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BioMed Research International
Volume 2014 (2014), Article ID 290967, 9 pages
http://dx.doi.org/10.1155/2014/290967
Research Article

Functional Screening of Antibiotic Resistance Genes from a Representative Metagenomic Library of Food Fermenting Microbiota

1CRA-NUT, Food & Nutrition Research Center, Agricultural Research Council, Via Ardeatina 546, 00178 Rome, Italy
2Department of Biology and Biotechnology Charles Darwin, Sapienza University of Rome, Piazzale Aldo Moro 5, 00185 Rome, Italy

Received 9 July 2014; Accepted 7 August 2014; Published 28 August 2014

Academic Editor: María Fernández

Copyright © 2014 Chiara Devirgiliis et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. B. Hansen, “Commercial bacterial starter cultures for fermented foods of the future,” International Journal of Food Microbiology, vol. 78, no. 1-2, pp. 119–131, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. W. R. Streit and R. A. Schmitz, “Metagenomic—the key to the uncultured microbes,” Current Opinion in Microbiology, vol. 7, no. 5, pp. 492–498, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. R. I. Amann, W. Ludwig, and K.-. Schleifer, “Phylogenetic identification and in situ detection of individual microbial cells without cultivation,” Microbiological Reviews, vol. 59, no. 1, pp. 143–169, 1995. View at Google Scholar · View at Scopus
  4. T. S. Lusk, A. R. Ottesen, J. R. White, M. W. Allard, E. W. Brown, and J. A. Kase, “Characterization of microflora in Latin-style cheeses by next-generation sequencing technology,” BMC Microbiology, vol. 12, article 254, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. K. M. Tuohy, C. Gougoulias, Q. Shen, G. Walton, F. Fava, and P. Ramnani, “Studying the human gut microbiota in the trans-omics era—focus on metagenomics and metabonomics,” Current Pharmaceutical Design, vol. 15, no. 13, pp. 1415–1427, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. D. Ercolini, “High-throughput sequencing and metagenomics: Moving forward in the culture-independent analysis of food microbial ecology,” Applied and Environmental Microbiology, vol. 79, no. 10, pp. 3148–3155, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. S. A. F. T. van Hijum, E. E. Vaughan, and R. F. Vogel, “Application of state-of-art sequencing technologies to indigenous food fermentations,” Current Opinion in Biotechnology, vol. 24, no. 2, pp. 178–186, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Devirgiliis, S. Barile, and G. Perozzi, “Antibiotic resistance determinants in the interplay between food and gut microbiota,” Genes and Nutrition, vol. 6, no. 3, pp. 275–284, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. C. Devirgiliis, D. Coppola, S. Barile, B. Colonna, and G. Perozzi, “Characterization of the Tn916 conjugative transposon in a food-borne strain of Lactobacillus paracasei,” Applied and Environmental Microbiology, vol. 75, no. 12, pp. 3866–3871, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. L. M. Durso, D. N. Miller, and B. J. Wienhold, “Distribution and quantification of antibiotic resistant genes and bacteria across agricultural and non-agricultural metagenomes,” PLoS ONE, vol. 7, no. 11, Article ID e48325, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. F. Rossi, L. Rizzotti, G. E. Felis, and S. Torriani, “Horizontal gene transfer among microorganisms in food: current knowledge and future perspectives,” Food Microbiology, vol. 42, pp. 232–243, 2014. View at Publisher · View at Google Scholar
  12. D. Ercolini, G. Moschetti, G. Blaiotta, and S. Coppola, “The potential of a polyphasic PCR-DGGE approach in evaluating microbial diversity of natural whey cultures for water-buffalo Mozzarella cheese production: bias of culture-dependent and culture-independent analyses,” Systematic and Applied Microbiology, vol. 24, no. 4, pp. 610–617, 2001. View at Publisher · View at Google Scholar · View at Scopus
  13. C. Devirgiliis, A. Caravelli, D. Coppola, S. Barile, and G. Perozzi, “Antibiotic resistance and microbial composition along the manufacturing process of Mozzarella di Bufala Campana,” International Journal of Food Microbiology, vol. 128, no. 2, pp. 378–384, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Ercolini, F. de Filippis, A. La Storia, and M. Iacono, ““Remake” by high-throughput sequencing of the microbiota involved in the production of water Buffalo mozzarella cheese,” Applied and Environmental Microbiology, vol. 78, no. 22, pp. 8142–8145, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. M. L. Diaz-Torres, A. Villedieu, N. Hunt et al., “Determining the antibiotic resistance potential of the indigenous oral microbiota of humans using ametagenomic approach,” FEMS Microbiology Letters, vol. 258, no. 2, pp. 257–262, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. J. H. A. Apajalahti, L. K. Särkilahti, B. R. E. Mäki, J. Pekka Heikkinen, P. H. Nurminen, and W. E. Holben, “Effective recovery of bacterial DNA and percent-guanine-plus-cytosine- based analysis of community structure in the gastrointestinal tract of broiler chickens,” Applied and Environmental Microbiology, vol. 64, no. 10, pp. 4084–4088, 1998. View at Google Scholar · View at Scopus
  17. M. Pilhofer, A. P. Bauer, M. Schrallhammer et al., “Characterization of bacterial operons consisting of two tubulins and a kinesin-like gene by the novel Two-Step Gene Walking method,” Nucleic Acids Research, vol. 35, no. 20, article e135, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Barile, C. Devirgiliis, and G. Perozzi, “Molecular characterization of a novel mosaic tet(S/M) gene encoding tetracycline resistance in foodborne strains of Streptococcus bovis,” Microbiology, vol. 158, no. 9, pp. 2353–2362, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. G. Churchward, “Conjugative transposons and related mobile elements,” in Mobile DNA II, N. Craig, R. Craigie, and M. Gellert, Eds., ASM Press, Washington, DC, USA, 2002. View at Google Scholar
  20. G. Dantas, M. O. Sommer, P. H. Degnan, and A. L. Goodman, “Experimental approaches for defining functional roles of microbes in the human gut,” Annual Review of Microbiology, vol. 67, pp. 459–475, 2013. View at Publisher · View at Google Scholar
  21. T. C. Hazen, A. M. Rocha, and S. M. Techtmann, “Advances in monitoring environmental microbes,” Current Opinion in Biotechnology, vol. 24, no. 3, pp. 526–533, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. E. C. Pehrsson, K. J. Forsberg, M. K. Gibson, S. Ahmadi, and G. Dantas, “Novel resistance functions uncovered using functional metagenomic investigations of resistance reservoirs,” Frontiers in Microbiology, vol. 4, article 145, 2013. View at Publisher · View at Google Scholar
  23. C. Devirgiliis, P. Zinno, and G. Perozzi, “pdate on antibiotic resistance in foodborne and species,” Frontiers in Microbiology, vol. 4, p. 301, 2013. View at Google Scholar
  24. F. Clementi and L. Aquilanti, “Recent investigations and updated criteria for the assessment of antibiotic resistance in food lactic acid bacteria,” Anaerobe, vol. 17, no. 6, pp. 394–398, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. M. S. Ammor, A. B. Flórez, and B. Mayo, “Antibiotic resistance in non-enterococcal lactic acid bacteria and bifidobacteria,” Food Microbiology, vol. 24, no. 6, pp. 559–570, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. R. Comunian, E. Daga, I. Dupré et al., “Susceptibility to tetracycline and erythromycin of Lactobacillus paracasei strains isolated from traditional Italian fermented foods,” International Journal of Food Microbiology, vol. 138, no. 1-2, pp. 151–156, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Nawaz, J. Wang, A. Zhou et al., “Characterization and transfer of antibiotic resistance in lactic acid bacteria from fermented food products,” Current Microbiology, vol. 62, no. 3, pp. 1081–1089, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. A. B. Flórez, P. Reimundo, S. Delgado et al., “Genome sequence of Lactococcus garvieae IPLA 31405, a bacteriocin-producing, tetracycline-resistant strain isolated from a raw-milk cheese,” Journal of Bacteriology, vol. 194, no. 18, pp. 5118–5119, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. L. Feld, E. Bielak, K. Hammer, and A. Wilcks, “Characterization of a small erythromycin resistance plasmid pLFE1 from the food-isolate Lactobacillus plantarum M345,” Plasmid, vol. 61, no. 3, pp. 159–170, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. E. López and J. Blázquez, “Effect of subinhibitory concentrations of antibiotics on intrachromosomal homologous recombination in Escherichia coli,” Antimicrobial Agents and Chemotherapy, vol. 53, no. 8, pp. 3411–3415, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Zervosen, E. Sauvage, J. Frère, P. Charlier, and A. Luxen, “Development of new drugs for an old target—the penicillin binding proteins,” Molecules, vol. 17, no. 11, pp. 12478–12505, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. K. Poole, “Resistance to β-lactam antibiotics,” Cellular and Molecular Life Sciences, vol. 61, no. 17, pp. 2200–2223, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. I. Moric, M. Savić, T. Ilić-Tomić et al., “rRNA Methyltransferases and their role in resistance to antibiotics,” Journal of Medical Biochemistry, vol. 29, pp. 165–174, 2010. View at Google Scholar
  34. K. S. Long, J. Poehlsgaard, C. Kehrenberg, S. Schwarz, and B. Vester, “The Cfr rRNA methyltransferase confers resistance to phenicols, lincosamides, oxazolidinones, pleuromutilins, and streptogramin A antibiotics,” Antimicrobial Agents and Chemotherapy, vol. 50, no. 7, pp. 2500–2505, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. M. W. Vetting, L. P. S. de Carvalho, M. Yu et al., “Structure and functions of the GNAT superfamily of acetyltransferases,” Archives of Biochemistry and Biophysics, vol. 433, no. 1, pp. 212–226, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. L. P. Tripathi and R. Sowdhamini, “Genome-wide survey of prokaryotic serine proteases: Analysis of distribution and domain architectures of five serine protease families in prokaryotes,” BMC Genomics, vol. 9, article 549, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. B. G. Hall and M. Barlow, “Evolution of the serine β-lactamases: past, present and future,” Drug Resistance Updates, vol. 7, no. 2, pp. 111–123, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. R. Mehra-Chaudhary, J. Mick, J. J. Tanner, M. T. Henzl, and L. J. Beamer, “Crystal structure of a bacterial phosphoglucomutase, an enzyme involved in the virulence of multiple human pathogens,” Proteins, vol. 79, no. 4, pp. 1215–1229, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. G. K. Paterson, D. B. Cone, S. E. Peters, and D. J. Maskell, “The enzyme phosphoglucomutase (Pgm) is required by Salmonella enterica serovar Typhimurium for O-antigen production, resistance to antimicrobial peptides and in vivo fitness,” Microbiology, vol. 155, no. 10, pp. 3403–3410, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. G. A. McKay, D. E. Woods, K. L. MacDonald, and K. Poole, “Role of phosphoglucomutase of Stenotrophomonas maltophilia in lipopolysaccharide biosynthesis, virulence, and antibiotic resistance,” Infection and Immunity, vol. 71, no. 6, pp. 3068–3075, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Mahillon and M. Chandler, “Insertion sequences,” Microbiology and Molecular Biology Reviews, vol. 62, no. 3, pp. 725–774, 1998. View at Google Scholar · View at Scopus
  42. B. M. Marshall, D. J. Ochieng, and S. B. Levy, “Commensals: underappreciated reservoir of antibiotic resistance,” Microbe, vol. 4, no. 5, pp. 231–238, 2009. View at Google Scholar · View at Scopus
  43. L. A. Old and R. R. B. Russell, “Distribution and activity of IS elements in Streptococcus mutans,” FEMS Microbiology Letters, vol. 287, no. 2, pp. 199–204, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. V. Martins dos Santos, M. Müller, and W. M. de Vos, “Systems biology of the gut: the interplay of food, microbiota and host at the mucosal interface,” Current Opinion in Biotechnology, vol. 21, no. 4, pp. 539–550, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nature Methods, vol. 9, no. 7, pp. 671–675, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. F. di Cello and R. Fani, “A molecular strategy for the study of natural bacterial communities by PCR-based techniques,” Minerva Biotecnologica, vol. 8, no. 3, pp. 126–134, 1996. View at Google Scholar · View at Scopus
  47. J. H. Calvo, R. Osta, and P. Zaragoza, “Quantitative PCR detection of pork in raw and heated ground beef and pâté,” Journal of Agricultural and Food Chemistry, vol. 50, no. 19, pp. 5265–5267, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. S.I. Fujita, Y. Senda, S. Nakaguchi, and T. Hashimoto, “Multiplex PCR using internal transcribed spacer 1 and 2 regions for rapid detection and identification of yeast strains,” Journal of Clinical Microbiology, vol. 39, no. 10, pp. 3617–3622, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. R. M. Lopparelli, B. Cardazzo, S. Balzan, V. Giaccone, and E. Novelli, “Real-time TaqMan polymerase chain reaction detection and quantification of cow DNA in pure water buffalo mozzarella cheese: method validation and its application on commercial samples,” Journal of Agricultural and Food Chemistry, vol. 55, no. 9, pp. 3429–3434, 2007. View at Publisher · View at Google Scholar · View at Scopus