Table of Contents
International Journal of Antibiotics
Volume 2014 (2014), Article ID 185068, 14 pages
http://dx.doi.org/10.1155/2014/185068
Research Article

Effects of Chlorophyll-Derived Efflux Pump Inhibitor Pheophorbide a and Pyropheophorbide a on Growth and Macrolide Antibiotic Resistance of Indicator and Anaerobic Swine Manure Bacteria

1National Center for Agricultural Utilization Research, ARS, USDA, 1815 N. University Street, Peoria, IL 61604, USA
2Leopold Center for Sustainable Agriculture, 209 Curtiss Hall, Iowa State University, Ames, IA 50011, USA

Received 21 October 2013; Revised 12 December 2013; Accepted 19 December 2013; Published 11 February 2014

Academic Editor: Federico Pea

Copyright © 2014 Mareike Kraatz 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. K. Silbergeld, J. Graham, and L. B. Price, “Industrial food animal production, antimicrobial resistance, and human health,” Annual Review of Public Health, vol. 29, pp. 151–169, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. G. Hansen, “Playing chicken with antibiotics: antibiotic use in food animals,” in Proceedings of the 140th APHA Annual Meeting & Exposition, San Francisco, Calif, USA, 2012.
  3. T. F. Landers, B. Cohen, T. E. Wittum, and E. L. Larson, “A review of antibiotic use in food animals: perspective, policy, and potential,” Public Health Reports, vol. 127, no. 1, pp. 4–22, 2012. View at Google Scholar · View at Scopus
  4. P. M. da Costa, L. Loureiro, and A. J. F. Matos, “Transfer of multidrug-resistant bacteria between intermingled ecological niches: the interface between humans, animals and the environment,” International Journal of Environmental Research and Public Health, vol. 10, pp. 278–294, 2013. View at Google Scholar
  5. M. D. Apley, E. J. Bush, R. B. Morrison, R. S. Singer, and H. Snelson, “Use estimates of in-feed antimicrobials in swine production in the United States,” Foodborne Pathogens and Disease, vol. 9, no. 3, pp. 272–279, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. D. C. Love, M. F. Davis, A. Bassett, A. Gunther, and K. E. Nachman, “Dose imprecision and resistance: free-choice medicated feeds in industrial food animal production in the United States,” Environmental Health Perspectives, vol. 119, no. 3, pp. 279–283, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. F. Baquero, “Low-level antibacterial resistance: a gateway to clinical resistance,” Drug Resistance Updates, vol. 4, no. 2, pp. 93–105, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. D. I. Andersson and D. Hughes, “Persistence of antibiotic resistance in bacterial populations,” FEMS Microbiology Reviews, vol. 35, no. 5, pp. 901–911, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. R. Cantón and M.-I. Morosini, “Emergence and spread of antibiotic resistance following exposure to antibiotics,” FEMS Microbiology Reviews, vol. 35, no. 5, pp. 977–991, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. M. A. van der Horst, J. M. Schuurmans, M. C. Smid, B. B. Koenders, and B. H. ter Kuile, “De novo acquisition of resistance to three antibiotics by escherichia coli,” Microbial Drug Resistance, vol. 17, no. 2, pp. 141–147, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. D. I. Andersson and D. Hughes, “Evolution of antibiotic resistance at non-lethal drug concentrations,” Drug Resistance Updates, vol. 15, pp. 162–172, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. R. Schmieder and R. Edwards, “Insights into antibiotic resistance through metagenomic approaches,” Future Microbiology, vol. 7, no. 1, pp. 73–89, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. N. Peak, C. W. Knapp, R. K. Yang et al., “Abundance of six tetracycline resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies,” Environmental Microbiology, vol. 9, no. 1, pp. 143–151, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. C. S. Hölzel, K. Schwaiger, K. Harms et al., “Sewage sludge and liquid pig manure as possible sources of antibiotic resistant bacteria,” Environmental Research, vol. 110, no. 4, pp. 318–326, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. H. K. Allen, T. Looft, D. O. Bayles et al., “Antibiotics in feed induce prophages in swine fecal microbiomes,” mBio, vol. 2, no. 6, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Looft, T. A. Johnson, H. K. Allen et al., “In-feed antibiotic effects on the swine intestinal microbiome,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 5, pp. 1691–1696, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. C. H. Bolster, “Factors controlling subsurface transport of manure-borne pathogens,” 2012, http://www.extension.org/pages/65647/microbes:-from-farm-to-public-risk.
  18. H. Heuer, H. Schmitt, and K. Smalla, “Antibiotic resistance gene spread due to manure application on agricultural fields,” Current Opinion in Microbiology, vol. 14, no. 3, pp. 236–243, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. B. M. Marshall and S. B. Levy, “Food animals and antimicrobials: impacts on human health,” Clinical Microbiology Reviews, vol. 24, no. 4, pp. 718–733, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. M. C. Roberts, “Environmental macrolide-lincosamide-streptogramin and tetracycline resistant bacteria,” Frontiers in Microbiology, vol. 2, pp. 1–8, 2011. View at Google Scholar
  21. K. J. Forsberg, A. Reyes, B. Wang et al., “The shared antibiotic resistome of soil bacteria and human pathogens,” Science, vol. 337, pp. 1107–1111, 2012. View at Google Scholar
  22. B. González-Zorn and J. A. Escudero, “Ecology of antimicrobial resistance: humans, animals, food and environment,” International Microbiology, vol. 15, pp. 101–109, 2012. View at Google Scholar
  23. M. Popowska, M. Rzeczycka, A. Miernik, A. Krawczyk-Balska, F. Walsh, and B. Duffy, “Influence of soil use on prevalence of tetracycline,streptomycin, and erythromycin resistance and associated resistance genes,” Antimicrobial Agents and Chemotherapy, vol. 56, no. 3, pp. 1434–1443, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. T. O. Rahube and C. K. Yost, “Characterization of a mobile and multiple resistance plasmid isolated from swine manure and its detection in soil after manure application,” Journal of Applied Microbiology, vol. 112, pp. 1123–1133, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. B. Marquez, “Bacterial efflux systems and efflux pumps inhibitors,” Biochimie, vol. 87, no. 12, pp. 1137–1147, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Stavri, L. J. V. Piddock, and S. Gibbons, “Bacterial efflux pump inhibitors from natural sources,” Journal of Antimicrobial Chemotherapy, vol. 59, no. 6, pp. 1247–1260, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Poole, “Efflux-mediated antimicrobial resistance,” Journal of Antimicrobial Chemotherapy, vol. 56, no. 1, pp. 20–51, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. J. L. Martínez and F. Rojo, “Metabolic regulation of antibiotic resistance,” FEMS Microbiology Reviews, vol. 35, no. 5, pp. 768–789, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. L. Fernandez and R. E. W. Hancock, “Adaptive and mutational resistance: role of porins and efflux pumps in drug resistance,” Clinical Microbiology Reviews, vol. 25, pp. 661–681, 2012. View at Google Scholar
  30. T. A. Krulwich, O. Lewinson, E. Padan, and E. Bibi, “Do physiological roles foster persistance of drug/multidrug-efflux transporters? A case study,” Nature Reviews Microbiology, vol. 3, no. 7, pp. 566–572, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. L. J. V. Piddock, “Multidrug-resistance efflux pumps—not just for resistance,” Nature Reviews Microbiology, vol. 4, no. 8, pp. 629–636, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. X.-Z. Li and H. Nikaido, “Efflux-mediated drug resistance in bacteria: an update,” Drugs, vol. 69, no. 12, pp. 1555–1623, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. A. C. Abreu, A. J. McBain, and M. Simoes, “Plants as sources of new antimicrobials and resistance-modifying agents,” Natural Product Reports, vol. 29, pp. 1007–1021, 2012. View at Google Scholar
  34. A. Ojeda-Sana, V. Repetto, and S. Moreno, “Carnosic acid is an efflux pumps modulator by dissipation of the membrane potential in Enterococcus faecalis and Staphylococcus aureus,” World Journal of Microbiology and Biotechnology, vol. 29, pp. 137–144, 2013. View at Google Scholar
  35. J. G. Holler, S. B. Christensen, H.-C. Slotved et al., “Novel inhibitory activity of the Staphylococcus aureus NorA efflux pump by a kaempferol rhamnoside isolated from Persea lingue Nees,” Journal of Antimicrobial Chemotherapy, vol. 67, no. 5, pp. 1138–1144, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. L. Ma and D. Dolphin, “The metabolites of dietary chlorophylls,” Phytochemistry, vol. 50, no. 2, pp. 195–202, 1999. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Holden, “Chlorophyll degradation products in leaf protein preparations,” Journal of the Science of Food and Agriculture, vol. 25, no. 11, pp. 1427–1432, 1974. View at Google Scholar · View at Scopus
  38. Y. Takeda, S. Uchiyama, and Y. Saito, “High performance liquid chromatography of pheophorbide a and pyropheophorbide a in salted vegetables and chlorella,” Journal of the Food Hygienic Society of Japan, vol. 26, pp. 56–60, 1985. View at Google Scholar
  39. Y. Shioi, Y. Tatsumi, and K. Shimokawa, “Enzymatic degradation of chlorophyll in chenopodium album,” Plant and Cell Physiology, vol. 32, no. 1, pp. 87–93, 1991. View at Google Scholar · View at Scopus
  40. H. Oshima, E. Ueno, I. Saito, and H. Matsumoto, “Development of a solid-phase extraction method for determination of pheophorbide a and pyropheophorbide a in health foods by liquid chromatography,” Journal of AOAC International, vol. 87, no. 4, pp. 937–942, 2004. View at Google Scholar · View at Scopus
  41. S. Aiamla-or, S. Kaewsuksaeng, M. Shigyo, and N. Yamauchi, “Impact of UV-B irradiation on chlorophyll degradation and chlorophyll-degrading enzyme activities in stored broccoli (Brassica oleracea L. Italica Group) florets,” Food Chemistry, vol. 120, no. 3, pp. 645–651, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. M. G. Ferruzzi, M. L. Failla, and S. J. Schwartz, “Assessment of degradation and intestinal cell uptake of carotenoids and chlorophyll derivatives from spinach puree using an in vitro digestion and Caco-2 human cell model,” Journal of Agricultural and Food Chemistry, vol. 49, no. 4, pp. 2082–2089, 2001. View at Publisher · View at Google Scholar · View at Scopus
  43. K. D. Ashby, J. Wen, P. Chowdhury, T. A. Casey, M. A. Rasmussen, and J. W. Petrich, “Fluorescence of dietary porphyrins as a basis for real-time detection of fecal contamination on meat,” Journal of Agricultural and Food Chemistry, vol. 51, no. 11, pp. 3502–3507, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. W. M. Campbell, G. S. Dombroski, I. Sharma, A. C. Partridge, and M. G. Collett, “Photodynamic chlorophyll a metabolites, including phytoporphyrin (phylloerythrin), in the blood of photosensitive livestock: overview and measurement,” New Zealand Veterinary Journal, vol. 58, no. 3, pp. 146–154, 2010. View at Google Scholar · View at Scopus
  45. M. Aprahamian, S. Evrardl, P. Keller et al., “Distribution of pheophorbide A in normal tissues and in an experimental pancreatic cancer in rats,” Anti-Cancer Drug Design, vol. 8, no. 2, pp. 101–114, 1993. View at Google Scholar · View at Scopus
  46. J. W. Jonker, M. Buitelaar, E. Wagenaar et al., “The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 24, pp. 15649–15654, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. R. W. Robey, K. Steadman, O. Polgar, and S. E. Bates, “ABCG2-mediated transport of photosensitizers: potential impact on photodynamic therapy,” Cancer Biology and Therapy, vol. 4, no. 2, pp. 187–194, 2005. View at Google Scholar · View at Scopus
  48. M. Li, H. Yuan, N. Li et al., “Identification of interspecies difference in efflux transporters of hepatocytes from dog, rat, monkey and human,” European Journal of Pharmaceutical Sciences, vol. 35, no. 1-2, pp. 114–126, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. M. R. F. Lee, V. J. Theobald, H. J. Ougham et al., “Natural faecal fluorophores and the potential of chlorophyll based markers to optimise fluorescence as a real-time solution for the detection of faecal contamination on carcasses,” Meat Science, vol. 86, no. 4, pp. 966–975, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. C. A. Barnes, S. L. Rasmussen, J. W. Petrich, and M. A. Rasmussen, “Determination of the concentration of potential efflux pump inhibitors, pheophorbide a and pyropheophorbide a, in the feces of animals by fluorescence spectroscopy,” Journal of Agricultural and Food Chemistry, vol. 60, pp. 10456–10460, 2012. View at Google Scholar
  51. F. R. Stermitz, J. Tawara-Matsuda, P. Lorenz, P. Mueller, L. Zenewicz, and K. Lewis, “5'-methoxyhydnocarpin-D and Pheophorbide A: Berberis species components that potentiate berberine growth inhibition of resistant Staphylococcus aureus,” Journal of Natural Products, vol. 63, no. 8, pp. 1146–1149, 2000. View at Publisher · View at Google Scholar · View at Scopus
  52. R. Musumeci, A. Speciale, R. Costanzo et al., “Berberis aetnensis C. Presl. extracts: antimicrobial properties and interaction with ciprofloxacin,” International Journal of Antimicrobial Agents, vol. 22, no. 1, pp. 48–53, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. M. C. Roberts, “Update on macrolide-lincosamide-streptogramin, ketolide, and oxazolidinone resistance genes,” FEMS Microbiology Letters, vol. 282, no. 2, pp. 147–159, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. Compassion in World Farming, Antibiotics in animal farming, Public health and animal welfare, 2011, http://www.ciwf.org.uk/includes/documents/cm_docs/2011/a/antibiotics_in_animal_farming.pdf.
  55. S. Döhne, R. Merle, A. V. Altrock et al., “Antibiotic susceptibility of Salmonella, Campylobacter coli, and Campylobacter jejuni isolated from northern German fattening pigs,” Journal of Food Protection, vol. 75, no. 10, pp. 1839–1845, 2012. View at Google Scholar
  56. H. Hao, Z. Yuan, Z. Shen et al., “Mutational and transcriptomic changes involved in the development of macrolide resistance in Campylobacter jejuni,” Antimicrobial Agents and Chemotherapy, vol. 57, pp. 1369–1378, 2013. View at Google Scholar
  57. J. Olmstead, Institute for Agriculture and Trade Policy, Bugs in the system, How the FDA fails to regulate antibiotics in ethanol production, 2012, http://www.iatp.org/files/2012_05_02_AntibioticsInEthanol_JO_0.pdf.
  58. C. G. Shurson, D. M. Paulus, A. DiCostanzo et al., Are antibiotics a concern in distiller's co-products?, University of Minnesota, 2012, http://www.ddgs.umn.edu/prod/groups/cfans/@pub/@cfans/@ddgs/documents/asset/cfans_asset_414344.pdf.
  59. FDA, U.S. Food and Drug Administration, Animal Drugs @ FDA, 2013, http://www.accessdata.fda.gov/scripts/animaldrugsatfda/.
  60. G. Tegos, F. R. Stermitz, O. Lomovskaya, and K. Lewis, “Multidrug pump inhibitors uncover remarkable activity of plant antimicrobials,” Antimicrobial Agents and Chemotherapy, vol. 46, no. 10, pp. 3133–3141, 2002. View at Publisher · View at Google Scholar · View at Scopus
  61. Å. Aakra, H. Vebø, L. Snipen et al., “Transcriptional response of Enterococcus faecalis V583 to erythromycin,” Antimicrobial Agents and Chemotherapy, vol. 49, no. 6, pp. 2246–2259, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. C. R. Jackson, P. J. Fedorka-Cray, J. B. Barrett, and S. R. Ladely, “Effects of tylosin use on erythromycin resistance in enterococci isolated from swine,” Applied and Environmental Microbiology, vol. 70, no. 7, pp. 4205–4210, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. M. E. Jacob, J. T. Fox, S. K. Narayanan, J. S. Drouillard, D. G. Renter, and T. G. Nagaraja, “Effects of feeding wet corn distillers grains with solubles with or without monensin and tylosin on the prevalence and antimicrobial susceptibilities of fecal foodborne pathogenic and commensal bacteria in feedlot cattle,” Journal of Animal Science, vol. 86, no. 5, pp. 1182–1190, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. D. B. Holman and M. R. Chénier, “Impact of subtherapeutic administration of tylosin and chlortetracycline on antimicrobial resistance in farrow-to-finish swine,” FEMS Microbiology Ecology, vol. 85, no. 1, pp. 1–13, 2013. View at Publisher · View at Google Scholar
  65. J. M. Andrews, “Determination of minimum inhibitory concentrations,” Journal of Antimicrobial Chemotherapy, vol. 48, no. 1, pp. 5–16, 2001. View at Google Scholar · View at Scopus
  66. TOKU-E, Erythromycin (E-mycin, Ery-tab, Benzamycin), 2012, http://antibiotics.toku-e.com/antimicrobial_599.html.
  67. J. Liu, P. Keelan, P. M. Bennett, and V. I. Enne, “Characterization of a novel macrolide efflux gene, mef(B), found linked to sul3 in porcine Escherichia coli,” Journal of Antimicrobial Chemotherapy, vol. 63, no. 3, pp. 423–426, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. R. Lindqvist, “Estimation of Staphylococcus aureus growth parameters from turbidity data: characterization of strain variation and comparison of methods,” Applied and Environmental Microbiology, vol. 72, no. 7, pp. 4862–4870, 2006. View at Publisher · View at Google Scholar · View at Scopus
  69. M. T. Madigan, J. M. Martinko, P. V. Dunlap, and D. P. Clark, “Growth of bacterial populations,” in Brock Biology of Microorganisms, pp. 147–152, Pearson Education, San Francisco, Calif, USA, 2008. View at Google Scholar
  70. E. Bast, “Mikroskopische zellzählung in einer zählkammer,” in Mikrobiologische Methoden: Eine Einführung in Grundlegende Arbeitstechniken, pp. 280–285, Spektrum-Akademischer Verlag, 2001, (German). View at Google Scholar
  71. K. P. Norris and E. O. Powell, “Improvements in determining total counts of bacteria,” Journal of the Royal Microscopical Society, vol. 80, pp. 107–119, 1961. View at Google Scholar
  72. M. P. Bryant, “Commentary on the Hungate technique for culture of anaerobic bacteria,” American Journal of Clinical Nutrition, vol. 25, no. 12, pp. 1324–1328, 1972. View at Google Scholar · View at Scopus
  73. M. A. Cotta, T. R. Whitehead, and R. L. Zeltwanger, “Isolation, characterization and comparison of bacteria from swine faeces and manure storage pits,” Environmental Microbiology, vol. 5, no. 9, pp. 737–745, 2003. View at Publisher · View at Google Scholar · View at Scopus
  74. S. Boisen and J. A. Fernández, “Prediction of the total tract digestibility of energy in feedstuffs and pig diets by in vitro analyses,” Animal Feed Science and Technology, vol. 68, no. 3-4, pp. 277–286, 1997. View at Google Scholar · View at Scopus
  75. J. Bindelle, A. Buldgen, C. Boudry, and P. Leterme, “Effect of inoculum and pepsin-pancreatin hydrolysis on fibre fermentation measured by the gas production technique in pigs,” Animal Feed Science and Technology, vol. 132, no. 1-2, pp. 111–122, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. J. L. Wickliff and S. Aronoff, “Degradation of chlorophyll a to pheophytin a, pheophorbide a, and pyrroporphine XV for tracer studies,” Analytical Biochemistry, vol. 6, no. 1, pp. 39–46, 1963. View at Google Scholar · View at Scopus
  77. Miller Publishing Co., S. MicroSource, Direct-fed Microbial, Enzyme & Forage Additive Compendium—Ninth Edition, 2013, http://www.microbialcompendium.com.
  78. EUCAST, European Committee on Antimicrobial Susceptibility Testing, Erythromycin / Staphylococcus aureus, EUCAST MIC Distribution, Version 5.13, 2013, http://mic.eucast.org/Eucast2/regShow.jsp?Id=2642.
  79. EUCAST, European Committee on Antimicrobial Susceptibility Testing, Erythromycin / Enterococcus faecalis, EUCAST MIC Distribution, Version 5.13, 2013, http://mic.eucast.org/Eucast2/regShow.jsp?Id=7183.
  80. J. L. Martinez, A. Fajardo, L. Garmendia et al., “A global view of antibiotic resistance,” FEMS Microbiology Reviews, vol. 33, pp. 44–65, 2009. View at Google Scholar
  81. B. M. Jonas, B. E. Murray, and G. M. Weinstock, “Characterization of emeA, a norA homolog and multidrug resistance efflux pump, in Enterococcus faecalis,” Antimicrobial Agents and Chemotherapy, vol. 45, no. 12, pp. 3574–3579, 2001. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Gibbons, M. Oluwatuyi, and G. W. Kaatz, “A novel inhibitor of multidrug efflux pumps in Staphylococcus aureus,” Journal of Antimicrobial Chemotherapy, vol. 51, no. 1, pp. 13–17, 2003. View at Publisher · View at Google Scholar · View at Scopus
  83. G. Belofsky, D. Percivill, K. Lewis, G. P. Tegos, and J. Ekart, “Phenolic metabolites of Dalea versicolor that enhance antibiotic activity against model pathogenic bacteria,” Journal of Natural Products, vol. 67, no. 3, pp. 481–484, 2004. View at Publisher · View at Google Scholar · View at Scopus
  84. L. Unger and A. Kisch, “Observations on bacteriostatic and bactericidal action of erythromycin,” Proceedings of the Society for Experimental Biology and Medicine, vol. 98, pp. 176–178, 1958. View at Google Scholar
  85. F. Fraschini, P. C. Braga, and V. Copponi, “Bactericidal activity of erythromycin in the respiratory system,” Current Medical Research and Opinion, vol. 7, no. 7, pp. 429–439, 1981. View at Google Scholar · View at Scopus
  86. G. A. Pankey and L. D. Sabath, “Clinical relevance of bacteriostatic versus bactericidal mechanisms of action in the treatment of gram-positive bacterial infections,” Clinical Infectious Diseases, vol. 38, no. 6, pp. 864–870, 2004. View at Publisher · View at Google Scholar · View at Scopus
  87. H. Nikaido, “Multidrug resistance in bacteria,” Annual Review of Biochemistry, vol. 78, pp. 119–146, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. J. L. Martínez, F. Baquero, and D. I. Andersson, “Beyond serial passages: new methods for predicting the emergence of resistance to novel antibiotics,” Current Opinion in Pharmacology, vol. 11, no. 5, pp. 439–445, 2011. View at Publisher · View at Google Scholar · View at Scopus
  89. E. Piątkowska, J. Piątkowski, and A. Przondo-Mordarska, “The strongest resistance of Staphylococcus aureus to erythromycin is caused by decreasing uptake of the antibiotic into the cells,” Cellular and Molecular Biology Letters, vol. 17, pp. 633–645, 2012. View at Google Scholar
  90. E. J. C. Goldstein and V. L. Sutter, “Effect of carbon dioxide on erythromycin,” Antimicrobial Agents and Chemotherapy, vol. 23, no. 2, pp. 325–327, 1983. View at Google Scholar · View at Scopus
  91. L. M. Ednie, M. R. Jacobs, and P. C. Appelbaum, “Anti-anaerobic activity of erythromycin, azithromycin and clarithromycin: effect of pH adjustment of media to compensate for pH shift caused by incubation in CO2,” Journal of Antimicrobial Chemotherapy, vol. 41, no. 3, pp. 387–389, 1998. View at Publisher · View at Google Scholar · View at Scopus
  92. T. T. Luong, P. M. Dunman, E. Murphy, S. J. Projan, and C. Y. Lee, “Transcription profiling of the mgrA regulon in Staphylococcus aureus,” Journal of Bacteriology, vol. 188, no. 5, pp. 1899–1910, 2006. View at Publisher · View at Google Scholar · View at Scopus
  93. K. Poole, “Bacterial stress responses as determinants of antimicrobial resistance,” Journal of Antimicrobial Chemotherapy, vol. 67, pp. 2069–2089, 2012. View at Google Scholar
  94. Q. C. Truong-Bolduc, L. C. Hsing, R. Villet et al., “Reduced aeration affects the expression of the NorB efflux pump of Staphylococcus aureus by posttranslational modification of MgrA,” Journal of Bacteriology, vol. 194, no. 7, pp. 1823–1834, 2012. View at Google Scholar · View at Scopus
  95. R. Leclercq, “Mechanisms of resistance to macrolides and lincosamides: nature of the resistance elements and their clinical implications,” Clinical Infectious Diseases, vol. 34, no. 4, pp. 482–492, 2002. View at Publisher · View at Google Scholar · View at Scopus
  96. V. A. Luna, M. Heiken, K. Judge et al., “Distribution of mef(A) in gram-positive bacteria from healthy Portuguese children,” Antimicrobial Agents and Chemotherapy, vol. 46, no. 8, pp. 2513–2517, 2002. View at Publisher · View at Google Scholar · View at Scopus
  97. J. L. Floyd, K. P. Smith, S. H. Kumar, J. T. Floyd, and M. F. Varela, “LmrS is a multidrug efflux pump of the major facilitator superfamily from Staphylococcus aureus,” Antimicrobial Agents and Chemotherapy, vol. 54, no. 12, pp. 5406–5412, 2010. View at Publisher · View at Google Scholar · View at Scopus
  98. G. W. Kaatz, V. V. Moudgal, S. M. Seo, J. B. Hansen, and J. E. Kristiansen, “Phenylpiperidine selective serotonin reuptake inhibitors interfere with multidrug efflux pump activity in Staphylococcus aureus,” International Journal of Antimicrobial Agents, vol. 22, no. 3, pp. 254–261, 2003. View at Publisher · View at Google Scholar · View at Scopus
  99. K. A. Hassan, R. A. Skurray, and M. H. Brown, “Active export proteins mediating drug resistance in staphylococci,” Journal of Molecular Microbiology and Biotechnology, vol. 12, no. 3-4, pp. 180–196, 2007. View at Publisher · View at Google Scholar · View at Scopus
  100. J. Huang, P. W. O'Toole, W. Shen et al., “Novel chromosomally encoded multidrug efflux transporter MdeA in Staphylococcus aureus,” Antimicrobial Agents and Chemotherapy, vol. 48, no. 3, pp. 909–917, 2004. View at Publisher · View at Google Scholar · View at Scopus
  101. J. I. Ross, E. A. Eady, J. H. Cove, and S. Baumberg, “Minimal functional system required for expression of erythromycin resistance by msrA in Staphylococcus aureus RN4220,” Gene, vol. 183, no. 1-2, pp. 143–148, 1996. View at Publisher · View at Google Scholar · View at Scopus
  102. K. Kadlec, A. T. Feßler, T. Hauschild, and S. Schwarz, “Novel and uncommon antimicrobial resistance genes in livestock-associated methicillin-resistant Staphylococcus aureus,” Clinical Microbiology and Infection, vol. 18, pp. 745–755, 2012. View at Publisher · View at Google Scholar · View at Scopus
  103. C. R. S. Teodoro, C. S. Mattos, F. S. Cavalcante, E. M. Pereira, and K. R. N. dos Santos, “Characterization of MLSb resistance among Staphylococcus aureus and Staphylococcus epidermidis isolates carrying different SCCmec types,” Microbiology and Immunology, vol. 56, pp. 647–650, 2012. View at Google Scholar
  104. M. A. Argudín, B.-A. Tenhagen, A. Fetsch et al., “Virulence and resistance determinants of German Staphylococcus aureus ST398 isolates from nonhuman sources,” Applied and Environmental Microbiology, vol. 77, no. 9, pp. 3052–3060, 2011. View at Publisher · View at Google Scholar · View at Scopus
  105. Z. Zhou, L. Raskin, and J. L. Zilles, “Macrolide resistance in microorganisms at antimicrobial-free swine farms,” Applied and Environmental Microbiology, vol. 75, no. 18, pp. 5814–5820, 2009. View at Publisher · View at Google Scholar · View at Scopus
  106. M. Kalmokoff, L. M. Waddington, M. Thomas et al., “Continuous feeding of antimicrobial growth promoters to commercial swine during the growing/finishing phase does not modify faecal community erythromycin resistance or community structure,” Journal of Applied Microbiology, vol. 110, no. 6, pp. 1414–1425, 2011. View at Publisher · View at Google Scholar · View at Scopus
  107. Santa Cruz Biotechnology, Tylosin tartrate (CAS, 1405-54-5), Material Safety Data Sheet, 2013, http://datasheets.scbt.com/sc-204933.pdf.
  108. M. C. Roberts, “Resistance to macrolide, lincosamide, streptogramin, ketolide, and oxazolidinone antibiotics,” Molecular Biotechnology, vol. 28, no. 1, pp. 47–62, 2004. View at Publisher · View at Google Scholar · View at Scopus
  109. C. Baker-Austin, M. S. Wright, R. Stepanauskas, and J. V. McArthur, “Co-selection of antibiotic and metal resistance,” Trends in Microbiology, vol. 14, no. 4, pp. 176–182, 2006. View at Publisher · View at Google Scholar · View at Scopus
  110. J. L. Martinez, M. B. Sánchez, L. Martínez-Solano et al., “Functional role of bacterial multidrug efflux pumps in microbial natural ecosystems,” FEMS Microbiology Reviews, vol. 33, no. 2, pp. 430–449, 2009. View at Publisher · View at Google Scholar · View at Scopus
  111. J. Kluytmans and J. L. Murk, “Lincomycin and clindamycin,” in Kucers' the Use of Antibiotics: A Clinical Review of Antibacterial, Antifungal and Antiviral Drugs, L. M. Grayson, Ed., pp. 987–1007, CRC Press, Boca Raton, Fla, USA, 2010. View at Google Scholar
  112. C. S. Hölzel, C. Müller, K. S. Harms et al., “Heavy metals in liquid pig manure in light of bacterial antimicrobial resistance,” Environmental Research, vol. 113, pp. 21–27, 2012. View at Publisher · View at Google Scholar · View at Scopus
  113. R. Leclercq, R. Cantón, D. F. J. Brown et al., “EUCAST expert rules in antimicrobial susceptibility testing,” Clinical Microbiology and Infection, vol. 19, pp. 141–160, 2013. View at Publisher · View at Google Scholar · View at Scopus
  114. A. P. Gerola, A. Santana, P. B. França et al., “Effects of metal and the phytyl chain on chlorophyll derivatives: physicochemical evaluation for photodynamic inactivation of microorganisms,” Photochemistry and Photobiology, vol. 87, no. 4, pp. 884–894, 2011. View at Publisher · View at Google Scholar · View at Scopus
  115. A. Bolotin, P. Wincker, S. Mauger et al., “The complete genome sequence of the lactic acid bacterium lactococcus lactis ssp. lactis IL1403,” Genome Research, vol. 11, no. 5, pp. 731–753, 2001. View at Publisher · View at Google Scholar · View at Scopus
  116. F. R. Stermitz, T. D. Beeson, P. J. Mueller, J.-F. Hsiang, and K. Lewis, “Staphylococcus aureus MDR efflux pump inhibitors from a Berberis and a Mahonia (sensu strictu) species,” Biochemical Systematics and Ecology, vol. 29, no. 8, pp. 793–798, 2001. View at Publisher · View at Google Scholar · View at Scopus
  117. L. J. V. Piddock, “Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria,” Clinical Microbiology Reviews, vol. 19, no. 2, pp. 382–402, 2006. View at Publisher · View at Google Scholar · View at Scopus
  118. T. R. Whitehead and M. A. Cotta, “Characterisation and comparison of microbial populations in swine faeces and manure storage pits by 16S rDNA gene sequence analyses,” Anaerobe, vol. 7, no. 4, pp. 181–187, 2001. View at Publisher · View at Google Scholar · View at Scopus
  119. R. Snell-Castro, J.-J. Godon, J.-P. Delgenès, and P. Dabert, “Characterisation of the microbial diversity in a pig manure storage pit using small subunit rDNA sequence analysis,” FEMS Microbiology Ecology, vol. 52, no. 2, pp. 229–242, 2005. View at Publisher · View at Google Scholar · View at Scopus
  120. A. Tello, B. Austin, and T. C. Telfer, “Selective pressure of antibiotic pollution on bacteria of importance to public health,” Environmental Health Perspectives, vol. 120, pp. 1100–1106, 2012. View at Google Scholar
  121. M. Wilson and J. A. Houghton, “Growth of algae on pig manure,” Irish Journal of Agricultural Research, vol. 13, pp. 49–60, 1974. View at Google Scholar
  122. M. V. Jiménez-Pérez, P. Sánchez-Castillo, O. Romera, D. Fernández-Moreno, and C. Pérez-Martínez, “Growth and nutrient removal in free and immobilized planktonic green algae isolated from pig manure,” Enzyme and Microbial Technology, vol. 34, pp. 392–398, 2004. View at Google Scholar
  123. M. K. Garrett, J. J. Strain, and M. D. B. Allen, “Composition of the product of algal culture in the liquid phase of animal slurry,” Journal of the Science of Food and Agriculture, vol. 27, pp. 603–611, 1976. View at Google Scholar
  124. E. W. Becker, “Micro-algae as a source of protein,” Biotechnology Advances, vol. 25, no. 2, pp. 207–210, 2007. View at Publisher · View at Google Scholar · View at Scopus
  125. I. de Godos, R. Muñoz, and B. Guieyssea, “Tetracycline removal during wastewater treatment in high-rate algal ponds,” Journal of Hazardous Materials, vol. 229-230, pp. 446–449, 2012. View at Google Scholar
  126. E. M. Ferrero, I. de Godos, E. M. Rodríguez, P. A. García-Encina, R. Muñoz, and E. Bécares, “Molecular characterization of bacterial communities in algal-bacterial photobioreactors treating piggery wastewaters,” Ecological Engineering, vol. 40, pp. 121–130, 2012. View at Publisher · View at Google Scholar · View at Scopus