This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Shoemaker, N. B.
Right arrow Articles by Salyers, A. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Shoemaker, N. B.
Right arrow Articles by Salyers, A. A.
Agricola
Right arrow Articles by Shoemaker, N. B.
Right arrow Articles by Salyers, A. A.

 Previous Article  |  Next Article 

Applied and Environmental Microbiology, February 2001, p. 561-568, Vol. 67, No. 2
0099-2240/01/$04.00+0   DOI: 10.1128/AEM.67.2.561-568.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Evidence for Extensive Resistance Gene Transfer among Bacteroides spp. and among Bacteroides and Other Genera in the Human Colon

N. B. Shoemaker, H. Vlamakis, K. Hayes, and A. A. Salyers*

Department of Microbiology, University of Illinois, Urbana, Illinois 61801

Received Recieved 20 September 2000/Accepted 7 November 2000

Transfer of antibiotic resistance genes by conjugation is thought to play an important role in the spread of resistance. Yet virtually no information is available about the extent to which such horizontal transfers occur in natural settings. In this paper, we show that conjugal gene transfer has made a major contribution to increased antibiotic resistance in Bacteroides species, a numerically predominant group of human colonic bacteria. Over the past 3 decades, carriage of the tetracycline resistance gene, tetQ, has increased from about 30% to more than 80% of strains. Alleles of tetQ in different Bacteroides species, with one exception, were 96 to 100% identical at the DNA sequence level, as expected if horizontal gene transfer was responsible for their spread. Southern blot analyses showed further that transfer of tetQ was mediated by a conjugative transposon (CTn) of the CTnDOT type. Carriage of two erythromycin resistance genes, ermF and ermG, rose from <2 to 23% and accounted for about 70% of the total erythromycin resistances observed. Carriage of tetQ and the erm genes was the same in isolates taken from healthy people with no recent history of antibiotic use as in isolates obtained from patients with Bacteroides infections. This finding indicates that resistance transfer is occurring in the community and not just in clinical environments. The high percentage of strains that are carrying these resistance genes in people who are not taking antibiotics is consistent with the hypothesis that once acquired, these resistance genes are stably maintained in the absence of antibiotic selection. Six recently isolated strains carried ermB genes. Two were identical to erm(B)-P from Clostridium perfringens, and the other four had only one to three mismatches. The nine strains with ermG genes had DNA sequences that were more than 99% identical to the ermG of Bacillus sphaericus. Evidently, there is a genetic conduit open between gram-positive bacteria, including bacteria that only pass through the human colon, and the gram-negative Bacteroides species. Our results support the hypothesis that extensive gene transfer occurs among bacteria in the human colon, both within the genus Bacteroides and among Bacteroides species and gram-positive bacteria.

* Corresponding author. Mailing address: Department of Microbiology---UIUC, B103 CLSL, 601 South Goodwin Ave., Urbana, IL 61801. Phone: (217) 333-7378. Fax: (217) 244-8485. E-mail: abigails{at}life.uiuc.edu.

Applied and Environmental Microbiology, February 2001, p. 561-568, Vol. 67, No. 2
0099-2240/01/$04.00+0   DOI: 10.1128/AEM.67.2.561-568.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Jeters, R. T., Wang, G.-R., Moon, K., Shoemaker, N. B., Salyers, A. A. (2009). Tetracycline-Associated Transcriptional Regulation of Transfer Genes of the Bacteroides Conjugative Transposon CTnDOT. J. Bacteriol. 191: 6374-6382 [Abstract] [Full Text]  
  • Sommer, M. O. A., Dantas, G., Church, G. M. (2009). Functional Characterization of the Antibiotic Resistance Reservoir in the Human Microflora. Science 325: 1128-1131 [Abstract] [Full Text]  
  • Rodriguez-Minguela, C. M., Apajalahti, J. H. A., Chai, B., Cole, J. R., Tiedje, J. M. (2009). Worldwide Prevalence of Class 2 Integrases outside the Clinical Setting Is Associated with Human Impact. Appl. Environ. Microbiol. 75: 5100-5110 [Abstract] [Full Text]  
  • Chee-Sanford, J. C., Mackie, R. I., Koike, S., Krapac, I. G., Lin, Y.-F., Yannarell, A. C., Maxwell, S., Aminov, R. I. (2009). Fate and Transport of Antibiotic Residues and Antibiotic Resistance Genes following Land Application of Manure Waste. J. Environ. Qual. 38: 1086-1108 [Abstract] [Full Text]  
  • Song, B., Wang, G.-R., Shoemaker, N. B., Salyers, A. A. (2009). An Unexpected Effect of Tetracycline Concentration: Growth Phase-Associated Excision of the Bacteroides Mobilizable Transposon NBU1. J. Bacteriol. 191: 1078-1082 [Abstract] [Full Text]  
  • Hunter, P. R., Wilkinson, D. C., Catling, L. A., Barker, G. C. (2008). Meta-Analysis of Experimental Data Concerning Antimicrobial Resistance Gene Transfer Rates during Conjugation. Appl. Environ. Microbiol. 74: 6085-6090 [Abstract] [Full Text]  
  • Scott, K. P., Martin, J. C., Mrazek, J., Flint, H. J. (2008). Transfer of Conjugative Elements from Rumen and Human Firmicutes Bacteria to Roseburia inulinivorans. Appl. Environ. Microbiol. 74: 3915-3917 [Abstract] [Full Text]  
  • Macovei, L., Zurek, L. (2007). Influx of Enterococci and Associated Antibiotic Resistance and Virulence Genes from Ready-To-Eat Food to the Human Digestive Tract. Appl. Environ. Microbiol. 73: 6740-6747 [Abstract] [Full Text]  
  • Wexler, H. M. (2007). Bacteroides: the Good, the Bad, and the Nitty-Gritty. Clin. Microbiol. Rev. 20: 593-621 [Abstract] [Full Text]  
  • Malanowska, K., Yoneji, S., Salyers, A. A., Gardner, J. F. (2007). CTnDOT integrase performs ordered homology-dependent and homology-independent strand exchanges. Nucleic Acids Res 35: 5861-5873 [Abstract] [Full Text]  
  • Munoz-Aguayo, J., Lang, K. S., LaPara, T. M., Gonzalez, G., Singer, R. S. (2007). Evaluating the Effects of Chlortetracycline on the Proliferation of Antibiotic-Resistant Bacteria in a Simulated River Water Ecosystem. Appl. Environ. Microbiol. 73: 5421-5425 [Abstract] [Full Text]  
  • Schlesinger, D. J., Shoemaker, N. B., Salyers, A. A. (2007). Possible Origins of CTnBST, a Conjugative Transposon Found Recently in a Human Colonic Bacteroides Strain. Appl. Environ. Microbiol. 73: 4226-4233 [Abstract] [Full Text]  
  • Dahl, K. H., Mater, D. D. G., Flores, M. J., Johnsen, P. J., Midtvedt, T., Corthier, G., Sundsfjord, A. (2007). Transfer of plasmid and chromosomal glycopeptide resistance determinants occurs more readily in the digestive tract of mice than in vitro and exconjugants can persist stably in vivo in the absence of glycopeptide selection. J Antimicrob Chemother 59: 478-486 [Abstract] [Full Text]  
  • Hawkyard, C. V., Koerner, R. J. (2007). The use of erythromycin as a gastrointestinal prokinetic agent in adult critical care: benefits versus risks. J Antimicrob Chemother 59: 347-358 [Abstract] [Full Text]  
  • Wesslund, N. A., Wang, G.-R., Song, B., Shoemaker, N. B., Salyers, A. A. (2007). Integration and Excision of a Newly Discovered Bacteroides Conjugative Transposon, CTnBST. J. Bacteriol. 189: 1072-1082 [Abstract] [Full Text]  
  • Lofmark, S., Jernberg, C., Jansson, J. K., Edlund, C. (2006). Clindamycin-induced enrichment and long-term persistence of resistant Bacteroides spp. and resistance genes. J Antimicrob Chemother 58: 1160-1167 [Abstract] [Full Text]  
  • Khachatryan, A. R., Besser, T. E., Hancock, D. D., Call, D. R. (2006). Use of a Nonmedicated Dietary Supplement Correlates with Increased Prevalence of Streptomycin-Sulfa-Tetracycline-Resistant Escherichia coli on a Dairy Farm.. Appl. Environ. Microbiol. 72: 4583-4588 [Abstract] [Full Text]  
  • Liebana, E., Batchelor, M., Hopkins, K. L., Clifton-Hadley, F. A., Teale, C. J., Foster, A., Barker, L., Threlfall, E. J., Davies, R. H. (2006). Longitudinal Farm Study of Extended-Spectrum {beta}-Lactamase-Mediated Resistance.. J. Clin. Microbiol. 44: 1630-1634 [Abstract] [Full Text]  
  • Rocco, J. M., Churchward, G. (2006). The Integrase of the Conjugative Transposon Tn916 Directs Strand- and Sequence-Specific Cleavage of the Origin of Conjugal Transfer, oriT, by the Endonuclease Orf20. J. Bacteriol. 188: 2207-2213 [Abstract] [Full Text]  
  • Van der Meulen, R., Makras, L., Verbrugghe, K., Adriany, T., De Vuyst, L. (2006). In Vitro Kinetic Analysis of Oligofructose Consumption by Bacteroides and Bifidobacterium spp. Indicates Different Degradation Mechanisms. Appl. Environ. Microbiol. 72: 1006-1012 [Abstract] [Full Text]  
  • Khachatryan, A. R., Hancock, D. D., Besser, T. E., Call, D. R. (2006). Antimicrobial Drug Resistance Genes Do Not Convey a Secondary Fitness Advantage to Calf-Adapted Escherichia coli. Appl. Environ. Microbiol. 72: 443-448 [Abstract] [Full Text]  
  • Agerso, Y., Sandvang, D. (2005). Class 1 Integrons and Tetracycline Resistance Genes in Alcaligenes, Arthrobacter, and Pseudomonas spp. Isolated from Pigsties and Manured Soil. Appl. Environ. Microbiol. 71: 7941-7947 [Abstract] [Full Text]  
  • Kumar, K., Gupta, S. C., Baidoo, S. K., Chander, Y., Rosen, C. J. (2005). Antibiotic Uptake by Plants from Soil Fertilized with Animal Manure. J. Environ. Qual. 34: 2082-2085 [Abstract] [Full Text]  
  • Moon, K., Shoemaker, N. B., Gardner, J. F., Salyers, A. A. (2005). Regulation of Excision Genes of the Bacteroides Conjugative Transposon CTnDOT. J. Bacteriol. 187: 5732-5741 [Abstract] [Full Text]  
  • Wang, Y., Wang, G.-R., Shoemaker, N. B., Whitehead, T. R., Salyers, A. A. (2005). Distribution of the ermG Gene among Bacterial Isolates from Porcine Intestinal Contents. Appl. Environ. Microbiol. 71: 4930-4934 [Abstract] [Full Text]  
  • Magee, J. T., Heginbothom, M. L., Mason, B. W. (2005). Finding a strategy: the case for co-operative research on resistance epidemiology. J Antimicrob Chemother 55: 628-633 [Abstract] [Full Text]  
  • Wang, Y., Rotman, E. R., Shoemaker, N. B., Salyers, A. A. (2005). Translational Control of Tetracycline Resistance and Conjugation in the Bacteroides Conjugative Transposon CTnDOT. J. Bacteriol. 187: 2673-2680 [Abstract] [Full Text]  
  • Bacic, M., Parker, A. C., Stagg, J., Whitley, H. P., Wells, W. G., Jacob, L. A., Smith, C. J. (2005). Genetic and Structural Analysis of the Bacteroides Conjugative Transposon CTn341. J. Bacteriol. 187: 2858-2869 [Abstract] [Full Text]  
  • Domingo, M.-C., Huletsky, A., Bernal, A., Giroux, R., Boudreau, D. K., Picard, F. J., Bergeron, M. G. (2005). Characterization of a Tn5382-like transposon containing the vanB2 gene cluster in a Clostridium strain isolated from human faeces. J Antimicrob Chemother 55: 466-474 [Abstract] [Full Text]  
  • Lofmark, S., Fang, H., Hedberg, M., Edlund, C. (2005). Inducible Metronidazole Resistance and nim Genes in Clinical Bacteroides fragilis Group Isolates. Antimicrob. Agents Chemother. 49: 1253-1256 [Abstract] [Full Text]  
  • Barbosa, T. M., Serra, C. R., La Ragione, R. M., Woodward, M. J., Henriques, A. O. (2005). Screening for Bacillus Isolates in the Broiler Gastrointestinal Tract. Appl. Environ. Microbiol. 71: 968-978 [Abstract] [Full Text]  
  • Stanton, T. B., McDowall, J. S., Rasmussen, M. A. (2004). Diverse Tetracycline Resistance Genotypes of Megasphaera elsdenii Strains Selectively Cultured from Swine Feces. Appl. Environ. Microbiol. 70: 3754-3757 [Abstract] [Full Text]  
  • Khachatryan, A. R., Hancock, D. D., Besser, T. E., Call, D. R. (2004). Role of Calf-Adapted Escherichia coli in Maintenance of Antimicrobial Drug Resistance in Dairy Calves. Appl. Environ. Microbiol. 70: 752-757 [Abstract] [Full Text]  
  • Parker, A. C., Smith, C. J. (2004). A Multicomponent System Is Required for Tetracycline-Induced Excision of Tn4555. J. Bacteriol. 186: 438-444 [Abstract] [Full Text]  
  • Gupta, A., Vlamakis, H., Shoemaker, N., Salyers, A. A. (2003). A New Bacteroides Conjugative Transposon That Carries an ermB Gene. Appl. Environ. Microbiol. 69: 6455-6463 [Abstract] [Full Text]  
  • Sjolund, M., Wreiber, K., Andersson, D. I., Blaser, M. J., Engstrand, L. (2003). Long-Term Persistence of Resistant Enterococcus Species after Antibiotics To Eradicate Helicobacter pylori. ANN INTERN MED 139: 483-487 [Abstract] [Full Text]  
  • Wang, Y., Wang, G.-R., Shelby, A., Shoemaker, N. B., Salyers, A. A. (2003). A Newly Discovered Bacteroides Conjugative Transposon, CTnGERM1, Contains Genes Also Found in Gram-Positive Bacteria. Appl. Environ. Microbiol. 69: 4595-4603 [Abstract] [Full Text]  
  • Johnson, J. R., Murray, A. C., Gajewski, A., Sullivan, M., Snippes, P., Kuskowski, M. A., Smith, K. E. (2003). Isolation and Molecular Characterization of Nalidixic Acid-Resistant Extraintestinal Pathogenic Escherichia coli from Retail Chicken Products. Antimicrob. Agents Chemother. 47: 2161-2168 [Abstract] [Full Text]  
  • Whittle, G., Whitehead, T. R., Hamburger, N., Shoemaker, N. B., Cotta, M. A., Salyers, A. A. (2003). Identification of a New Ribosomal Protection Type of Tetracycline Resistance Gene, tet(36), from Swine Manure Pits. Appl. Environ. Microbiol. 69: 4151-4158 [Abstract] [Full Text]  
  • Diaz-Torres, M. L., McNab, R., Spratt, D. A., Villedieu, A., Hunt, N., Wilson, M., Mullany, P. (2003). Novel Tetracycline Resistance Determinant from the Oral Metagenome. Antimicrob. Agents Chemother. 47: 1430-1432 [Abstract] [Full Text]  
  • Xu, J., Bjursell, M. K., Himrod, J., Deng, S., Carmichael, L. K., Chiang, H. C., Hooper, L. V., Gordon, J. I. (2003). A Genomic View of the Human-Bacteroides thetaiotaomicron Symbiosis. Science 299: 2074-2076 [Abstract] [Full Text]  
  • Villedieu, A., Diaz-Torres, M. L., Hunt, N., McNab, R., Spratt, D. A., Wilson, M., Mullany, P. (2003). Prevalence of Tetracycline Resistance Genes in Oral Bacteria. Antimicrob. Agents Chemother. 47: 878-882 [Abstract] [Full Text]  
  • Cheng, Q., Wesslund, N., Shoemaker, N. B., Salyers, A. A., Gardner, J. F. (2002). Development of an In Vitro Integration Assay for the Bacteroides Conjugative Transposon CTnDOT. J. Bacteriol. 184: 4829-4837 [Abstract] [Full Text]  
  • Whittle, G., Shoemaker, N. B., Salyers, A. A. (2002). Characterization of Genes Involved in Modulation of Conjugal Transfer of the Bacteroides Conjugative Transposon CTnDOT. J. Bacteriol. 184: 3839-3847 [Abstract] [Full Text]  
  • Laich, F., Fierro, F., Martin, J. F. (2002). Production of Penicillin by Fungi Growing on Food Products: Identification of a Complete Penicillin Gene Cluster in Penicillium griseofulvum and a Truncated Cluster in Penicillium verrucosum. Appl. Environ. Microbiol. 68: 1211-1219 [Abstract] [Full Text]  
  • Woegerbauer, M., Jenni, B., Thalhammer, F., Graninger, W., Burgmann, H. (2002). Natural Genetic Transformation of Clinical Isolates of Escherichia coli in Urine and Water. Appl. Environ. Microbiol. 68: 440-443 [Abstract] [Full Text]  
  • Sorensen, T. L., Blom, M., Monnet, D. L., Frimodt-Moller, N., Poulsen, R. L., Espersen, F. (2001). Transient Intestinal Carriage after Ingestion of Antibiotic-Resistant Enterococcus faecium from Chicken and Pork. NEJM 345: 1161-1166 [Abstract] [Full Text]  
  • Gorbach, S. L. (2001). Antimicrobial Use in Animal Feed -- Time to Stop. NEJM 345: 1202-1203 [Full Text]  
  • Whittle, G., Hund, B. D., Shoemaker, N. B., Salyers, A. A. (2001). Characterization of the 13-Kilobase ermF Region of the Bacteroides Conjugative Transposon CTnDOT. Appl. Environ. Microbiol. 67: 3488-3495 [Abstract] [Full Text]  
  • Oppegaard, H., Steinum, T. M., Wasteson, Y. (2001). Horizontal Transfer of a Multi-Drug Resistance Plasmid between Coliform Bacteria of Human and Bovine Origin in a Farm Environment. Appl. Environ. Microbiol. 67: 3732-3734 [Abstract] [Full Text]  
  • Hooper, L. V., Gordon, J. I. (2001). Commensal Host-Bacterial Relationships in the Gut. Science 292: 1115-1118 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»