Abstract
Antibiotic-resistant bacteria can be detected in pristine environments and animals. Tetracycline (TC) is frequently used for wide areas of veterinary medicine, which selects TC-resistant bacteria. The TC resistance genes are known from natural environments, and tet(M) is the broadest host range tet gene. Here, we report that TC-resistant bacteria and the TC resistance gene tet(M) were diverse in Adélie penguin intestines, even within a single penguin colony. Total bacterial counts were as high as 107 CFU g−1, and TC-resistant bacteria ranged from 1.4 × 102 to 6.6 × 103 CFU g−1 intestinal contents, which was 0–0.54 % of the total viable count. Phylogenetic affiliation of TC-resistant bacteria revealed a variety of Gram-positive and Gram-negative bacteria. The tet(M) gene was identified in 32.3 % of TC-resistant strains, and two tet(M) genotypes were identified within one penguin colony, suggesting various contamination origins of tet(M).
References
Aarestrup FM, Agerso Y, Gerner-Smidt P et al (2000) Comparison of antimicrobial resistance phenotypes and resistance genes in Enterococcus faecalis and Enterococcus faecium from human in the community, broilers, and pigs in Denmark. Diag Microbial Infect Dis 37:127–137
Agersø Y, Sengelov G, Jensen LB (2004) Development of a rapid method for direct detection of tet(M) genes in soil from Danish farmland. Environ Int 30:117–122
Agersø Y, Pedersen AG, Aarestrup FM (2006) Identification of Tn5397-like and Tn916-like transposons and diversity of the tetracycline resistance gene tet(M) in enterococci from humans, pigs and poultry. J Antimicrob Chemother 57:832–839
Al-Bahry SN, Al-Zadjali MA, Mahmoud IY et al (2012) Biomonitoring marine habitats in reference to antibiotic resistant bacteria and ampicillin resistance determinants from oviductal fluid of the nesting green sea turtle, Chelonia mydas. Chemosphere 87:1308–1315
Aminov RI, Garrigues-Jeanjean N, Mackie RI (2001) Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Appl Environ Microbiol 67:22–32
Andersson DI, Hughes D (2012) Evolution of antibiotic resistance at non-lethal drug concentrations. Drug Resist Updates 15:162–172
Ash RJ, Mauck B, Morgan M (2002) Antibiotic resistance of Gram-negative bacteria in rivers, United States. Emerg Infect Dis 8:713–716
Baya AM, Brayton PR, Brown VL et al (1986) Coincident plasmids and antimicrobial resistance in marine bacteria isolated from polluted and unpolluted Atlantic Ocean samples. Appl Environ Microbiol 51:1285–1292
Ben-Gigirey B, Basptista Vieites, de Sousa JM, Villa TG et al (1998) Changes in biogenic amines and microbiological analysis in albacore (Thunnus alalunga) muscle during frozen storage. J Food Prot 61:608–615
Blackburn JK, Mitchell MA, Blackburn MCH et al (2010) Evidence of antibiotic resistance in free-swimming, top level marine predatory fishes. J Zoo Wildl Med 41:7–16
Bozal N, Jesus M, Tudela E et al (2003) Characterization of several Psychrobacter strains isolated from Antarctic environments and description of Psychobacter luti sp. nov. and Psychrobacter fozii sp. nov. Int J Syst Evol Microbiol 53:1093–1100
Chee-Sanford JC, Aminov RI, Krapac IJ et al (2001) Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater underlying two swine production facilities. Appl Environ Microbiol 67:494–502
Chopra I, Robers M (2001) Tetracycline resistance: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65:232–260
D’Costa VM, King CE, Kalan L et al (2011) Antibiotic resistance is ancient. Nature 477:457–461. doi:10.1038/nature10388
De Souza MJ, Nair S, Bharathi PAL et al (2006) Metal and antibiotic-resistance in psychrophilic bacteria from Antarctic marine waters. Ecotoxicology 15:379–384
Denner EBM, Mark B, Busse HJ et al (2001) Psychrobacter proteolyticus sp. nov., a psychrophilic, halotolerant bacterium isolated from the Antarctic krill Euphausia superba Dana, excreting a cold-adapted metalloprotease. Syst Appl Microbiol 24:44–53
Gilliver MA, Bennett M, Begon M et al (1999) Antibiotic resistance found in wild rodents. Nature 401:233–234
Kim SR, Nonaka L, Suzuki S (2004) Occurrence of tetracycline resistance gene tet(M) and tet(S) in bacteria from marine aquaculture sites. FEMS Microbiol Lett 237:147–156
Kobayashi T, Nonaka L, Maruyama F et al (2007) Molecular evidence for the ancient origin of the ribosomal protection protein that mediates tetracycline resistance in bacteria. J Mol Evol 65:228–235
Leotta GA, Chinen I, Vigo GB et al (2006) Outbreaks of avian cholera in Hope Bay, Antarctica. J Wildl Dis 42:259–270
Miles TD, McLaughlin W, Brown PD (2006) Antimicrobial resistance Escherichia coli isolates from broiler chickens and humans. BMC Vet Res 2:7
Neela FA, Nonaka L, Suzuki S (2007) The diversity of multi-drug resistance profiles in tetracycline-resistance Vibrio species isolated from coastal sediments and seawater. J Microbiol 45:64–68
Neela FA, Nonaka L, Rahman MH et al (2009) Transfer of the chromosomally encoded tetracycline resistance gene tet(M) from marine bacteria to Escherichia coli and Enterococcus faecalis. World J Microbiol Biotechnol 25:1095–1101
Nonaka L, Ikeno K, Suzuki S (2007) Distribution of tetracycline resistance gene, tet(M), in Gram-positive and Gram-negative bacteria isolated from sediment and seawater at a coastal aquaculture site in Japan. Microbes Environ 22:335–364
Popowska M, Rzeczycka M, Miernik A et al (2012) Influence of soil use on prevalence of tetracycline, streptomycin, and erythromycin resistance and associated resistance genes. Antimicrob Agents Chemother 56:1434–1443
Radhouani H, Igrejas G, Pinto L et al (2011) Molecular characterization of antibiotic resistance in enterococci recovered from seagulls (Larus cachinnans) representing an environmental health problem. J Environ Monit 13:2227–2233
Rahman MH, Nonaka L, Tago R et al (2008a) Occurrence of two genotypes of tetracycline (TC) resistance gene tet(M) in the TC-resistant bacteria in marine sediments of Japan. Environ Sci Technol 42:5055–5061
Rahman MH, Sakamoto KQ, Nonaka L et al (2008b) Occurrence and diversity of the tetracycline resistance gene tet(M) in enteric bacteria of Antarctic Adelie penguins. J Antimicrob Chemother 62:627–628
Roberts MC, Schwarz S, Aarts HJM (2012) Erratum: Acquired antibiotic resistance genes: and overview. Front Microbiol 3, Article 384:1–17. doi:10.3389/fmicb.2012.00384
Schmidt AS, Bruun MS, Dalsgaard L et al (2001) Incidence, distribution and spread of tetracycline resistance determinants and integron-associated antibiotic resistance genes among mobile aeromonads from a fish farming environment. Appl Environ Microbiol 67:5675–5682
Segawa T, Takeuchi N, Rivera A et al (2013) Distribution of antibiotic resistance genes in glacier environments. Environ Microbiol Rep 5:127–134
Sjölund M, Bonnedahl J, Hernandez J et al (2008) Dissemination of multidrug-resistant bacteria into Arctic. Emerg Infect Dis 14:1–4
Waldenstrom J, Mevius D, Veldman K et al (2005) Antimicrobial resistance profiles of Campylobacter jejuni isolates from wild birds in Sweden. Appl Environ Microbiol 71:2438–2441
Wright GD (2010) Antibiotic resistance in the environment: a link to the clinic? Curr Opin Microbiol 13:580–594
Acknowledgments
We thank the members of the 45th and 46th Japanese Antarctic Research Expedition (JARE) and the crew of the icebreaker Shirase for their logistic support. Funding was partly supported by grants-in-aid from the twenty-first century COE and Global COE Programs (MEXT) and grants-in-aid from JSPS (14208063). M.H.R. was a postdoctoral fellow funded by twenty-first century COE and Global COE Programs. We thank Dr. Todd Miller for his critical review of the manuscript.
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Rahman, M.H., Sakamoto, K.Q., Kitamura, SI. et al. Diversity of tetracycline-resistant bacteria and resistance gene tet(M) in fecal microbial community of Adélie penguin in Antarctica. Polar Biol 38, 1775–1781 (2015). https://doi.org/10.1007/s00300-015-1732-x
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DOI: https://doi.org/10.1007/s00300-015-1732-x