Horizontal gene transfer in the human gastrointestinal tract: Potential spread of antibiotic resistance genes

Infection and Drug Resistance

Volumn 7, Issue , 2014, Pages 167-176

  Huddleston, Jennifer R ^a  

^a ABILENE CHRISTIAN UNIVERSITY   (United States)

Author keywords

Conjugation; Gut microbiome; Natural transformation; Transduction

Indexed keywords

AMINOGLYCOSIDE; AMPICILLIN; ANTIBIOTIC AGENT; BACITRACIN; BETA LACTAM; CARBAPENEM DERIVATIVE; CEPHALOSPORIN DERIVATIVE; CHLORAMPHENICOL; CIPROFLOXACIN; COLISTIN; DALFOPRISTIN; ERTAPENEM; ERYTHROMYCIN; LINCOSAMIDE; MACROLIDE; METRONIDAZOLE; MONOBACTAM DERIVATIVE; NALIDIXIC ACID; NORFLOXACIN; OXAZOLIDINONE DERIVATIVE; PENICILLIN G; PLEUROMUTILIN; QUINOLONE DERIVATIVE; SULFONAMIDE; TETRACYCLINE DERIVATIVE; VANCOMYCIN;

ACINETOBACTER; ACINETOBACTER BAYLYI; ACINETOBACTER OLEIVORANS; AEROMONAS SALMONICIDA; ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTANCE GENE; B12E CFXA GENE; BACA GENE; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIUM; BACTERIUM CONJUGATION; BACTERIUM TRANSDUCTION; BACTERIUM TRANSFORMATION; BURKHOLDERIA THAILANDENSIS; CAMPYLOBACTER JEJUNI; DNA REPAIR; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ERMB GENE; ESCHERICHIA COLI; GALLIBACTERIUM ANATIS; GENE; HAEMOPHILUS INFLUENZAE; HORIZONTAL GENE TRANSFER; HUMAN; INFECTION RESISTANCE; INTESTINE FLORA; LARGE INTESTINE; LEGIONELLA PNEUMOPHILA; MOLECULAR EVOLUTION; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; NONHUMAN; PSEUDOMONAS AERUGINOSA; REVIEW; SALMONELLA; SALMONELLA TYPHIMURIUM; SERRATIA LIQUEFACIENS; STREPTOCOCCUS PNEUMONIAE; STREPTOCOCCUS PYOGENES; STREPTOCOCCUS UBERIS; UPPP GENE; VANA GENE; VANRG GENE;

EID: 84903167988     PISSN: 11786973     EISSN: None     Source Type: Journal    
DOI: 10.2147/IDR.S48820     Document Type: Review

References (108)

1. Levy SB, Marshall B. Antibacterial resistance worldwide: causes, challenges and responses. Nat Med. 2004;10(Suppl 12):S122-S129.
2. de Kraker MEA, Davey PG, Grundmann H; BURDEN study group. Mortality and hospital stay associated with resistant Staphylococcus aureus and Escherichia coli bacteremia: estimating the burden of antibiotic resistance in Europe. PLoS Med. 2011;8(10):e1001104.
3. Armstrong GL, Conn LA, Pinner RW. Trends in infectious disease mortality in the United States during the 20th century. JAMA. 1999; 281(1):61-66.
4. Spellberg B, Powers JH, Brass EP, Miller LG, Edwards JE Jr. Trends in antimicrobial drug development: Implications for the future. Clin Infect Dis. 2004;38(9):1279-1286.
5. Arutyunov D, Frost LS. F conjugation: back to the beginning. Plasmid. 2013;70(1):18-32.
6. Smillie C, Garcillán-Barcia MP, Francia MV, Rocha EPC, de la Cruz F. Mobility of plasmids. Microbiol Mol Biol Rev MMBR. 2010;74(3): 434-452.
7. Zechner EL, Lang S, Schildbach JF. Assembly and mechanisms of bacterial type IV secretion machines. Philos Trans R Soc B Biol Sci. 2012;367(1592):1073-1087.
8. Bacon DJ, Alm RA, Burr DH, et al. Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect Immun. 2000;68(8):4384-4390.
9. Waldor MK, Tschape H, Mekalanos JJ. A new type of conjugative transposon encodes resistance to sulfamethoxazole, trimethoprim, and streptomycin in Vibrio cholerae O139. J Bacteriol. 1996;178(14): 4157-4165.
10. Zechner EL, de la Cruz F, Eisenbrandt R, et al. Conjugative-DNA transfer processes. In: Thomas CM, ed. Horizontal Gene Pool: Bacterial Plasmids and Gene Spread. CRC Press; 2003:87-174.
11. Guglielmini J, de la Cruz F, Rocha EP. Evolution of conjugation and type IV secretion systems. Mol Biol Evol. 2013;30(2):315-331.
12. Salyers AA, Shoemaker NB, Stevens AM, Li LY. Conjugative transposons: an unusual and diverse set of integrated gene transfer elements. Microbiol Rev. 1995;59(4):579-590.
13. Walsh TR. Combinatorial genetic evolution of multiresistance. Curr Opin Microbiol. 2006;9(5):476-482.
14. Hall RM. Integrons and gene cassettes: hotspots of diversity in bacterial genomes: Hall. Ann N Y Acad Sci. 2012;1267(1):71-78.
15. Beaber JW, Hochhut B, Waldor MK. Genomic and functional analyses of SXT, an integrating antibiotic resistance gene transfer element derived from Vibrio cholerae. J Bacteriol. 2002;184(15): 4259-4269.
16. Davies J, Davies D. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev MMBR. 2010;74(3):417-433.
17. Norman A, Hansen LH, Sorensen SJ. Conjugative plasmids: vessels of the communal gene pool. Philos Trans R Soc B Biol Sci. 2009; 364(1527):2275-2289.
18. Lorenz MG, Wackernagel W. Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev. 1994;58(3): 563-602.
19. Johnston C, Martin B, Fichant G, Polard P, Claverys J-P. Bacterial transformation: distribution, shared mechanisms and divergent control. Nat Rev Microbiol. 2014;12(3):181-196.
20. Johnsborg O, Eldholm V, Håvarstein LS. Natural genetic transformation: prevalence, mechanisms and function. Res Microbiol. 2007;158(10):767-778.
21. Sparling PF. Genetic transformation of Neisseria gonorrhoeae to streptomycin resistance. J Bacteriol. 1966;92(5):1364-1371.
22. Finkel SE, Kolter R. DNA as a nutrient: Novel role for bacterial competence gene homologs. J Bacteriol. 2001;183(21):6288-6293.
23. Redfield RJ. Genes for breakfast: the have-your-cake-and-eat-it-too of bacterial transformation. J Hered. 1993;84(5):400-404.
24. Kristensen BM, Sinha S, Boyce JD, Bojesen AM, Mell JC, Redfield RJ. Natural transformation of Gallibacterium anatis. Appl Environ Microbiol. 2012;78(14):4914-4922.
25. Chandler MS. The gene encoding cAMP receptor protein is required for competence development in Haemophilus influenzae Rd. Proc Natl Acad Sci U S A. 1992;89(5):1626-1630.
26. Huddleston JR, Brokaw JM, Zak JC, Jeter RM. Natural transformation as a mechanism of horizontal gene transfer among environmental Aeromonas species. Syst Appl Microbiol. 2013;36(4): 224-234.
27. Sinha S, Mell J, Redfield R. The availability of purine nucleotides regulates natural competence by controlling translation of the competence activator Sxy. Mol Microbiol. 2013;88(6):1106-1119.
28. Michod RE, Wojciechowski MF, Hoelzer MA. DNA repair and the evolution of transformation in the bacterium Bacillus subtilis. Genetics. 1988;118(1):31-39.
29. Prudhomme M, Attaiech L, Sanchez G, Martin B, Claverys J-P. Antibiotic stress induces genetic transformability in the human pathogen Streptococcus pneumoniae. Science. 2006;313(5783):89-92.
30. Vos M. Why do bacteria engage in homologous recombination? Trends Microbiol. 2009;17(6):226-232.
31. Bacher JM, Metzgar D, Crécy-Lagard V de. Rapid evolution of diminished transformability in Acinetobacter baylyi. J Bacteriol. 2006;188(24):8534-8542.
32. Engelstädter J, Moradigaravand D. Adaptation through genetic time travel? Fluctuating selection can drive the evolution of bacterial transformation. Proc Biol Sci. 2014;281(1775):20132609.
33. Johnsen PJ, Dubnau D, Levin BR. Episodic selection and the maintenance of competence and natural transformation in Bacillus subtilis. Genetics. 2009;181(4):1521-1533.
34. Haijema BJ, Hahn J, Haynes J, Dubnau D. A ComGA-dependent checkpoint limits growth during the escape from competence. Mol Microbiol. 2001;40(1):52-64.
35. Bigger J. Treatment of staphylococcal infections with penicillin by intermittent sterilisation I. The Lancet. 1944;244(6320):497-500.
36. Lewis K. Persister cells, dormancy and infectious disease. Nat Rev Microbiol. 2007;5(1):48-56.
37. Bakkali M. Could DNA uptake be a side effect of bacterial adhesion and twitching motility? Arch Microbiol. 2013;195(4):279-289.
38. Averhoff B. DNA transport and natural transformation in mesophilic and thermophilic bacteria. J Bioenerg Biomembr. 2004;36(1): 25-33.
39. Chen I, Dubnau D. DNA transport during transformation. Front Biosci J Virtual Libr. 2003;8:s544-s556.
40. Beiko RG, Harlow TJ, Ragan MA. Highways of gene sharing in prokaryotes. Proc Natl Acad Sci U S A. 2005;102(40):14332-14337.
41. Fortier L-C, Sekulovic O. Importance of prophages to evolution and virulence of bacterial pathogens. Virulence. 2013;4(5):354-365.
42. Muniesa M, Colomer-Lluch M, Jofre J. Could bacteriophages transfer antibiotic resistance genes from environmental bacteria to human-body associated bacterial populations? Mob Genet Elem. 2013;3(4): e25847.
43. Schmieger H, Schicklmaier P. Transduction of multiple drug resistance of Salmonella enterica serovar typhimurium DT104. FEMS Microbiol Lett. 1999;170(1):251-256.
44. Mann BA, Slauch JM. Transduction of low-copy number plasmids by bacteriophage P22. Genetics. 1997;146(2):447-456.
45. Dinsdale EA, Edwards RA, Hall D, et al. Functional metagenomic profiling of nine biomes. Nature. 2008;452(7187):629-632.
46. Mazaheri Nezhad Fard R, Barton MD, Heuzenroeder MW. Bacteriophage-mediated transduction of antibiotic resistance in enterococci: Transduction in Enterococcus spp. Lett Appl Microbiol. 2011;52(6):559-564.
47. Whitman WB, Coleman DC, Wiebe WJ. Prokaryotes: The unseen majority. Proc Natl Acad Sci U S A. 1998;95(12):6578-6583.
48. Eckburg PB, Bik EM, Bernstein CN, et al. Diversity of the human intestinal microbial flora. Science. 2005;308(5728):1635-1638.
49. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124(4): 837-848.
50. Sørensen SJ, Bailey M, Hansen LH, Kroer N, Wuertz S. Studying plasmid horizontal transfer in situ: a critical review. Nat Rev Microbiol. 2005;3(9):700-710.
51. Licht TR, Christensen BB, Krogfelt KA, Molin S. Plasmid transfer in the animal intestine and other dynamic bacterial populations: the role of community structure and environment. Microbiology. 1999;145(9):2615-2622.
52. Krogfelt KA, Poulsen LK, Molin S. Identification of coccoid Escherichia coli BJ4 cells in the large intestine of streptomycin-treated mice. Infect Immun. 1993;61(12):5029-5034.
53. Poulsen LK, Lan F, Kristensen CS, Hobolth P, Molin S, Krogfelt KA. Spatial distribution of Escherichia coli in the mouse large intestine inferred from rRNA in situ hybridization. Infect Immun. 1994;62(11): 5191-5194.
54. Marks LR, Mashburn-Warren L, Federle MJ, Hakansson AP. Streptococcus pyogenes biofilm growth in vitro and in vivo and its role in colonization, virulence and genetic exchange. J Infect Dis. 2014: Epub January 23, 2014.
55. Mills S, Shanahan F, Stanton C, Hill C, Coffey A, Ross RP. Movers and shakers. Gut Microbes. 2013;4(1):4-16.
56. Anwar H, Dasgupta MK, Costerton JW. Testing the susceptibility of bacteria in biofilms to antibacterial agents. Antimicrob Agents Chemother. 1990;34(11):2043-2046.
57. Salyers AA, Gupta A, Wang Y. Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol. 2004;12(9): 412-416.
58. Liu B, Pop M. ARDB-Antibiotic Resistance Genes Database. Nucleic Acids Res. 2009;37(suppl 1):D443-D447.
59. Ghosh TS, Gupta SS, Nair GB, Mande SS. In silico analysis of antibiotic resistance genes in the gut microflora of individuals from diverse geographies and age-groups. PLoS ONE. 2013;8(12):e83823.
60. Sommer MOA, Dantas G, Church GM. Functional characterization of the antibiotic resistance reservoir in the human microflora. Science. 2009;325(5944):1128-1131.
61. Hu Y, Yang X, Qin J, et al. Metagenome-wide analysis of antibiotic resistance genes in a large cohort of human gut microbiota. Nat Commun. 2013;4:2151.
62. Forslund K, Sunagawa S, Kultima JR, et al. Country-specific antibiotic use practices impact the human gut resistome. Genome Res. 2013;23(7): 1163-1169.
63. Marshall BM, Levy SB. Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev. 2011;24(4):718-733.
64. Schjorring, Susanne, Krogfelt KA. Assessment of bacterial antibiotic resistance transfer in the gut. Int J Microbiol. 2011;2011:1-10.
65. Carr FJ, Chill D, Maida N. The lactic acid bacteria: A literature survey. Crit Rev Microbiol. 2002;28(4):281.
66. Ammor MS, Flórez AB, Mayo B. Antibiotic resistance in non-enterococcal lactic acid bacteria and bifidobacteria. Food Microbiol. 2007;24(6):559-570.
67. Perreten V, Schwarz F, Cresta L, Boeglin M, Dasen G, Teuber M. Antibiotic resistance spread in food. Nature. 1997;389(6653):801-802.
68. Egervärn M, Lindmark H, Olsson J, Roos S. Transferability of a tetracycline resistance gene from probiotic Lactobacillus reuteri to bacteria in the gastrointestinal tract of humans. Antonie Van Leeuwenhoek. 2010;97(2):189-200.
69. Drago L, Rodighiero V, Mattina R, Toscano M, DE Vecchi E. In vitro selection and transferability of antibiotic resistance in the probiotic strain Lactobacillus reuteri DSM 17938. J Chemother Florence Italy. 2011;23(6):371-373.
70. Lester CH, Frimodt-Møller N, Sørensen TL, Monnet DL, Hammerum AM. In vivo transfer of the vanA resistance gene from an Enterococcus faecium isolate of animal origin to an E. faecium isolate of human origin in the intestines of human volunteers. Antimicrob Agents Chemother. 2006;50(2):596-599.
71. Trobos M, Lester CH, Olsen JE, Frimodt-Møller N, Hammerum AM. Natural transfer of sulphonamide and ampicillin resistance between Escherichia coli residing in the human intestine. J Antimicrob Chemother. 2009;63(1):80-86.
72. OXA-48gene in the gut flora. J Antimicrob Chemother. 2012;67(4):1041-1043.
73. Karami N, Martner A, Enne VI, Swerkersson S, Adlerberth I, Wold AE. Transfer of an ampicillin resistance gene between two Escherichia coli strains in the bowel microbiota of an infant treated with antibiotics. J Antimicrob Chemother. 2007;60(5):1142-1145.
74. Goren MG, Carmeli Y, Schwaber MJ, Chmelnitsky I, Schechner V, Navon-Venezia S. Transfer of carbapenem-resistant plasmid from Klebsiella pneumoniae ST258 to Escherichia coli in patient. Emerg Infect Dis. 2010;16(6):1014-1017.
75. Duval-Iflah Y, Raibaud P, Tancrede C, Rousseau M. R-plasmic transfer from Serratia liquefaciens to Escherichia coli in vitro and in vivo in the digestive tract of gnotobiotic mice associated with human fecal flora. Infect Immun. 1980;28(3):981-990.
76. Sparo M, Urbizu L, Solana MV, et al. High-level resistance to gentamicin: genetic transfer between Enterococcus faecalis isolated from food of animal origin and human microbiota. Lett Appl Microbiol. 2012;54(2):119-125.
77. Lester CH, Frimodt-Moller N, Hammerum AM. Conjugal transfer of aminoglycoside and macrolide resistance between Enterococcus faecium isolates in the intestine of streptomycin-treated mice. FEMS Microbiol Lett. 2004;235(2):385-391.
78. Carattoli A. Resistance plasmid families in Enterobacteriaceae. Antimicrob Agents Chemother. 2009;53(6):2227-2238.
79. Khajuria A, Praharaj AK, Kumar M, Grover N, Aggarwal A. Multidrug resistant NDM-1 metallo-beta-lactamase producing Klebsiella pneumoniae sepsis outbreak in a neonatal intensive care unit in a tertiary care center at central India. Indian J Pathol Microbiol. 2014;57(1): 65-68.
80. DHA-1, and qnrB4 genes recovered from animal isolates. Antimicrob Agents Chemother. 2014.
81. Marchaim D, Chopra T, Pogue JM, et al. Outbreak of colistin-resistant, carbapenem-resistant Klebsiella pneumoniae in Metropolitan Detroit, Michigan. Antimicrob Agents Chemother. 2011;55(2):593-599. [Epub ahead of print].
82. Long KS, Poehlsgaard J, Kehrenberg C, Schwarz S, Vester B. The Cfr rRNA methyltransferase confers resistance to phenicols, lincosamides, oxazolidinones, pleuromutilins, and streptogramin A antibiotics. Antimicrob Agents Chemother. 2006;50(7):2500-2505.
83. De Vries LE, Vallès Y, Agersø Y, et al. The gut as reservoir of antibiotic resistance: Microbial diversity of tetracycline resistance in mother and infant. PLoS ONE. 2011;6(6):e21644.
84. Shoemaker NB, Vlamakis H, Hayes K, Salyers AA. Evidence for extensive resistance gene transfer among Bacteroides spp. and among Bacteroides and other genera in the human colon. Appl Environ Microbiol. 2001;67(2):561-568.
85. Radman M. SOS repair hypothesis: phenomenology of an inducible DNA repair which is accompanied by mutagenesis. Basic Life Sci. 1975;5A:355-367.
86. Michel B. After 30 years of study, the bacterial SOS response still surprises us. PLoS Biol. 2005;3(7):e255.
87. Varhimo E, Savijoki K, Jefremoff H, Jalava J, Sukura A, Varmanen P. Ciprofloxacin induces mutagenesis to antibiotic resistance independent of UmuC in Streptococcus uberis. Environ Microbiol. 2008;10(8): 2179-2183.
88. Alonso A, Campanario E, Marti{dotless}́nez JL. Emergence of multidrug-resistant mutants is increased under antibiotic selective pressure in Pseudomonas aeruginosa. Microbiology. 1999;145(10):2857-2862.
89. Kim J, Noh J, Park W. Insight into norfloxacin resistance of Acinetobacter oleivorans DR1: target gene mutation, persister, and RNA-Seq analyses. J Microbiol Biotechnol. 2013;23(9):1293-1303.
90. Charpentier X, Kay E, Schneider D, Shuman HA. Antibiotics and UV radiation induce competence for natural transformation in Legionella pneumophila. J Bacteriol. 2011;193(5):1114-1121.
91. Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. Extracellular DNA required for bacterial biofilm formation. Science. 2002;295(5559):1487.
92. Charpentier X, Polard P, Claverys J-P. Induction of competence for genetic transformation by antibiotics: convergent evolution of stress responses in distant bacterial species lacking SOS? Curr Opin Microbiol. 2012;15(5):570-576.
93. Lemire S, Figueroa-Bossi N, Bossi L. Bacteriophage crosstalk: Coordination of prophage induction by trans-acting antirepressors. PLoS Genet. 2011;7(6):e1002149.
94. Ulrich RL, Deshazer D, Kenny TA, et al. Characterization of the Burkholderia thailandensis SOS response by using whole-transcriptome shotgun sequencing. Appl Environ Microbiol. 2013;79(19): 5830-5843.
95. Modi SR, Lee HH, Spina CS, Collins JJ. Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature. 2013;499(7457):219-222.
96. Collins SM, Denou E, Verdu EF, Bercik P. The putative role of the intestinal microbiota in the irritable bowel syndrome. Dig Liver Dis Off J Ital Soc Gastroenterol Ital Assoc Study Liver. 2009;41(12):850-853.
97. Reiff C, Kelly D. Inflammatory bowel disease, gut bacteria and probiotic therapy. Int J Med Microbiol IJMM. 2010;300(1):25-33.
98. Wagner J, Maksimovic J, Farries G, et al. Bacteriophages in gut samples from pediatric Crohn's disease patients: metagenomic analysis using 454 pyrosequencing. Inflamm Bowel Dis. 2013;19(8):1598-1608.
99. Beaber JW, Hochhut B, Waldor MK. SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature. 2004;427(6969):72-74.
100. Úbeda C, Maiques E, Knecht E, Lasa Í, Novick RP, Penadés JR. Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci: Horizontal dissemination of virulence genes. Mol Microbiol. 2005;56(3):836-844.
101. Andersson DI, Levin BR. The biological cost of antibiotic resistance. Curr Opin Microbiol. 1999;2(5):489-493.
102. Bjorkman J, Hughes D, Andersson DI. Virulence of antibiotic-resistant Salmonella typhimurium. Proc Natl Acad Sci U S A. 1998;95(7): 3949-3953.
103. Baker S, Duy PT, Nga TVT, et al. Fitness benefits in fluoroquinolone-resistant Salmonella typhi in the absence of antimicrobial pressure. eLife. 2013;2.
104. Löfmark S, Jernberg C, Billström H, Andersson DI, Edlund C. Restored fitness leads to long-term persistence of resistant Bacteroides strains in the human intestine. Anaerobe. 2008;14(3):157-160.
105. Jernberg C, Löfmark S, Edlund C, Jansson JK. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J. 2007;1(1):56-66.
106. Sjölund M, Tano E, Blaser MJ, Andersson DI, Engstrand L. Persistence of resistant Staphylococcus epidermidis after single course of clarithromycin. Emerg Infect Dis. 2005;11(9):1389-1393.
107. Sjölund M, Wreiber K, Andersson DI, Blaser MJ, Engstrand L. Long-term persistence of resistant Enterococcus species after antibiotics to eradicate Helicobacter pylori. Ann Intern Med. 2003;139(6): 483-487.
108. Jakobsson HE, Jernberg C, Andersson AF, Sjölund-Karlsson M, Jansson JK, Engstrand L. Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PloS One. 2010;5(3):e9836.