The bacterial mobile resistome transfer network connecting the animal and human microbiomes

Applied and Environmental Microbiology

Volumn 82, Issue 22, 2016, Pages 6672-6681

  Hu, Yongfei ^a,b,c   Yang, Xi ^a   Li, Jing ^a,b   Lv, Na ^a,b   Liu, Fei ^a,b,c   Wu, Jun ^a,b   Lin, Ivan Y C ^a,b   Wu, Na ^d   Weimer, Bart C ^e   Gao, George F ^a,f   Liu, Yulan ^d   Zhu, Baoli ^a,b,c  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b Beijing Key Laboratory of Microbial Drug Resistance and Resistome   (China)

^c ZHEJIANG UNIVERSITY   (China)

^d PEKING UNIVERSITY PEOPLE S HOSPITAL   (China)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ANTIBIOTICS; ECOLOGY;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTANCE GENES; BACTERIAL GENOMES; BACTERIAL SPECIES; DRIVING FORCES; HUMAN PATHOGENS; SYNERGISTIC EFFECT; TRANSFER NETWORK;

BACTERIA;

ANIMAL; ANTIBIOTIC RESISTANCE; BACTERIUM; COLONIZATION; DIGESTIVE SYSTEM; GENE; GENOME; MICROBIAL COMMUNITY; PATHOGEN; PHYLOGENY;

ANIMALIA; BACTERIA (MICROORGANISMS); PROTEOBACTERIA;

RNA 16S;

ANIMAL; ANTIBIOTIC RESISTANCE; BACTERIAL GENOME; BACTERIUM; DOMESTIC ANIMAL; ECOSYSTEM; GASTROINTESTINAL TRACT; GENETICS; HORIZONTAL GENE TRANSFER; HUMAN; METAGENOME; MICROBIOLOGY; MICROFLORA; PATHOGENICITY; PHYLOGENY; PROTEOBACTERIA;

ANIMALS; ANIMALS, DOMESTIC; BACTERIA; DRUG RESISTANCE, BACTERIAL; ECOSYSTEM; GASTROINTESTINAL TRACT; GENE TRANSFER, HORIZONTAL; GENOME, BACTERIAL; HUMANS; METAGENOME; MICROBIOTA; PHYLOGENY; PROTEOBACTERIA; RNA, RIBOSOMAL, 16S; SOIL MICROBIOLOGY;

EID: 84995532206     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01802-16     Document Type: Article

References (46)

1. World Health Organization. 2014. Antimicrobial resistance: global report on surveillance 2014. World Health Organization, Geneva, Switzerland. http://www.who.int/drugresistance/documents/surveillancereport/en/.
2. Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J. 2010. Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol 8:251-259. http://dx.doi.org/10.1038/nrmicro2312.
3. Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M, Landraud L, Rolain JM. 2014. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother 58:212-220. http://dx.doi.org/10.1128/AAC.01310-13.
4. McArthur AG, Waglechner N, Nizam F, Yan A, Azad MA, Baylay AJ, Bhullar K, Canova MJ, De Pascale G, Ejim L, Kalan L, King AM, Koteva K, Morar M, Mulvey MR, O'Brien JS, Pawlowski AC, Piddock LJ, Spanogiannopoulos P, Sutherland AD, Tang I, Taylor PL, Thaker M, Wang W, Yan M, Yu T, Wright GD. 2013. The comprehensive antibiotic resistance database. Antimicrob Agents Chemother 57:3348-3357. http://dx.doi.org/10.1128/AAC.00419-13.
5. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, Aarestrup FM, Larsen MV. 2012. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67:2640-2644. http://dx.doi.org/10.1093/jac/dks261.
6. Liu B, Pop M. 2009. ARDB-Antibiotic Resistance Genes Database. Nucleic Acids Res 37:D443-D447. http://dx.doi.org/10.1093/nar/gkn656.
7. Courvalin P. 2008. Predictable and unpredictable evolution of antibiotic resistance. J Intern Med 264:4-16. http://dx.doi.org/10.1111/j.1365-2796.2008.01940.x.
8. D'Costa VM, McGrann KM, Hughes DW, Wright GD. 2006. Sampling the antibiotic resistome. Science 311:374-377. http://dx.doi.org/10.1126/science.1120800.
9. Wright GD. 2007. The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 5:175-186. http://dx.doi.org/10.1038/nrmicro1614.
10. Fajardo A, Martínez-Martín N, Mercadillo M, Galán JC, Ghysels B, Matthijs S, Cornelis P, Wiehlmann L, Tümmler B, Baquero F, Martínez JL. 2008. The neglected intrinsic resistome of bacterial pathogens. PLoS One 3:e1619. http://dx.doi.org/10.1371/journal.pone.0001619.
11. Wellington EM, Boxall AB, Cross P, Feil EJ, Gaze WH, Hawkey PM, Johnson-Rollings AS, Jones DL, Lee NM, Otten W, Thomas CM, Williams AP. 2013. The role of the natural environment in the emergence of antibiotic resistance in gram-negative bacteria. Lancet Infect Dis 13: 155-165. http://dx.doi.org/10.1016/S1473-3099(12)70317-1.
12. Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MO, Dantas G. 2012. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337:1107-1111. http://dx.doi.org/10.1126/science.1220761.
13. Hu Y, Yang X, Qin J, Lu N, Cheng G, Wu N, Pan Y, Li J, Zhu L, Wang X, Meng Z, Zhao F, Liu D, Ma J, Qin N, Xiang C, Xiao Y, Li L, Yang H, Wang J, Yang R, Gao GF, Wang J, Zhu B. 2013. Metagenome-wide analysis of antibiotic resistance genes in a large cohort of human gut microbiota. Nat Commun 4:2151. http://dx.doi.org/10.1038/ncomms3151.
14. Forslund K, Sunagawa S, Kultima JR, Mende DR, Arumugam M, Typas A, Bork P. 2013. Country-specific antibiotic use practices impact the human gut resistome. Genome Res 23:1163-1169. http://dx.doi.org/10.1101/gr.155465.113.
15. Sommer MO, Dantas G, Church GM. 2009. Functional characterization of the antibiotic resistance reservoir in the human microflora. Science 325:1128-1131. http://dx.doi.org/10.1126/science.1176950.
16. Martínez JL, Coque TM, Baquero F. 2015. What is a resistance gene? Ranking risk in resistomes. Nat Rev Microbiol 13:116-123. http://dx.doi.org/10.1038/nrmicro3399.
17. Gogarten JP, Townsend JP. 2005. Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 3:679-687. http://dx.doi.org/10.1038/nrmicro1204.
18. Ochman H, Lawrence JG, Groisman EA. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299-304. http://dx.doi.org/10.1038/35012500.
19. Popa O, Dagan T. 2011. Trends and barriers to lateral gene transfer in prokaryotes. Curr Opin Microbiol 14:615-623. http://dx.doi.org/10.1016/j.mib.2011.07.027.
20. Forsberg KJ, Patel S, Gibson MK, Lauber CL, Knight R, Fierer N, Dantas G. 2014. Bacterial phylogeny structures soil resistomes across habitats. Nature 509:612-616. http://dx.doi.org/10.1038/nature13377.
21. Smillie CS, Smith MB, Friedman J, Cordero OX, David LA, Alm EJ. 2011. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480:241-244. http://dx.doi.org/10.1038/nature10571.
22. Gibson MK, Forsberg KJ, Dantas G. 2015. Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology. ISME J 9:207-216. http://dx.doi.org/10.1038/ismej.2014.106.
23. Li J, Jia H, Cai X, Zhong H, Feng Q, Sunagawa S, Arumugam M, Kultima JR, Prifti E, Nielsen T, Juncker AS, Manichanh C, Chen B, Zhang W, Levenez F, Wang J, Xu X, Xiao L, Liang S, Zhang D, Zhang Z, Chen W, Zhao H, Al-Aama JY, Edris S, Yang H, Wang J, Hansen T, Nielsen HB, Brunak S, Kristiansen K, Guarner F, Pedersen O, Doré J, Ehrlich SD, MetaHIT Consortium, Bork P, Wang J. 2014. An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol 32:834-841. http://dx.doi.org/10.1038/nbt.2942.
24. UniProt Consortium. 2014. Activities at the universal protein resource (UniProt). Nucleic Acids Res 42:D191-D198. http://dx.doi.org/10.1093/nar/gkt1140.
25. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Doré J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, MetaHIT Consortium, Bork P, Ehrlich SD, Wang J. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59-65. http://dx.doi.org/10.1038/nature08821.
26. Noguchi H, Taniguchi T, Itoh T. 2008. MetaGeneAnnotator: detecting species-specific patterns of ribosomal binding site for precise gene prediction in anonymous prokaryotic and phage genomes. DNA Res 15:387-396. http://dx.doi.org/10.1093/dnares/dsn027.
27. Huson DH, Auch AF, Qi J, Schuster SC. 2007. MEGAN analysis of metagenomic data. Genome Res 17:377-386. http://dx.doi.org/10.1101/gr.5969107.
28. Schmidt H, Hensel M. 2004. Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev 17:14-56. http://dx.doi.org/10.1128/CMR.17.1.14-56.2004.
29. Fournier PE, Vallenet D, Barbe V, Audic S, Ogata H, Poirel L, Richet H, Robert C, Mangenot S, Abergel C, Nordmann P, Weissenbach J, Raoult D, Claverie JM. 2006. Comparative genomics of multidrug resistance in Acinetobacter baumannii. PLoS Genet 2:e7. http://dx.doi.org/10.1371/journal.pgen.0020007.
30. Chiu CH, Tang P, Chu C, Hu S, Bao Q, Yu J, Chou YY, Wang HS, Lee YS. 2005. The genome sequence of Salmonella enterica serovar Choleraesuis, a highly invasive and resistant zoonotic pathogen. Nucleic Acids Res 33:1690-1698. http://dx.doi.org/10.1093/nar/gki297.
31. Gillings M, Boucher Y, Labbate M, Holmes A, Krishnan S, Holley M, Stokes HW. 2008. The evolution of class 1 integrons and the rise of antibiotic resistance. J Bacteriol 190:5095-5100. http://dx.doi.org/10.1128/JB.00152-08.
32. Edmond KM, Kortsalioudaki C, Scott S, Schrag SJ, Zaidi AK, Cousens S, Heath PT. 2012. Group B streptococcal disease in infants aged younger than 3 months: systematic review and meta-analysis. Lancet 379:547-556. http://dx.doi.org/10.1016/S0140-6736(11)61651-6.
33. Antonopoulos DA, Huse SM, Morrison HG, Schmidt TM, Sogin ML, Young VB. 2009. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect Immun 77: 2367-2375. http://dx.doi.org/10.1128/IAI.01520-08.
34. Young VB, Schmidt TM. 2004. Antibiotic-associated diarrhea accompanied by large-scale alterations in the composition of the fecal microbiota. J Clin Microbiol 42:1203-1206. http://dx.doi.org/10.1128/JCM.42.3.1203-1206.2004.
35. Dantas G, Sommer MO, Oluwasegun RD, Church GM. 2008. Bacteria subsisting on antibiotics. Science 320:100-103. http://dx.doi.org/10.1126/science.1155157.
36. Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, Scheld M, Spellberg B, Bartlett J. 2009. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis 48:1-12. http://dx.doi.org/10.1086/595011.
37. Perry JA, Wright GD. 2013. The antibiotic resistance "mobilome": searching for the link between environment and clinic. Front Microbiol 4:138.
38. Yap MNF. 2013. The double life of antibiotics. Mo Med 110:320-324.
39. Ghosh S, LaPara TM. 2007. The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. ISME J 1:191-203. http://dx.doi.org/10.1038/ismej.2007.31.
40. Moubareck C, Bourgeois N, Courvalin P, Doucet-Populaire F. 2003. Multiple antibiotic resistance gene transfer from animal to human enterococci in the digestive tract of gnotobiotic mice. Antimicrob Agents Chemother 47:2993-2996. http://dx.doi.org/10.1128/AAC.47.9.2993-2996.2003.
41. Smith DL, Harris AD, Johnson JA, Silbergeld EK, Morris JG. 2002. Animal antibiotic use has an early but important impact on the emergence of antibiotic resistance in human commensal bacteria. Proc Natl Acad Sci U S A 99:6434-6439. http://dx.doi.org/10.1073/pnas.082188899.
42. Hu Y, Yang X, Lu N, Zhu B. 2014. The abundance of antibiotic resistance genes in human guts has correlation to the consumption of antibiotics in animal. Gut Microbes 5:245-249. http://dx.doi.org/10.4161/gmic.27916.
43. Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld RD, Hashsham SA, Tiedje JM. 2013. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci U S A 110:3435-3440. http://dx.doi.org/10.1073/pnas.1222743110.
44. D'Costa VM, King CE, Kalan L, Morar M, Sung WW, Schwarz C, Froese D, Zazula G, Calmels F, Debruyne R, Golding GB, Poinar HN, Wright GD. 2011. Antibiotic resistance is ancient. Nature 477:457-461. http://dx.doi.org/10.1038/nature10388.
45. Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, Yu LF, Gu D, Ren H, Chen X, Lv L, He D, Zhou H, Liang Z, Liu JH, Shen J. 2016. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 16:161-168. http://dx.doi.org/10.1016/S1473-3099(15)00424-7.
46. Hu Y, Liu F, Lin IY, Gao GF, Zhu B. 2016. Dissemination of the mcr-1 colistin resistance gene. Lancet Infect Dis 16:146-147. http://dx.doi.org/10.1016/S1473-3099(15)00533-2.