Bacterial phylogeny structures soil resistomes across habitats

Nature

Volumn 509, Issue 7502, 2014, Pages 612-616

  Forsberg, Kevin J ^a   Patel, Sanket ^a   Gibson, Molly K ^a   Lauber, Christian L ^b   Knight, Rob ^b,c   Fierer, Noah ^b   Dantas, Gautam ^a,d  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRASE; NITROGEN FERTILIZER; RNA 16S; TRANSPOSASE;

ANTIBIOTIC RESISTANCE; BACTERIUM; GENOME; GRASSLAND; HABITAT TYPE; PHYLOGENETICS; PHYLOGENY; SOIL MICROORGANISM; SOIL TYPE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; GENE SEQUENCE; GRASSLAND; HORIZONTAL GENE TRANSFER; METAGENOMICS; MICROBIAL COMMUNITY; MICROHABITAT; NONHUMAN; OPEN READING FRAME; PHYLOGENY; PRIORITY JOURNAL; SOIL; SOIL MICROFLORA; TAXONOMY;

BACTERIA (MICROORGANISMS);

AGRICULTURE; ANTI-BACTERIAL AGENTS; BACTERIA; DRUG RESISTANCE, MICROBIAL; ECOSYSTEM; FERTILIZERS; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; GENOME, BACTERIAL; INTEGRASES; METAGENOME; METAGENOMICS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; NITROGEN; OPEN READING FRAMES; PHYLOGENY; POACEAE; RNA, RIBOSOMAL, 16S; SOIL MICROBIOLOGY; SYNTENY; TRANSPOSASES;

EID: 84901652050     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13377     Document Type: Article

References (42)

1. D'Costa, V. M. et al. Antibiotic resistance is ancient. Nature 477, 457-461 (2011).
2. Allen, H. K., Moe, L. A., Rodbumrer, J., Gaarder, A. & Handelsman, J. Functional metagenomics reveals diverse beta-lactamases in a remote Alaskan soil. ISMEJ. 3, 243-251 (2009).
3. Allen, H. K. et al. Call of the wild: antibiotic resistance genes in natural environments. Nature Rev. Microbiol. 8, 251-259 (2010).
4. Forsberg, K. J. et al. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337, 1107-1111 (2012).
5. Wright, G. D. Antibiotic resistance in the environment: a link to the clinic? Curr. Opin. Microbiol. 13, 589-594 (2010).
6. Benveniste, R. & Davies, J. Aminoglycoside antibiotic-inactivating enzymes in actinomycetes similar to those present in clinical isolates of antibiotic-resistant bacteria. Proc. Natl Acad. Sci. USA 70, 2276-2280 (1973).
7. Langille, M. G. et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnol. 31, 814-821 (2013).
8. Fierer, N. et al. Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J. 6, 1007-1017 (2012).
9. Fierer, N. et al. Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc. Natl Acad. Sci. USA 109, 21390-21395 (2012).
10. Fierer, N. et al. Reconstructing the microbial diversity and function of pre-agricultural tallgrass prairie soils in the United States. Science 342, 621-624 (2013).
11. Muegge, B. D. et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332, 970-974 (2011).
12. Zaneveld, J. R., Lozupone, C., Gordon, J. I. & Knight, R. Ribosomal RNA diversity predicts genomediversity in gut bacteria and their relatives. Nucleic Acids Res. 38, 3869-3879 (2010).
13. Smillie, C. S. et al. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480, 241-244 (2011).
14. Stokes, H. W. & Gillings, M. R. Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into Gram-negative pathogens. FEMS Microbiol. Rev. 35, 790-819 (2011).
15. Walsh, C. Molecular mechanisms that confer antibacterial drug resistance. Nature 406, 775-781 (2000).
16. Pehrsson, E. C., Forsberg, K. J., Gibson, M. K., Ahmadi, S. & Dantas, G. Novel resistance functions uncovered using functional metagenomic investigations of resistance reservoirs. Front. Microbiol. 4, 145 (2013).
17. Delmont, T. O. et al. Structure, fluctuation and magnitude of a natural grasslandsoil metagenome. ISME J. 6, 1677-1687 (2012).
18. Jacoby, G. A. & Munoz-Price, L. S. The new beta-lactamases. N. Engl. J. Med. 352, 380-391 (2005).
19. Nalbantoglu, O. U., Way, S. F., Hinrichs, S. H. & Sayood, K. RAIphy: phylogenetic classification of metagenomics samples using iterative refinement of relative abundance index profiles. BMC Bioinform. 12, 41 (2011).
20. Ramirez, K. S., Lauber, C. L., Knight, R., Bradford, M. A. & Fierer, N. Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systems. Ecology 91, 3463-3470; discussion 3503-3414 (2010).
21. Ventura, M. et al. Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol. Mol. Biol. Rev. 71, 495-548 (2007).
22. Aminov, R. I. & Mackie, R. I. Evolution and ecology of antibiotic resistance genes. FEMS Microbiol. Lett. 271, 147-161 (2007).
23. Davies, J. & Davies, D. Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 74, 417-433 (2010).
24. Medeiros, A. A. Evolution and dissemination of beta-lactamases accelerated by generations of beta-lactam antibiotics. Clin. Inf. Diseases 24 (Suppl. 1), 19-45 (1997).
25. Dantas, G., Sommer, M. O., Oluwasegun, R. D. & Church, G. M. Bacteria subsisting on antibiotics. Science 320, 100-103 (2008).
26. Boucher, H. W. et al. Bad bugs, no drugs: no ESKAPE! Clin. Inf. Diseases 48, 1-12 (2009).
27. Knapp, C. W., Dolfing, J., Ehlert, P. A. & Graham, D. W. Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ. Sci. Technol. 44, 580-587 (2010).
28. Lutz, R. & Bujard, H. Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res. 25, 1203-1210 (1997).
29. Zerbino, D. R. & Birney, E. Velvet: algorithmsfor de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821-829 (2008).
30. de la Bastide, M. & McCombie, W. R. Assembling Genomic DNA sequences with PHRAP 2008/04/23 edn, Vol. 11 (John Wiley, 2007).
31. Moore, A. M. et al. Pediatric fecal microbiota harbor diverse and novel antibiotic resistance genes. PLoS ONE 8, e78822 (2013).
32. Tatusov, R. L., Galperin, M. Y., Natale, D. A. & Koonin, E. V. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 28, 33-36 (2000).
33. Zhu, W., Lomsadze, A. & Borodovsky, M. Ab initio gene identification in metagenomic sequences. Nucleic Acids Res. 38, e132 (2010).
34. Finn, R. D., Clements, J. & Eddy, S. R. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 39, W29-37 (2011).
35. Haft, D. H. et al. TIGRFAMs: a protein family resource for the functional identification of proteins. Nucleic Acids Res. 29, 41-43 (2001).
36. Bateman, A. et al. The Pfam protein families database. Nucleic Acids Res. 28, 263-266 (2000).
37. McArthur, A. G. et al. The comprehensive antibiotic resistance database. Antimicrob. Agents Chemother. 57, 3348-3357 (2013).
38. Li, W. & Godzik, A. Cd-hit: a fast programfor clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658-1659 (2006).
39. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335-336 (2010).
40. Lozupone, C., Hamady, M. & Knight, R. UniFrac-an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinform. 7, 371 (2006).
41. Lozupone, C., Lladser, M. E., Knights, D., Stombaugh, J. & Knight, R. UniFrac: an effective distance metric for microbial community comparison. ISME J. 5, 169-172 (2011).
42. Clarke, K. R. & Gorley, R. N. PRIMER v6: User Manual/Tutorial 6th edn, Ch. 13 (PRIMER-E, 2006).