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Comparative analysis of bacterial community and antibiotic-resistant strains in different developmental stages of the housefly (Musca domestica)

  • Environmental biotechnology
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Abstract

The housefly (Musca domestica) is an important host for a variety of bacteria, including some pathogenic and antibiotic-resistant strains. To further investigate the relationship between the housefly and the bacteria it harbors, it is necessary to understand the fate of microorganisms during the larval metamorphosis. The major bacterial communities in three developmental stages of the housefly (maggot, pupa, and adult fly) were investigated by a culture-independent method, polymerase chain reaction–denaturing gradient gel electrophoresis (PCR−DGGE) analysis of 16S rRNA genes. The bacteria that were identified using DGGE analysis spanned phyla Proteobacteria, Firmicutes, and Bacteroidetes. Changes in the predominant genera were observed during the housefly development. Bacteroides, Koukoulia, and Schineria were detected in maggots, Neisseria in pupae, and Macrococcus, Lactococcus, and Kurthia in adult flies. Antibiotic-resistant bacteria were screened using a selective medium and tested for antibiotic susceptibility. Most resistant isolates from maggots and pupae were classified as Proteus spp., while those from adult flies were much more diverse and spanned 12 genera. Among 20 tested strains across the three stages, 18 were resistant to at least two antibiotics. Overall, we demonstrated that there are changes in the major bacterial communities and antibiotic-resistant strains as the housefly develops.

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References

  • Ahmad A, Ghosh A, Schal C, Zurek L (2011) Insects in confined swine operations carry a large antibiotic resistant and potentially virulent enterococcal community. BMC Microbiol 11:23

    Article  Google Scholar 

  • Akhtar M, Hirt H, Zurek L (2009) Horizontal transfer of the tetracycline resistance gene tetM mediated by pCF10 among Enterococcus faecalis in the house fly (Musca domestica L.) alimentary canal. Microb Ecol 58:509–518

    Article  CAS  Google Scholar 

  • Alam MJ, Zurek L (2004) Association of Escherichia coli O157: H7 with houseflies on a cattle farm. Appl Environ Microbiol 70:7578–7580

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  Google Scholar 

  • Andersen AS, Sandvang D, Schnorr KM, Kruse T, Neve S, Joergensen B, Karlsmark T, Krogfelt KA (2010) A novel approach to the antimicrobial activity of maggot debridement therapy. J Antimicrob Chemother 65:1646–1654

    Article  CAS  Google Scholar 

  • Babendreier D, Joller D, Romeis J, Bigler F, Widmer F (2007) Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. FEMS Microbiol Ecol 59:600–610

    Article  CAS  Google Scholar 

  • Benson MJ, Gawronski JD, Eveleigh DE, Benson DR (2004) Intracellular symbionts and other bacteria associated with deer ticks (Ixodes scapularis) from Nantucket and Wellfleet, Cape Cod, Massachusetts. Appl Environ Microbiol 70:616–620

    Article  CAS  Google Scholar 

  • Butaye P, Devriese LA, Haesebrouck F (2001) Differences in antibiotic resistance patterns of Enterococcus faecalis and Enterococcus faecium strains isolated from farm and pet animals. Antimicrob Agents Chemother 45:1374–1378

    Article  CAS  Google Scholar 

  • Cole JR, Chai B, Farris RJ, Wang Q, Kulam SA, McGarrell DM, Garrity GM, Tiedje JM (2005) The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res 33:D294–D296

    Article  CAS  Google Scholar 

  • Corby-Harris V, Pontaroli AC, Shimkets LJ, Bennetzen JL, Habel KE, Promislow DEL (2007) Geographical distribution and diversity of bacteria associated with natural populations of Drosophila melanogaster. Appl Environ Microbiol 73:3470–3479

    Article  CAS  Google Scholar 

  • Dang XL, Wang YS, Huang YD, Yu XQ, Zhang WQ (2010) Purification and characterization of an antimicrobial peptide, insect defensin, from immunized house fly (Diptera: Muscidae). J Med Entomol 47:1141–1145

    Article  CAS  Google Scholar 

  • Diez B, Pedros-Alio C, Marsh TL, Massana R (2001) Application of denaturing gradient gel electrophoresis (DGGE) to study the diversity of marine picoeukaryotic assemblages and comparison of DGGE with other molecular techniques. Appl Environ Microbiol 67:2942–2951

    Article  CAS  Google Scholar 

  • Erdmann GR, Khalil SK (1986) Isolation and identification of two antibacterial agents produced by a strain of Proteus mirabilis isolated from larvae of the screwworm (Cochliomyia hominivorax) (Diptera: Calliphoridae). J Med Entomol 23:208–211

    CAS  Google Scholar 

  • Förster M, Klimpel S, Mehlhorn H, Sievert K, Messler S, Pfeffer K (2007) Pilot study on synanthropic flies (e.g. Musca, Sarcophaga, Calliphora, Fannia, Lucilia, Stomoxys) as vectors of pathogenic microorganisms. Parasitol Res 101:243–246

    Article  Google Scholar 

  • Graczyk TK, Knight R, Gilman RH, Cranfield MR (2001) The role of non-biting flies in the epidemiology of human infectious diseases. Microbes Infect 3:231–235

    Article  CAS  Google Scholar 

  • Graham JP, Price LB, Evans SL, Graczyk TK, Silbergeld EK (2009) Antibiotic resistant enterococci and staphylococci isolated from flies collected near confined poultry feeding operations. Sci Total Environ 407:2701–2710

    Article  CAS  Google Scholar 

  • Hall BG (2004) Predicting the evolution of antibiotic resistance genes. Nat Rev Microbiol 2:430–435

    Article  CAS  Google Scholar 

  • Iwasa M, Makino S, Asakura H, Kobori H, Morimoto Y (1999) Detection of Escherichia coli O157:H7 from Musca domestica (Diptera: Muscidae) at a cattle farm in Japan. J Med Entomol 36:108–112

    CAS  Google Scholar 

  • Jaklic D, Lapanje A, Zupancic K, Smrke D, Gunde-Cimerman N (2008) Selective antimicrobial activity of maggots against pathogenic bacteria. J Med Microbiol 57:617–625

    Article  Google Scholar 

  • Kadavy DR, Hornby JM, Haverkost T, Nickerson KW (2000) Natural antibiotic resistance of bacteria isolated from larvae of the oil fly, Helaeomyia petrolei. Appl Environ Microbiol 66:4615–4619

    Article  CAS  Google Scholar 

  • Kadavy DR, Plantz B, Shaw CA, Myatt J, Kokjohn TA, Nickerson KW (1999) Microbiology of the oil fly, Helaeomyia petrolei. Appl Environ Microbiol 65:1477–1482

    CAS  Google Scholar 

  • Kuang Y, Jia H, Miyanaga K, Tanji Y (2009) Effect of milk on antibacterial activity of tetracycline against Escherichia coli and Staphylococcus aureus isolated from bovine mastitis. Appl Microbiol Biotechnol 84:135–142

    Article  CAS  Google Scholar 

  • Kümmerer K (2004) Resistance in the environment. J Antimicrob Chemother 54:311–320

    Article  Google Scholar 

  • Macovei L, Zurek L (2006) Ecology of antibiotic resistance genes: characterization of enterococci from houseflies collected in food settings. Appl Environ Microbiol 72:4028–4035

    Article  CAS  Google Scholar 

  • Murray AE, Hollibaugh JT, Orrego C (1996) Phylogenetic compositions of bacterioplankton from two California estuaries compared by denaturing gradient gel electrophoresis of 16S rDNA fragments. Appl Environ Microbiol 62:2676–2680

    CAS  Google Scholar 

  • Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    CAS  Google Scholar 

  • Poole T, Crippen T (2009) Conjugative plasmid transfer between Salmonella enterica Newport and Escherichia coli within the gastrointestinal tract of the lesser mealworm beetle, Alphitobius diaperinus (Coleoptera: Tenebrionidae). Poult Sci 88:1553–1558

    Article  CAS  Google Scholar 

  • Schabereiter-Gurtner C, Lubitz W, Rölleke S (2003) Application of broad-range 16S rRNA PCR amplification and DGGE fingerprinting for detection of tick-infecting bacteria. J Microbiol Methods 52:251–260

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  Google Scholar 

  • Tóth EM, Hell E, Kovács G, Borsodi AK, Márialigeti K (2006) Bacteria isolated from the different developmental stages and larval organs of the obligate parasitic fly, Wohlfahrtia magnifica (Diptera: Sarcophagidae). Microb Ecol 51:13–21

    Article  Google Scholar 

  • Tóth E, Kovács G, Schumann P, Kovács AL, Steiner U, Halbritter A, Márialigeti K (2001) Schineria larvae gen. nov., sp. nov., isolated from the 1st and 2nd larval stages of Wohlfahrtia magnifica (Diptera: Sarcophagidae). Int J Syst Evol Microbiol 51:401–407

    Google Scholar 

  • Vallaeys T (1997) Evaluation of denaturing gradient gel electrophoresis in the detection of 16S rDNA sequence variation in rhizobia and methanotrophs. FEMS Microbiol Ecol 24:279–285

    Article  CAS  Google Scholar 

  • Vela AI, Vázquez J, Gibello A, Blanco MM, Moreno MA, Liébana P, Albendea C, Alcalá B, Mendez A, Domínguez L, Fernández-Garayzábal JF (2000) Phenotypic and genetic characterization of Lactococcus garvieae isolated in Spain from lactococcosis outbreaks and comparison with isolates of other countries and sources. J Clin Microbiol 38:3791–3795

    CAS  Google Scholar 

  • von Wintzingerode F, Göbel UB, Stackebrandt E (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21:213–229

    Article  Google Scholar 

  • Wexler HM (2007) Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev 20:593–621

    Article  CAS  Google Scholar 

  • Yan S, Miyanaga K, Xing X, Tanji Y (2008) Succession of bacterial community and enzymatic activities of activated sludge by heat-treatment for reduction of excess sludge. Biochem Eng J 39:598–603

    Article  CAS  Google Scholar 

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Acknowledgments

This study was supported in part by a grant (21360399) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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Correspondence to Yasunori Tanji.

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Wei, T., Hu, J., Miyanaga, K. et al. Comparative analysis of bacterial community and antibiotic-resistant strains in different developmental stages of the housefly (Musca domestica). Appl Microbiol Biotechnol 97, 1775–1783 (2013). https://doi.org/10.1007/s00253-012-4024-1

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  • DOI: https://doi.org/10.1007/s00253-012-4024-1

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