan AS, Huycke MM, Lindahl G, Gilmore MS. 1999. Infection-derived Enterococcus faecalis strains are enriched in esp, a gene encoding a novel surface protein. Infect. Immun. 67:193-200
106. Sherman JM. 1937. The streptococci. Bacteriol. Rev. 1:3-97
107. Sherman JM. 1938. The enterococci and related streptococci. J. Bacteriol. 35:81-93
108. Silverman J, Thal LA, Perri MB, Bostic G, ZervosMJ. 1998. Epidemiologic evaluation of antimicrobial resistance in community-acquired enterococci. J. Clin. Microbiol. 36:830-32
109. Singh KV, Nallapareddy SR, Sillanpää J, Murray BE. 2010. Importance of the collagen adhesin Ace in pathogenesis and protection against Enterococcus faecalis experimental endocarditis. PLoS Pathog. 6:e1000716
110. Sinton LW, Braithwaite RR, Hall CH, Mackenzie ML. 2007. Survival of indicator and pathogenic bacteria in bovine feces on pasture. Appl. Environ. Microbiol. 73:7917-25
111. Sinton LW, Hall CH, Lynch PA, Davies-Colley RJ. 2002. Sunlight inactivation of fecal indicator bacteria and bacteriophages from waste stabilization pond effluent in fresh and saline waters. Appl. Environ. Microbiol. 68:1122-31
112. Solheim M, Brekke MC,Snipen LG, Willems RJ, Nes IF, Brede DA. 2011. Comparative genomic analysis reveals significant enrichment of mobile genetic elements and genes encoding surface structure-proteins in hospital-associated clonal complex 2 Enterococcus faecalis. BMC Microbiol. 11:3
113. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-90
114. Sussmuth SD, Muscholl-Silberhorn A, Wirth R, Susa M, Marre R, Rozdzinski E. 2000. Aggregation substance promotes adherence, phagocytosis, and intracellular survival of Enterococcus faecalis within human macrophages and suppresses respiratory burst. Infect. Immun. 68:4900-6
115. Tang W, van der Donk WA. 2013. The sequence of the enterococcal cytolysin imparts unusual lanthionine stereochemistry. Nat. Chem. Biol. 9:157-59
116. Thal LA, Chow JW, Mahayni R, Bonilla H, Perri MB, et al. 1995. Characterization of antimicrobial resistance in enterococci of animal origin. Antimicrob. Agents Chemother. 39:2112-15
117. Thiercelin ME. 1899. Sur un diplocoque saprophyte de lintestin susceptible de devenir pathogen. C. R. Soc. Biol. 5:269-71
118. Thrall PH, Burdon JJ. 2003. Evolution of virulence in a plant host-pathogen metapopulation. Science 299:1735-37
119. Todd EW. 1934. A comparative serological study of streptolysins derived from human and from animal infections, with notes on pneumococcal hemolysin, tetanolysin, and staphylococcus toxin. J. Pathol. Bacteriol. 39:299-321
120. Toledo-Arana A, Valle J, Solano C, Arrizubieta MJ, Cucarella C, et al. 2001. The enterococcal surface protein, Esp, is involved in Enterococcus faecalis biofilm formation. Appl. Environ. Microbiol. 67:4538-45
121. Tung H, Guss B, Hellman U, Persson L, Rubin K, Ryden C. 2000. A bone sialoprotein-binding protein from Staphylococcus aureus: a member of the staphylococcal Sdr family. Biochem. J. 345(Part 3):611-19
122. Uttley AH, Collins CH, Naidoo J, George RC. 1988. Vancomycin-resistant enterococci. Lancet 331:57-58
123. Van Tyne D, MartinMJ, GilmoreMS. 2013. Structure, function, and biology of the Enterococcus faecalis cytolysin. Toxins 5:895-911
124. Vollaard EJ, Clasener HA. 1994. Colonization resistance. Antimicrob. Agents Chemother. 38:409-14
125. Wegener HC. 1998. Historical yearly usage of glycopeptides for animals and humans: the American- European paradox revisited. Antimicrob. Agents Chemother. 42:3049
126. Weigel LM, Clewell DB, Gill SR, Clark NC, McDougal LK, et al. 2003. Genetic analysis of a high-level vancomycin-resistant isolate of Staphylococcus aureus. Science 302:1569-71
127. Wells CL, Moore EA, Hoag JA, Hirt H, Dunny GM, Erlandsen SL. 2000. Inducible expression of Enterococcus faecalis aggregation substance surface protein facilitates bacterial internalization by cultured enterocytes. Infect. Immun. 68:7190-94
128. Welton LA, Thal LA, Perri MB, Donabedian S, McMahon J, et al. 1998. Antimicrobial resistance in enterococci isolated from Turkey flocks fed virginiamycin. Antimicrob. Agents Chemother. 42:705-8
129. Werner G, Coque TM, Hammerum AM, Hope R, Hryniewicz W, et al. 2008. Emergence and spread of vancomycin resistance among enterococci in Europe. Euro. Surveill. 13:19046
130. WhitmanWB, Coleman DC, WiebeWJ. 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. USA 95:6578-83
131. Willems RJ, Homan W, Top J, van Santen-Verheuvel M, Tribe D, et al. 2001. Variant esp gene as a marker of a distinct genetic lineage of vancomycin-resistant Enterococcus faecium spreading in hospitals. Lancet 357:853-55
132. Willey JM, van der Donk WA. 2007. Lantibiotics: peptides of diverse structure and function. Annu. Rev. Microbiol. 61:477-501
133. Williamson R, al-Obeid S, Shlaes JH, Goldstein FW, Shlaes DM. 1989. Inducible resistance to vancomycin in Enterococcus faecium D366. J. Infect. Dis. 159:1095-104
134. Yamahara KM, Walters SP, Boehm AB. 2009. Growth of enterococci in unaltered, unseeded beach sands subjected to tidal wetting. Appl. Environ. Microbiol. 75:1517-24
135. Zhang X, Top J, de Been M, Bierschenk D, Rogers M, et al. 2013. Identification of a genetic determinant in clinical Enterococcus faecium strains that contributes to intestinal colonization during antibiotic treatment. J. Infect. Dis. 207:1780-86