Skip to main content
SpringerLink
Log in

The Threat of Antimicrobial Resistance on the Human Microbiome

  • Human Microbiome
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Ubiquitous in nature, antimicrobial resistance (AMR) has existed long before the golden age of antimicrobials. While antimicrobial agents are beneficial to combat infection, their widespread use contributes to the increase in and emergence of novel resistant microbes in virtually all environmental niches. The human microbiome is an important reservoir of AMR with initial exposure occurring in early life. Once seeded with AMR, commensal organisms may be key contributors to the dissemination of resistance due to the interconnectedness of microbial communities. When acquired by pathogens however, AMR becomes a serious public health threat worldwide. Our ability to combat the threat of emerging resistance relies on accurate AMR detection methods and the development of therapeutics that function despite the presence of antimicrobial resistance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Antibiotic resistance threats in the United States, 2013 | Antibiotic/antimicrobial resistance | CDC. http://www.cdc.gov/drugresistance/threat-report-2013/. Accessed 31 Aug 2016

  2. Wright GD (2007) The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 5:175–186

    Article  CAS  PubMed  Google Scholar 

  3. Alexander BD, Johnson MD, Pfeiffer CD, et al (2013) Increasing echinocandin resistance in Candida glabrata: clinical failure correlates with presence of FKS mutations and elevated minimum inhibitory concentrations. Clin. Infect. Dis. 56:1724–1732

    Article  PubMed  PubMed Central  Google Scholar 

  4. Mediavilla JR, Patrawalla A, Chen L, et al (2016) Colistin- and carbapenem-resistant Escherichia coli harboring mcr-1 and bla NDM-5, causing a complicated urinary tract infection in a patient from the United States: TABLE 1. MBio 7:e01191–e01116

    Article  PubMed  PubMed Central  Google Scholar 

  5. Alareqi LMQ, Mahdy MAK, Lau Y-L, et al (2016) Molecular markers associated with resistance to commonly used antimalarial drugs among Plasmodium falciparum isolates from a malaria-endemic area in Taiz governorate—Yemen during the transmission season. Acta Trop. 162:174–179

    Article  CAS  PubMed  Google Scholar 

  6. Lima YAR, Cardoso LPV, Reis MN d G, Stefani MMA (2016) Incident and long-term HIV-1 infection among pregnant women in Brazil: transmitted drug resistance and mother-to-child transmission. J. Med. Virol. 88:1936–1943

    Article  CAS  PubMed  Google Scholar 

  7. Vale-Silva LA, Sanglard D (2015) Tipping the balance both ways: drug resistance and virulence in Candida glabrata. FEMS Yeast Res. 15:fov025

    Article  PubMed  CAS  Google Scholar 

  8. Cleveland AA, Farley MM, Harrison LH, et al (2012) Changes in incidence and antifungal drug resistance in candidemia: results from population-based laboratory surveillance in Atlanta and Baltimore, 2008-2011. Clin. Infect. Dis. 55:1352–1361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Bassett EJ, Keith MS, Armelagos GJ, et al (1980) Tetracycline-labeled human bone from ancient Sudanese Nubia (A.D. 350). Science 209:1532–1534

    Article  CAS  PubMed  Google Scholar 

  10. Santiago-Rodriguez TM, Fornaciari G, Luciani S, et al (2015) Gut microbiome of an 11th century A.D. pre-Columbian Andean mummy. PLoS One 10:e0138135

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. D’Costa VM, King CE, Kalan L, et al (2011) Antibiotic resistance is ancient. Nature 477:457–461

    Article  PubMed  CAS  Google Scholar 

  12. Bhullar K, Waglechner N, Pawlowski A, et al (2012) Antibiotic resistance is prevalent in an isolated cave microbiome. PLoS One 7:e34953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Leisner JJ, Jørgensen NOG, Middelboe M (2016) Predation and selection for antibiotic resistance in natural environments. Evol. Appl. 9:427–434

    Article  PubMed  PubMed Central  Google Scholar 

  14. Modi SR, Collins JJ, Relman DA (2014) Antibiotics and the gut microbiota. J. Clin. Invest. 124:4212–4218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Davies J, Davies D (2010) Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 74:417–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Knox R (1960) A new penicillin (BRL 1241) active against penicillin-resistant staphylococci. Br. Med. J. 2:690–693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Müller B, Borrell S, Rose G, Gagneux S (2013) The heterogeneous evolution of multidrug-resistant Mycobacterium tuberculosis. Trends Genet. 29:160–169

    Article  PubMed  CAS  Google Scholar 

  18. Chang S, Sievert DM, Hageman JC, et al (2003) Infection with vancomycin-resistant Staphylococcus aureus containing the vanA resistance gene. N. Engl. J. Med. 348:1342–1347

    Article  PubMed  Google Scholar 

  19. Rowe B, Ward LR, Threlfall EJ (1997) Multidrug-resistant Salmonella typhi: a worldwide epidemic. Clin. Infect. Dis. 24(Suppl 1):S106–S109

    Article  PubMed  Google Scholar 

  20. Manchanda V, Sanchaita S, Singh N (2010) Multidrug resistant Acinetobacter. J Glob Infect Dis 2:291–304

    Article  PubMed  PubMed Central  Google Scholar 

  21. Beceiro A, Tomás M, Bou G (2013) Antimicrobial resistance and virulence: a successful or deleterious association in the bacterial world? Clin. Microbiol. Rev. 26:185–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Qin J, Li R, Raes J, et al (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. International Human Genome Sequencing Consortium (2004) Finishing the euchromatic sequence of the human genome. Nature 431:931–945

    Article  CAS  Google Scholar 

  24. Bäckhed F, Ding H, Wang T, et al (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. U. S. A. 101:15718–15723

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Round JL, Mazmanian SK (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9:313–323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Eckburg PB, Bik EM, Bernstein CN, et al (2005) Diversity of the human intestinal microbial flora. Science 308:1635–1638

    Article  PubMed  PubMed Central  Google Scholar 

  27. Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–848

    Article  CAS  PubMed  Google Scholar 

  28. Chen J, Novick RP (2009) Phage-mediated intergeneric transfer of toxin genes. Science 323:139–141

    Article  CAS  PubMed  Google Scholar 

  29. Lester CH, Frimodt-Møller N, Sørensen TL, et al (2006) 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. 50:596–599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Liu L, Chen X, Skogerbø G, et al (2012) The human microbiome: a hot spot of microbial horizontal gene transfer. Genomics 100:265–270

    Article  CAS  PubMed  Google Scholar 

  31. Human Microbiome Project Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214

    Article  CAS  Google Scholar 

  32. Smillie CS, Smith MB, Friedman J, et al (2011) Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480:241–244

    Article  CAS  PubMed  Google Scholar 

  33. Aarestrup FM, Wegener HC, Collignon P (2008) Resistance in bacteria of the food chain: epidemiology and control strategies. Expert Rev. Anti-Infect. Ther. 6:733–750

    Article  PubMed  Google Scholar 

  34. Forsberg KJ, Patel S, Gibson MK, et al (2014) Bacterial phylogeny structures soil resistomes across habitats. Nature 509:612–616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Jernberg C, Löfmark S, Edlund C, Jansson JK (2010) Long-term impacts of antibiotic exposure on the human intestinal microbiota. Microbiology 156:3216–3223

    Article  CAS  PubMed  Google Scholar 

  36. Seville LA, Patterson AJ, Scott KP, et al (2009) Distribution of tetracycline and erythromycin resistance genes among human oral and fecal metagenomic DNA. Microb. Drug Resist. 15:159–166

    Article  CAS  PubMed  Google Scholar 

  37. Diaz-Torres ML, Villedieu A, Hunt N, et al (2006) Determining the antibiotic resistance potential of the indigenous oral microbiota of humans using a metagenomic approach. FEMS Microbiol. Lett. 258:257–262

    Article  CAS  PubMed  Google Scholar 

  38. Ready D, Bedi R, Spratt DA, et al (2003) Prevalence, proportions, and identities of antibiotic-resistant bacteria in the oral microflora of healthy children. Microb. Drug Resist. 9:367–372

    Article  CAS  PubMed  Google Scholar 

  39. Villedieu A, Diaz-Torres ML, Hunt N, et al (2003) Prevalence of tetracycline resistance genes in oral bacteria. Antimicrob. Agents Chemother. 47:878–882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Dominguez-Bello MG, Costello EK, Contreras M, et al (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. U. S. A. 107:11971–11975

    Article  PubMed  PubMed Central  Google Scholar 

  41. Penders J, Thijs C, Vink C, et al (2006) Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118:511–521

    Article  PubMed  Google Scholar 

  42. Adlerberth I, Wold AE (2009) Establishment of the gut microbiota in Western infants. Acta Paediatr. 98:229–238

    Article  CAS  PubMed  Google Scholar 

  43. Azad MB, Konya T, Maughan H, et al (2013) Infant gut microbiota and the hygiene hypothesis of allergic disease: impact of household pets and siblings on microbiota composition and diversity. Allergy Asthma Clin Immunol 9:15

    Article  PubMed  PubMed Central  Google Scholar 

  44. De Filippo C, Cavalieri D, Di Paola M, et al (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. U. S. A. 107:14691–14696

    Article  PubMed  PubMed Central  Google Scholar 

  45. Harmsen HJ, Wildeboer-Veloo AC, Raangs GC, et al (2000) Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J. Pediatr. Gastroenterol. Nutr. 30:61–67

    Article  CAS  PubMed  Google Scholar 

  46. Koenig JE, Spor A, Scalfone N, et al (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. U. S. A. 108(Suppl 1):4578–4585

    Article  CAS  PubMed  Google Scholar 

  47. Gosalbes MJ, Vallès Y, Jiménez-Hernández N, et al (2016) High frequencies of antibiotic resistance genes in infants’ meconium and early fecal samples. J. Dev. Orig. Health Dis. 7:35–44

    Article  CAS  PubMed  Google Scholar 

  48. Fouhy F, Ogilvie LA, Jones BV, et al (2014) Identification of aminoglycoside and β-lactam resistance genes from within an infant gut functional metagenomic library. PLoS One 9:e108016

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Kirtzalidou EI, Mitsou EK, Pramateftaki P, Kyriacou A (2012) Screening fecal enterococci from Greek healthy infants for susceptibility to antimicrobial agents. Microb. Drug Resist. 18:578–585

    Article  CAS  PubMed  Google Scholar 

  50. Moore AM, Patel S, Forsberg KJ, et al (2013) Pediatric fecal microbiota harbor diverse and novel antibiotic resistance genes. PLoS One 8:e78822

    Article  PubMed  PubMed Central  Google Scholar 

  51. Gasparrini AJ, Crofts TS, Gibson MK, et al (2016) Antibiotic perturbation of the preterm infant gut microbiome and resistome. Gut Microbes:1–7

  52. Gibson MK, Wang B, Ahmadi S, et al (2016) Developmental dynamics of the preterm infant gut microbiota and antibiotic resistome. Nat Microbiol 1:16024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Yassour M, Vatanen T, Siljander H, et al (2016) Natural history of the infant gut microbiome and impact of antibiotic treatment on bacterial strain diversity and stability. Sci. Transl. Med. 8:343ra81

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Bryce A, Costelloe C, Hawcroft C, et al (2016) Faecal carriage of antibiotic resistant Escherichia coli in asymptomatic children and associations with primary care antibiotic prescribing: a systematic review and meta-analysis. BMC Infect. Dis. 16:359

    Article  PubMed  PubMed Central  Google Scholar 

  55. Zhang L, Kinkelaar D, Huang Y, et al (2011) Acquired antibiotic resistance: are we born with it? Appl. Environ. Microbiol. 77:7134–7141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Ravi A, Avershina E, Foley SL, et al (2015) The commensal infant gut meta-mobilome as a potential reservoir for persistent multidrug resistance integrons. Sci Rep 5:15317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. de Vries LE, Vallès Y, Agersø Y, et al (2011) The gut as reservoir of antibiotic resistance: microbial diversity of tetracycline resistance in mother and infant. PLoS One 6:e21644

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Moore AM, Ahmadi S, Patel S, et al (2015) Gut resistome development in healthy twin pairs in the first year of life. Microbiome 3:27

    Article  PubMed  PubMed Central  Google Scholar 

  59. Ghosh TS, Gupta SS, Nair GB, Mande SS (2013) In silico analysis of antibiotic resistance genes in the gut microflora of individuals from diverse geographies and age-groups. PLoS One 8:e83823

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Yatsunenko T, Rey FE, Manary MJ, et al (2012) Human gut microbiome viewed across age and geography. Nature 486:222–227

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Gomez A, Petrzelkova KJ, Burns MB, et al (2016) Gut microbiome of coexisting BaAka pygmies and Bantu reflects gradients of traditional subsistence patterns. Cell Rep. 14:2142–2153

    Article  CAS  PubMed  Google Scholar 

  62. Martínez JL (2008) Antibiotics and antibiotic resistance genes in natural environments. Science 321:365–367

    Article  PubMed  CAS  Google Scholar 

  63. Vaz-Moreira I, Nunes OC, Manaia CM (2014) Bacterial diversity and antibiotic resistance in water habitats: searching the links with the human microbiome. FEMS Microbiol. Rev. 38:761–778

    Article  CAS  PubMed  Google Scholar 

  64. Allen HK, Moe LA, Rodbumrer J, et al (2008) Functional metagenomics reveals diverse β-lactamases in a remote Alaskan soil. ISME J 3:243–251

    Article  PubMed  CAS  Google Scholar 

  65. Perron GG, Whyte L, Turnbaugh PJ, et al (2015) Functional characterization of bacteria isolated from ancient arctic soil exposes diverse resistance mechanisms to modern antibiotics. PLoS One 10:e0069533

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Pallecchi L, Lucchetti C, Bartoloni A, et al (2007) Population structure and resistance genes in antibiotic-resistant bacteria from a remote community with minimal antibiotic exposure. Antimicrob. Agents Chemother. 51:1179–1184

    Article  CAS  PubMed  Google Scholar 

  67. Clemente JC, Pehrsson EC, Blaser MJ, et al (2015) The microbiome of uncontacted Amerindians. Sci. Adv. doi:10.1126/sciadv.1500183

    PubMed  PubMed Central  Google Scholar 

  68. Bartoloni A, Bartalesi F, Mantella A, et al (2004) High prevalence of acquired antimicrobial resistance unrelated to heavy antimicrobial consumption. J Infect Dis 189:1291–1294

    Article  CAS  PubMed  Google Scholar 

  69. Pehrsson EC, Tsukayama P, Patel S, et al (2016) Interconnected microbiomes and resistomes in low-income human habitats. Nature 533:212–216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Fahrenfeld N, Knowlton K, Krometis LA, et al (2014) Effect of manure application on abundance of antibiotic resistance genes and their attenuation rates in soil: field-scale mass balance approach. Environ Sci Technol 48:2643–2650

    Article  CAS  PubMed  Google Scholar 

  71. Thanner S, Drissner D, Walsh F (2016) Antimicrobial resistance in agriculture. MBio 7:e02227–e02215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Aubry-Damon H, Grenet K, Sall-Ndiaye P, et al (2004) Antimicrobial resistance in commensal flora of pig farmers. Emerg. Infect. Dis. 10:873–879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. van den Bogaard AE, Stobberingh EE (2000) Epidemiology of resistance to antibiotics. Links between animals and humans. Int. J. Antimicrob. Agents 14:327–335

    Article  PubMed  Google Scholar 

  74. Devirgiliis C, Barile S, Perozzi G (2011) Antibiotic resistance determinants in the interplay between food and gut microbiota. Genes Nutr. 6:275–284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Kassenborg HD, Smith KE, Vugia DJ, et al (2004) Fluoroquinolone-resistant Campylobacter infections: eating poultry outside of the home and foreign travel are risk factors. Clin. Infect. Dis. 38(Suppl 3):S279–S284

    Article  PubMed  Google Scholar 

  76. Johnson JR, Sannes MR, Croy C, et al (2007) Antimicrobial drug-resistant Escherichia coli from humans and poultry products, Minnesota and Wisconsin, 2002-2004. Emerg. Infect. Dis. 13:838–846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Holmberg SD, Wells JG, Cohen ML (1984) Animal-to-man transmission of antimicrobial-resistant Salmonella: investigations of U.S. outbreaks, 1971-1983. Science 225:833–835

    Article  CAS  PubMed  Google Scholar 

  78. Pal C, Bengtsson-Palme J, Kristiansson E, Larsson DGJ (2016) The structure and diversity of human, animal and environmental resistomes. Microbiome 4:54

    Article  PubMed  PubMed Central  Google Scholar 

  79. Rutgersson C, Fick J, Marathe N, et al (2014) Fluoroquinolones and qnr genes in sediment, water, soil, and human fecal flora in an environment polluted by manufacturing discharges. Environ Sci Technol 48:7825–7832

    Article  CAS  PubMed  Google Scholar 

  80. Hocquet D, Muller A, Bertrand X (2016) What happens in hospitals does not stay in hospitals: antibiotic-resistant bacteria in hospital wastewater systems. J Hosp Infect 93:395–402

    Article  CAS  PubMed  Google Scholar 

  81. Hansen TA, Joshi T, Larsen AR, et al (2016) Vancomycin gene selection in the microbiome of urban Rattus norvegicus from hospital environment. Evol Med Public Health 2016:219–226

    Article  PubMed  PubMed Central  Google Scholar 

  82. Johnning A, Moore ERB, Svensson-Stadler L, et al (2013) Acquired genetic mechanisms of a multiresistant bacterium isolated from a treatment plant receiving wastewater from antibiotic production. Appl. Environ. Microbiol. 79:7256–7263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Bengtsson-Palme J, Angelin M, Huss M, et al (2015) The human gut microbiome as a transporter of antibiotic resistance genes between continents. Antimicrob. Agents Chemother. 59:6551–6560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Murray BE, Mathewson JJ, DuPont HL, et al (1990) Emergence of resistant fecal Escherichia coli in travelers not taking prophylactic antimicrobial agents. Antimicrob. Agents Chemother. 34:515–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Li B, Yang Y, Ma L, et al (2015) Metagenomic and network analysis reveal wide distribution and co-occurrence of environmental antibiotic resistance genes. ISME J 9:2490–2502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. MetaSUB International Consortium (2016) The Metagenomics and Metadesign of the Subways and Urban Biomes (MetaSUB) International Consortium inaugural meeting report. Microbiome 4:24

    Article  Google Scholar 

  87. Levy SB, Marshall B, Schluederberg S, et al (1988) High frequency of antimicrobial resistance in human fecal flora. Antimicrob. Agents Chemother. 32:1801–1806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Sommer MOA, Dantas G, Church GM (2009) Functional characterization of the antibiotic resistance reservoir in the human microflora. Science 325:1128–1131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Field W, Hershberg R (2015) Alarmingly high segregation frequencies of quinolone resistance alleles within human and animal microbiomes are not explained by direct clinical antibiotic exposure. Genome Biol Evol 7:1743–1757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Forslund K, Sunagawa S, Kultima JR, et al (2013) Country-specific antibiotic use practices impact the human gut resistome. Genome Res. 23:1163–1169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Hu Y, Yang X, Qin J, et al (2013) Metagenome-wide analysis of antibiotic resistance genes in a large cohort of human gut microbiota. Nat. Commun. 4:2151

    PubMed  Google Scholar 

  92. Alekshun MN, Levy SB (2006) Commensals upon us. Biochem. Pharmacol. 71:893–900

    Article  CAS  PubMed  Google Scholar 

  93. Andremont A (2003) Commensal flora may play key role in spreading antibiotic resistance. ASM News 69:601–607

    Google Scholar 

  94. Blake DP, Hillman K, Fenlon DR, Low JC (2003) Transfer of antibiotic resistance between commensal and pathogenic members of the Enterobacteriaceae under ileal conditions. J. Appl. Microbiol. 95:428–436

    Article  CAS  PubMed  Google Scholar 

  95. Karami N, Martner A, Enne VI, et al (2007) Transfer of an ampicillin resistance gene between two Escherichia coli strains in the bowel microbiota of an infant treated with antibiotics. J. Antimicrob. Chemother. 60:1142–1145

    Article  CAS  PubMed  Google Scholar 

  96. Poirel L, Rodriguez-Martinez J-M, Mammeri H, et al (2005) Origin of plasmid-mediated quinolone resistance determinant QnrA. Antimicrob. Agents Chemother. 49:3523–3525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Poirel L, Kampfer P, Nordmann P (2002) Chromosome-encoded Ambler class A β-lactamase of Kluyvera georgiana, a probable progenitor of a subgroup of CTX-M extended-spectrum β-lactamases. Antimicrob. Agents Chemother. 46:4038–4040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Hopkins JD, O’Brien TF, Syvanen M (1988) Functional and structural map of pLST1000: a multiresistance plasmid widely distributed in Enterobacteriaceae. Plasmid 20:163–166

    Article  CAS  PubMed  Google Scholar 

  99. Hall RM, Collis CM (1995) Mobile gene cassettes and integrons: capture and spread of genes by site-specific recombination. Mol. Microbiol. 15:593–600

    Article  CAS  PubMed  Google Scholar 

  100. Liebert CA, Hall RM, Summers AO (1999) Transposon Tn21, flagship of the floating genome. Microbiol. Mol. Biol. Rev. 63:507–522

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Gibson MK, Forsberg KJ, Dantas G (2015) Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology. ISME J 9:207–216

    Article  CAS  PubMed  Google Scholar 

  102. McArthur AG, Waglechner N, Nizam F, et al (2013) The comprehensive antibiotic resistance database. Antimicrob. Agents Chemother. 57:3348–3357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Piddock LJV (2016) Assess drug-resistance phenotypes, not just genotypes. Nat Microbiol 1:16120

    Article  CAS  PubMed  Google Scholar 

  104. Martínez JL, Coque TM, Baquero F (2015) What is a resistance gene? Ranking risk in resistomes. Nat Rev Microbiol 13:116–123

    Article  PubMed  CAS  Google Scholar 

  105. van Hoek AHAM, Mevius D, Guerra B, et al (2011) Acquired antibiotic resistance genes: an overview. Front. Microbiol. 2:203

    PubMed  PubMed Central  Google Scholar 

  106. Shterzer N, Mizrahi I (2015) The animal gut as a melting pot for horizontal gene transfer. Can. J. Microbiol. 61:603–605

    Article  CAS  PubMed  Google Scholar 

  107. Leplae R, Lima-Mendez G, Toussaint A (2010) ACLAME: a CLAssification of Mobile genetic Elements, update 2010. Nucleic Acids Res. 38:D57–D61

    Article  CAS  PubMed  Google Scholar 

  108. Fouts DE (2006) Phage_Finder: automated identification and classification of prophage regions in complete bacterial genome sequences. Nucleic Acids Res. 34:5839–5851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Fouts DE, Brinkac L, Beck E, et al (2012) PanOCT: automated clustering of orthologs using conserved gene neighborhood for pan-genomic analysis of bacterial strains and closely related species. Nucleic Acids Res. 40:e172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Chan AP, Sutton G, DePew J, et al (2015) A novel method of consensus pan-chromosome assembly and large-scale comparative analysis reveal the highly flexible pan-genome of Acinetobacter baumannii. Genome Biol. 16:143

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  111. Dick GJ, Andersson AF, Baker BJ, et al (2009) Community-wide analysis of microbial genome sequence signatures. Genome Biol. 10:R85

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Calvo B, Melo ASA, Perozo-Mena A, et al (2016) First report of Candida auris in America: clinical and microbiological aspects of 18 episodes of candidemia. J. Inf. Secur. doi:10.1016/j.jinf.2016.07.008

    Google Scholar 

  113. Jones MB, Nierman WC, Shan Y, et al (2017) Reducing the bottleneck in discovery of novel antibiotics. Microb. Ecol. 73:658–667

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. J. Craig Venter Institute|, Rockville, MD, 20850, USA

    Lauren Brinkac, Alexander Voorhies, Andres Gomez & Karen E. Nelson

  2. Department of Biotechnology and Food Technology, Durban University of Technology, Durban, 4000, South Africa

    Lauren Brinkac & Karen E. Nelson

Authors
  1. Lauren Brinkac
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexander Voorhies
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andres Gomez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Karen E. Nelson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lauren Brinkac.

Ethics declarations

Funding

This project has been funded in whole or part with federal funds from the National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services, under Award Number U19AI110819.

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brinkac, L., Voorhies, A., Gomez, A. et al. The Threat of Antimicrobial Resistance on the Human Microbiome. Microb Ecol 74, 1001–1008 (2017). https://doi.org/10.1007/s00248-017-0985-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-017-0985-z

Keywords

Search

Navigation