Worldwide prevalence of class 2 integrases outside the clinical setting is associated with human impact

Applied and Environmental Microbiology

Volumn 75, Issue 15, 2009, Pages 5100-5110

  Rodríguez Minguela, Carlos M ^a,c   Apajalahti, Juha H A ^b   Chai, Benli ^a   Cole, James R ^a   Tiedje, James M ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Alimetrics Ltd   (Finland)

^c UNIVERSITY OF PUERTO RICO   (Puerto Rico)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA; AGRICULTURAL SOILS; ANTHROPOGENIC IMPACTS; CLINICAL SETTINGS; CLONE LIBRARY; DISTRIBUTION PATTERNS; ENTEROBACTERIACEAE; FIRMICUTES; HUMAN IMPACT; MANURED SOIL; PCR ASSAY; PHYLOTYPES; SWINE MANURE;

AMINATION; AMINES; AMINO ACIDS; BACTERIOLOGY; BIOSOLIDS; CLONING; DNA; GENES; MANURES; NUCLEIC ACIDS; ORGANIC ACIDS; SOILS;

ASSAYS;

AMINO ACID; INTEGRASE; RNA 16S;

AMINO ACID; BACTERIUM; BIOASSAY; BIOSOLID; CLONE; DNA; ENZYME ACTIVITY; FECES; HOMINID; MANURE; PIG; POLYMERASE CHAIN REACTION;

ARTICLE; BACILLUS; BACTEROIDETES; BIOSOLID; CLINICAL EVALUATION; CLOSTRIDIUM; CODON; CONTROLLED STUDY; CROPLAND; DNA EXTRACTION; ENTEROBACTERIACEAE; FECES; FRACTIONATION; GENE LOCUS; GENE SEQUENCE; GENETIC VARIABILITY; HOST; HUMAN; HUMAN IMPACT (ENVIRONMENT); MANURE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PREVALENCE; SOIL; SWINE;

AMINO ACID SEQUENCE; ANIMALS; CLUSTER ANALYSIS; DNA, BACTERIAL; ENVIRONMENTAL MICROBIOLOGY; GRAM-POSITIVE BACTERIA; HUMAN ACTIVITIES; HUMANS; INTEGRASES; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; PREVALENCE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY;

BACILLUS (BACTERIUM); BACTEROIDETES; CHITINOPHAGA; CLOSTRIDIUM; ENTEROBACTERIACEAE; FIRMICUTES; SPHINGOBACTERIUM; SUIDAE;

EID: 67651253179     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00133-09     Document Type: Article

References (72)

1. Ahmed, A. M., F. Kawaguchi, and T. Shimamoto. 2006. Class 2 integrons in Vibrio cholerae. J. Med. Microbiol. 55:643-644.
2. Altschul, S. F., T. L. Madden, A. A. Schäffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Amman, R. I., W. Ludwig, and K. H. Schleifer. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59:143-169.
4. Apajalahti, J. H. A., H. Kettunen, A. Kettunen, W. E. Holben, P. H. Nurminen, N. Rautonen, and M. Mutanen. 2002. Culture-independent microbial community analysis reveals that inulin in the diet primarily affects previously unknown bacteria in the mouse cecum. Appl. Environ. Microbiol. 68:4986-4995.
5. Apajalahti, J. H., L. K. Särkilahti, B. R. Mäki, J. P. Heikkinen, P. H. Nurminen, and W. E. Holben. 1998. Effective recovery of bacterial DNA and percent-guanine-plus-cytosine-based analysis of community structure in the gastrointestinal tract of broiler chickens. Appl. Environ. Microbiol. 64:4084-4088.
6. Barlow, R. S., and K. S. Gobius. 2006. Diverse class 2 integrons in bacteria from beef cattle sources. J. Antimicrob. Chemother. 58:1133-1138.
7. Bateman, A., L. Coin, R. Durbin, R. D. Finn, V. Hollich, S. Griffiths-Jones, A. Khanna, M. Marshall, S. Moxon, E. L. Sonnhammer, D. J. Studholme, C. Yeats, and S. R. Eddy. 2004. The Pfam protein families database. Nucleic Acids Res. 32:D138-D141.
8. Biskri, L., M. Bouvier, A.-M. Guérout, S. Boisnard, and D. Mazel. 2005. Comparative study of class 1 integron and Vibrio cholerae superintegron integrase activities. J. Bacteriol. 187:1740-1750.
9. Boucher, Y., M. Labbate, J. E. Koenig, and H. W. Stokes. 2007. Integrons: mobilizable platforms that promote genetic diversity in bacteria. Trends Microbiol. 15:301-309.
10. Cole, J. R., B. Chai, R. J. Farris, Q. Wang, A. S. Kulam-Syed-Mohideen, D. M. McGarrell, A. M. Bandela, E. Cardenas, G. M. Garrity, and J. M. Tiedje. 2007. The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res. 35:D169-D172.
11. Collis, C. M., G. D. Recchia, M.-J. Kim, H. W. Stokes, and R. M. Hall. 2001. Efficiency of recombination reactions catalyzed by class 1 integron integrase IntI1. J. Bacteriol. 183:2535-2542.
12. Cornet, F., B. Hallet, and D. J. Sherratt. 1997. Xer recombination in Escherichia coli. Site-specific DNA topoisomerase activity of the XerC and XerD recombinases. J. Biol. Chem. 272:21927-21931.
13. Cotta, M. A., T. R. Whitehead, and R. L. Zeltwanger. 2003. Isolation, characterization and comparison of bacteria from swine faeces and manure storage pits. Environ. Microbiol. 5:737-745.
14. Crespo, O., M. Catalano, S. Piñeiro, M. Matteo, A. Leanza, and D. Centrón. 2005. Tn7 distribution in Helicobacter pylori: a selective paradox. Int. J. Antimicrob. Agents 25:341-344.
15. Dillon, B., L. Thomas, G. Mohmand, A. Zelynski, and J. Iredell. 2005. Multiplex PCR for screening of integrons in bacterial lysates. J. Microbiol. Methods 62:221-232.
16. Eddy, S. 1998. HMMER user's guide: biological sequence analysis using profile hidden Markov models. http://www.csb.yale.edu/userguides/seq/ hmmer/docs/index.html.
17. Elli, M., M. L. Callegari, S. Ferrari, E. Bessi, D. Cattivelli, S. Soldi, L. Morelli, N. Goupil Feuillerat, and J. M. Antoine. 2006. Survival of yogurt bacteria in the human gut. Appl. Environ. Microbiol. 72:5113-5117.
18. Elsaied, H., H. W., Stokes, T. Nakamura, K. Kitamura, H. Fuse, and A. Maruyama. 2007. Novel and diverse integron integrase genes and integron-like gene cassettes are prevalent in deep-sea hydrothermal vents. Environ. Microbiol. 9:2298-2312.
19. Fluit, A. C., and F. J. Schmitz. 2004. Resistance integrons and super-integrons. Clin. Microbiol. Infect. 10:272-288.
20. Francia, M. V., F. de la Cruz, and J. M. García Lobo. 1993. Secondary-sites for integration mediated by the Tn21 integrase. Mol. Microbiol. 10:823-828.
21. Gillings, M. R., M. P. Holley, H. W. Stokes, and A. J. Holmes. 2005. Integrons in Xanthomonas: a source of species genome diversity. Proc. Natl. Acad. Sci. USA 102:4419-4424.
22. Gillings, M. R., S. Krishnan, P. J. Worden, and S. A. Hardwick. 2008. Recovery of diverse genes for class 1 integron-integrases from environmental DNA samples. FEMS Microbiol. Lett. 287:56-62.
23. Giovannoni, S. J. 1991. The polymerase chain reaction, p. 177-201. In E. Stackenbrandt (ed.), Nucleic acids techniques in bacterial systematics. John Wiley & Sons, New York, NY.
24. Haft, D. H., B. J. Loftus, D. L. Richardson, F. Yang, J. A. Eisen, I. T. Paulsen, and O. White. 2001. TIGRFAMs: a protein family resource for the functional identification of proteins. Nucleic Acids Res. 29:41-43.
25. Hall, R. M., D. E. Brookes, and H. W. Stokes. 1991. Site-specific insertion of genes into integrons: role of the 59-base element and determination of the recombination cross-over point. Mol. Microbiol. 15:1941-1959.
26. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
27. Hansson, K., L. Sundström, A. Pelletier, and P. H. Roy. 2002. IntI2 integron integrase in Tn7. J. Bacteriol. 184:1712-1721.
28. Hardwick, S. A., H. W. Stokes, S. Findlay, M. Taylor, and M. R. Gillings. 2008. Quantification of class 1 integron abundance in natural environments using real-time quantitative PCR. FEMS Microbiol. Lett. 278:207-212.
29. Holben, W. E., and D. Harris. 1995. DNA-based monitoring of total bacterial community structure in environmental samples. Mol. Ecol. 4:627-631.
30. Holben, W. E., K. P. Feris, A. Kettunen, and J. H. A. Apajalahti. 2004. GC fractionation enhances microbial community diversity assessment and detection of minority populations of bacteria by denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 70:2263-2270.
31. Holmes, A. J., M. P. Holley, A. Mahon, B. Nield, M. Gillings, and H. W. Stokes. 2003. Recombination activity of a distinctive integron-gene cassette system associated with Pseudomonas stutzeri populations in soil. J. Bacteriol. 185:918-928.
32. Janssen, P. H. 2006. Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl. Environ. Microbiol. 72:1719-1728.
33. Leser, T. D., J. Z. Amenuvor, T. K. Jensen, R. H. Lindecrona, M. Boye, and K. Møller. 2002. Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl. Environ. Microbiol. 68:673-690.
34. Leung, K., and E. Topp. 2001. Bacterial community dynamics in liquid swine manure during storage: molecular analysis using DGGE/PCR of 16S rDNA. FEMS Microbiol. Ecol. 38:169-177.
35. Ley, R. E., P. J. Turnbaugh, S. Klein, and J. I. Gordon. 2006. Microbial ecology: human gut microbes associated with obesity. Nature 444:1022-1023.
36. Lick, S., K. Drescher, and K. J. Heller. 2001. Survival of Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus thermophilus in the terminal ileum of fistulated Göttingen minipigs. Appl. Environ. Microbiol. 67:4137-4143.
37. Lu, J., S. Sanchez, C. Hofacre, J. J. Maurer, B. G. Harmon, and M. D. Lee. 2003. Evaluation of broiler litter with reference to the microbial composition as assessed by using 16S rRNA and functional gene markers. Appl. Environ. Microbiol. 69:901-908.
38. MacDonald, D., G. Demarre, M. Bouvier, D. Mazel, and D. N. Gopaul. 2006. Structural basis for broad DNA-specificity in integron recombination. Nature 440:1157-1162.
39. Marchler-Bauer, A., and S. H. Bryant. 2004. CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 32:W327-W331.
40. Márquez, C., M. Labbate, A. J. Ingold, P. R. Chowdhury, M. S. Ramírez, D. Centrón, G. Borthagaray, and H. W. Stokes. 2008. Recovery of a functional class 2 integron from an Escherichia coli strain mediating a urinary tract infection. Antimicrob. Agents Chemother. 52:4153-4154.
41. Mater, D. D., L. Bretigny, O. Firmesse, M. J. Flores, A. Mogenet, J. L. Bresson, and G. Corthier. 2005. Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus survive gastrointestinal transit of healthy volunteers consuming yogurt. FEMS Microbiol. Lett. 250:185-187.
42. Mazel, D. 2006. Integrons: agents of bacterial evolution. Nat. Rev. Microbiol. 4:608-620.
43. Mazel, D., B. Dychinco, V. A. Webb, and J. Davies. 1998. A distinctive class of integron in the Vibrio cholerae genome. Science 280:605-608.
44. Messier, N., and P. H. Roy. 2001. Integron integrases possess a unique additional domain necessary for activity. J. Bacteriol. 183:6699-6706.
45. Michael, C. A., M. R. Gillings, A. J. Holmes, L. Hughes, N. R. Andrew, M. P. Holley, and H. W. Stokes. 2004. Mobile gene cassettes: a fundamental resource for bacterial evolution. Am. Nat. 164:1-12.
46. Moura, A., I. Henriques, R. Ribeiro, and A. Correia. 2007. Prevalence and characterization of integrons from bacteria isolated from a slaughterhouse wastewater treatment plant. J. Antimicrob. Chemother. 60:1243-1250.
47. Moura, A., M. Soares, C. Pereira, N. Leitão, I. Henriques, and A. Correia. 2009. INTEGRALL: a database and search engine for integrons, integrases and gene cassettes. Bioinformatics 25:1096-1098.
48. Nandi, S., J. J. Maurer, C. Hofacre, and A. O. Summers. 2004. Gram-positive bacteria are a major reservoir of class 1 antibiotic resistance integrons in poultry litter. Proc. Natl. Acad. Sci. USA 101:7118-7122.
49. Nemergut, D. R., A. P. Martin, and S. K. Schmidt. 2004. Integron diversity in heavy-metal-contaminated mine tailings and inferences about integron evolution. Appl. Environ. Microbiol. 70:1160-1168.
50. Nemergut, D. R., M. S. Robeson, R. F. Kysela, A. P. Martin, S. K. Schmidt, and R. Knight. 2008. Insights and inferences about integron evolution from genomic data. BMC Genomics 9:261.
51. Nield, B. S., A. J. Holmes, M. R. Gillings, G. D. Recchia, B. C. Mabbutt, K. M. Nevalainen, and H. W. Stokes. 2001. Recovery of new integron classes from environmental DNA. FEMS Microbiol. Lett. 195:59-65.
52. Nunes-Düby, S. E., H. J. Kwon, R. S. Tirumalai, T. Ellenberger, and A. Landy. 1998. Similarities and differences among 105 members of the Int family of site-specific recombinases. Nucleic Acids Res. 26:391-406.
53. Nüsslein, K., and J. M. Tiedje. 1998. Characterization of the dominant and rare members of a young Hawaiian soil bacterial community with small-subunit ribosomal DNA amplified from DNA fractionated on the basis of its guanine and cytosine composition. Appl. Environ. Microbiol. 64:1283-1289.
54. Nüsslein, K., and J. M. Tiedje. 1999. Soil bacterial community shift correlated with change from forest to pasture vegetation in a tropical soil. Appl. Environ. Microbiol. 65:3622-3626.
55. Partridge, S. R., G. D. Recchia, C. Scaramuzzi, C. M. Collis, H. W. Stokes, and R. M. Hall. 2000. Definition of the attI1 site of class 1 integrons. Microbiology 146:2855-2864.
56. Ramírez, M. S., C. Quiroga, and D. Centrón. 2005. Novel rearrangement of a class 2 integron in two non-epidemiologically related isolates of Acinetobacter baumanni. Antimicrob. Agents Chemother. 49:5179-5181.
57. Ramírez, M. S., L. J. Vargas, V. Cagnoni, M. Tokumoto, and D. Centrón. 2005. Class 2 integron with a novel cassette array in a Burkholderia cenocepacia isolate. Antimicrob. Agents Chemother. 49:4418-4420.
58. Rowe-Magnus, D. A., A. M. Guerout, and D. Mazel. 2002. Bacterial resistance evolution by recruitment of super-integron gene cassettes. Mol. Microbiol. 43:1657-1669.
59. Rowe-Magnus, D. A., and D. Mazel. 2001. Integrons: natural tools for bacterial genome evolution. Curr. Opin. Microbiol. 4:565-569.
60. Salyers, A. A., A. Gupta, and Y. Wang. 2004. Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol. 12:412-416.
61. Schmieger, H., and P. Schicklmaier. 1999. Transduction of multiple drug resistance of Salmonella enterica serovar typhimurium DT104. FEMS Microbiol. Lett. 170:251-256.
62. Shoemaker, N. B., H. Vlamakis, K. Hayes, and A. A. Salyers. 2001. Evidence for extensive resistance gene transfer among Bacteroides spp. and among Bacteroides and other genera in the human colon. Appl. Environ. Microbiol. 67:561-568.
63. Snell-Castro, R., J. J. Godon, J. P. Delgenès, and P. Dabert. 2005. Characterisation of the microbial diversity in a pig manure storage pit using small subunit rDNA sequence analysis. FEMS Microbiol. Ecol. 52:229-242.
64. Stokes, H. W., and R. M. Hall. 1989. A novel family of potentially mobile DNA elements encoding site-specific gene-integration functions: integrons. Mol. Microbiol. 3:1669-1683.
65. Stokes, H. W., C. L. Nesbø, M. Holley, M. I. Bahl, M. R. Gillings, and Y. Boucher. 2006. Class 1 integrons potentially predating the association with Tn402-like transposition genes are present in a sediment microbial community. J. Bacteriol. 188:5722-5730.
66. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
67. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24:4876-4882.
68. Vandamme, P., B. Pot, M. Gillis, P. de Vos, K. Kersters, and J. Swings. 1996. Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol. Rev. 60:407-438.
69. White, P. A., C. J. McIver, Y. Deng, and W. D. Rawlinson. 2000. Characterisation of two new gene cassettes, aadA5 and dfrA17. FEMS Microbiol. Lett. 182:265-269.
70. Wright, M. S., C. Baker-Austin, A. H. Lindell, R. Stepanauskas, H. W. Stokes, and J. V. McArthur. 2008. Influence of industrial contamination on mobile genetic elements: class 1 integron abundance and gene cassette structure in aquatic bacterial communities. ISME J. 2:417-428
71. Xu, H., J. Davies, and V. Miao. 2007. Molecular characterization of class 3 integrons from Delftia spp. J. Bacteriol. 17:6276-6283.
72. Zhou, J., M. A. Bruns, and J. M. Tiedje. 1996. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62:316-322.