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Identification of 18 vector species belonging to Group I, Group II, and Group III ‘Dirty 22’ species known to contaminate food and spread foodborne pathogens: DNA barcoding study of public health importance

Published online by Cambridge University Press:  12 December 2016

Irshad M. Sulaiman ,
Emily Jacobs ,
Steven Simpson  and
Khalil Kerdahi
Irshad M. Sulaiman*
Affiliation:
Microbiological Sciences Branch, South Regional Laboratory, US Food and Drug Administration, 60, Eight Street, Atlanta, Georgia, 30309, USA
Emily Jacobs
Affiliation:
Microbiological Sciences Branch, South Regional Laboratory, US Food and Drug Administration, 60, Eight Street, Atlanta, Georgia, 30309, USA
Steven Simpson
Affiliation:
Microbiological Sciences Branch, South Regional Laboratory, US Food and Drug Administration, 60, Eight Street, Atlanta, Georgia, 30309, USA
Khalil Kerdahi
Affiliation:
Microbiological Sciences Branch, South Regional Laboratory, US Food and Drug Administration, 60, Eight Street, Atlanta, Georgia, 30309, USA
*
*E-mail: irshad.sulaiman@fda.hhs.gov
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Abstract

The US Food and Drug Administration (US-FDA) uses the presence of filth and extraneous materials as one of the criteria in implementing regulatory actions and assessing food adulteration of public health importance. So far, 22 common pest species (‘Dirty 22’ species) have been considered by this agency for the spreading of foodborne illness, and their presence is an indicator of unsanitary conditions in food processing and storage facilities. Recently, we classified the ‘Dirty 22’ species into four groups: Group I (four cockroach species), Group II (two ant species), Group III (12 fly species), and Group IV (four rodent species), and described two molecular diagnostic methods for group-specific identification. We developed a PCR-RFLP assay based on rRNA gene for the detection and differentiation of Group I ‘Dirty 22’ species. Later, we designed three Group II ‘Dirty 22’ species-specific nested PCR primer sets and sequence characterized the rRNA, elongation factor 1-alpha (EF-1a), and wingless (WNT-1) loci. In this follow-up study, we have evaluated the robustness of five unique sets of published primers targeting the mitochondrial cytochrome oxidase I (COI) gene for insect barcoding. With modified PCR conditions, we successfully used COI barcoding for 18 members of Group I, Group II, and Group III ‘Dirty 22’ species. Results of this study reveal that COI barcoding is an effective tool for rapid identification of insects of Groups I, II, and III ‘Dirty 22’ species known to contaminate food and spread foodborne pathogens.

Keywords

‘Dirty 22’ vector speciesDNA barcodingfoodborne diseasepublic health
Type
Research Paper
Information
International Journal of Tropical Insect Science , Volume 37 , Issue 1 , March 2017 , pp. 1 - 10
Copyright
Copyright © icipe 2016 

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References

Anbalagan, S., Arunprasanna, V., Kannan, M., Dinakaran, S. and Krishnan, M. (2015) Simulium (Gomphostilbia) (Diptera: Simuliidae) from Southern Western Ghats, India: two new species and DNA barcoding. Acta Tropica 149, 94–105.Google Scholar
Aransay, A. M., Scoulica, E., Chaniotis, B. and Tselentis, Y. (1999) Typing of sand flies from Greece and Cyprus by DNA polymorphism of 18S rRNA gene. Insect Molecular Biology 8, 179–184.Google Scholar
Banerjee, D., Kumar, V., Maity, A., Ghosh, B., Tyagi, K., Singha, D., Kundu, S., Laskar, B. A., Naskar, A. and Rath, S. (2015) Identification through DNA barcoding of Tabanidae (Diptera) vectors of surra disease in India. Acta Tropica 150, 52–58. doi: 10.1016/j.actatropica.2015.06.023.CrossRefGoogle ScholarPubMed
Biles, P. V. and Ziobro, G. C. (2000) Regulatory action criteria for filth and other extraneous materials. IV. Visual detection of hair in food. Regulatory Toxicology and Pharmacology 32, 73–77.CrossRefGoogle ScholarPubMed
Blacket, M. J., Rice, A. D., Semeraro, L. and Malipati, M. B. (2015) DNA-based identifications reveal multiple introductions of the vegetable leafminer Liriomyza sativae (Diptera: Agromyzidae) into the Torres Strait Islands and Papua New Guinea. Bulletin of Entomological Research 105, 533–544. doi: 10.1017/S0007485315000383.Google Scholar
Bybee, S. M., Taylor, S. D., Riley Nelson, C. and Whiting, M. F. (2004) A phylogeny of robber flies (Diptera: Asilidae) at the sub familial level: molecular evidence. Molecular Phylogenetics and Evolution 30, 789–797.Google Scholar
Caterino, M. S., Cho, S. and Sperling, F. A. (2000) The current state of insect molecular systematics: a thriving Tower of Babel. Annual Review of Entomology 45, 1–54. doi: 10.1146/annurev.ento.45.1.1.Google Scholar
Conflitti, I. M., Pruess, K. P., Cywinska, A., Powers, T. O. and Currie, D. C. (2013) DNA barcoding distinguishes pest species of the black fly genus Cnephia (Diptera: Simuliidae). Journal of Medical Entomology 50, 1250–1260.Google Scholar
Cruickshank, R. H., Johnson, K. P., Smith, V. S., Adams, R. J., Clayton, D. H. and Page, R. D. (2001) Phylogenetic analysis of partial sequences of Elongation Factor 1alpha identifies major groups of lice (Insecta: Phthiraptera). Molecular Phylogenetics and Evolution 19, 202–215.Google Scholar
Cywinska, A., Hunter, F. F. and Hebert, P. D. N. (2006) Identifying Canadian mosquito species through DNA barcodes. Medical and Veterinary Entomology 20, 413–424.Google Scholar
Danforth, B. N., Brady, S. G., Sipes, S. D. and Pearson, A. (2004) Single-copy nuclear genes recover cretaceous-age divergences in bees. Systematic Biology 53, 309–326.Google Scholar
Danforth, B. N. and Ji, S. (1998) Elongation Factor-1α occurs as two copies in bees: Implications for phylogenetic analysis of EF-1α sequences in insects. Molecular Biology and Evolution 15, 225–235.Google Scholar
Dittmar, K., Porter, M. L., Murray, S. and Whiting, M. F. (2006) Molecular phylogenetic analysis of nycteribiid and streblid bat flies (Diptera: Brachycera, Calyptratae): implications for host associations and phylogeographic origins. Molecular Phylogenetics and Evolution 38, 155–170.Google Scholar
FDA [Food and Drug Administration] (2004) Federal Food, Drug, and Cosmetic Act. As Amended through December 31, 2004. U.S. Department of Health and Human Services, Government Printing Office, Washington, DC. Available at: http://medical.cms.itri.org.tw/pdf/u01.pdf.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Fournier, D., Tindo, M., Kenne, M., Mbenoun Masse, P. S., Van Bossche, V., De Coninck, E. and Aron, S. (2012) Genetic structure, nestmate recognition and behaviour of two cryptic species of the invasive big-headed ant Pheidole megacephala . PLoS One 7(2): e31480. doi: 10.1371/journal.pone.0031480.Google Scholar
Giribet, G., Edgecombe, G. D. and Wheeler, W. C. (2001) Arthropod phylogeny based on eight molecular loci and morphology. Nature 413, 157–161.Google Scholar
Gunay, F., Alten, B., Simsek, F., Aldemir, A. and Linton, Y.-M. (2015) Barcoding Turkish Culex mosquitoes to facilitate arbovirus vector incrimination studies reveals hidden diversity and new potential vectors. Acta Tropica 143, 112–120.Google Scholar
Hajibabaei, M., Janzen, D.H., Burns, J.M., Hallwachs, W. and Hebert, P.D.N. (2006) DNA barcodes distinguish species of tropical Lepidoptera. Proceedings of the National Academy of Sciences of the United States of America 103, 968–971.Google Scholar
Hebert, P. D., Cywinska, A., Ball, S. L. and deWaard, J. R. (2003 a) Biological identifications through DNA barcodes. Proceedings of the Royal Society B 270, 313–321.Google Scholar
Hebert, P. D., Ratnasingham, S. and deWaard, J. R. (2003 b) Barcoding animal life: cytochrome c oxidase subunit divergences among closely related species. Proceedings of the Royal Society B 270, S96–99.Google Scholar
Hebert, P.D.N., Penton, E.H., Burns, J.M., Janzen, D. H. and Hallwachs, W. (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator . Proceedings of the National Academy of Sciences of the United States of America 101, 14812–14817.Google Scholar
Jones, Y. L., Peters, S. M., Weland, C., Ivanova, N. V. and Yancy, H. F. (2013) Potential use of DNA barcodes in regulatory science: identification of the U.S. Food and Drug Administration's “Dirty 22,” contributors to the spread of foodborne pathogens. Journal of Food Protection 76, 144–149. doi: 10.4315/0362-028X.JFP-12-168.Google Scholar
Jordaens, K., Goergen, G., Virgilio, M., Backeljau, T., Vokaer, A. and De Meyer, M. (2015) DNA barcoding to improve the taxonomy of the Afrotropical hoverflies (Insecta: Diptera: Syrphidae). PLoS One 10(10): e0140264. doi: 10.1371/journal.pone.0140264.Google Scholar
Kato, H., Cáceres, A. G., Gomez, E. A., Mimori, T., Uezato, H., Marco, J. D., Barroso, P.A., Iwata, H. and Hashiguchi, Y. (2008) Molecular mass screening to incriminate sand fly vectors of Andean-type cutaneous leishmaniasis in Ecuador and Peru. The American Journal of Tropical Medicine and Hygiene 79, 719–721.CrossRefGoogle ScholarPubMed
Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.Google Scholar
Kress, W. J., Wurdack, K. J., Zimmer, E. A., Weigt, L. A. and Janzen, D. H. (2005) Use of DNA barcodes to identify flowering plants. Proceedings of the National Academy of Sciences of the United States of America 102, 8369–8374. doi: 10.1073/pnas.0503123102.Google Scholar
May, R. M. (1988) How many species are there on Earth? Science 241, 1441–1449. doi: 10.1126/science.241.4872.1441.Google Scholar
Meyer, C. P. (2003) Molecular systematics of cowries (Gastropoda: Cypraeidae) and diversification patterns in the tropics. Biological Journal of the Linnean Society 79, 401–459.Google Scholar
Mukha, D. V., Sidorenko, A. P., Lazebnaya, I. V., Wiegmann, B. M. and Schal, C. (2000) Analysis of intra species polymorphism in the ribosomal DNA cluster of the cockroach Blattella germanica . Insect Molecular Biology 9, 217–222.Google Scholar
Murat, S., Hopfen, C. and McGregor, A. P. (2010) The function and evolution of Wnt genes in arthropods. Arthropod Structure & Development 39, 446–452. doi: 10.1016/j.asd.2010.05.007.Google Scholar
Nakano, A. and Honda, J. (2015) Use of DNA sequences to identify forensically important fly species and their distribution in the coastal region of Central California. Forensic Science International 253, 1–13. doi: 10.1016/j.forsciint.2015.05.001.Google Scholar
Ng'endo, R. N., Osiemo, Z. B. and Brandl, R. (2013) DNA barcodes for species identification in the hyperdiverse ant genus Pheidole (Formicidae: Myrmicinae). Journal of Insect Science 13, 27. Available online: http://www.insectscience.org/13.27.CrossRefGoogle Scholar
Nirmala, X., Hypsa, V. and Zurovec, M. (2001) Molecular phylogeny of Calyptratae (Diptera: Brachycera): the evolution of 18S and 16S ribosomal rDNAs in higher dipterans and their use in phylogenetic inference. Insect Molecular Biology 10, 475–485.Google Scholar
Nzelu, C. O., Cáceres, A. G., Arrunátegui-Jiménez, M. J., Lañas-Rosas, M. F., Yañez-Trujillano, H. H., Luna-Caipo, D.V., Holguín-Mauricci, C. E., Katakura, K., Hashiguchi, Y. and Kato, H. (2015) DNA barcoding for identification of sand fly species (Diptera: Psychodidae) from leishmaniasis-endemic areas of Peru. Acta Tropica 145, 45–51. doi: 10.1016/j.actatropica.2015.02.003.Google Scholar
Olsen, A. R. (1998 a) Regulatory action criteria for filth and other extraneous materials: I. Review of hard or sharp foreign objects as physical hazards in food. Regulatory Toxicology and Pharmacology 28, 181–189.Google Scholar
Olsen, A. R. (1998 b) Regulatory action criteria for filth and other extraneous materials: II. Allergenic mites: an emerging food safety issue. Regulatory Toxicology and Pharmacology 28, 190–198.CrossRefGoogle ScholarPubMed
Olsen, A. R. (1998 c) Regulatory action criteria for filth and other extraneous materials: III. Review of flies and foodborne enteric disease. Regulatory Toxicology and Pharmacology 28, 199–211.Google Scholar
Olsen, A. R., Gecan, J. S., Ziobro, G. S. and Bryce, J. R. (2001) Regulatory action criteria for filth and other extraneous materials: V. Strategy for evaluating hazardous and nonhazardous filth. Regulatory Toxicology and Pharmacology 33, 363–392.Google Scholar
Park, S. H., Zhang, Y., Piao, H., Yu, D. H., Jeong, H.J., Yoo, G. Y., Chung, U., Jo, T. H. and Hwang, J. J. (2009) Use of cytochrome c oxidase subunit I (COI) nucleotide sequences for identification of the Korean Luciliinae fly species (Diptera: Calliphoridae) in forensic investigations. Journal of Korean Medical Science 24, 1058–1063. doi: 10.3346/jkms.2009.24.6.1058.Google Scholar
Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.Google Scholar
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. and Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–701.Google Scholar
Simon, S., Schierwater, B. and Hadrys, H. (2010) On the value of Elongation factor-1α for reconstructing pterygote insect phylogeny. Molecular Phylogenetics and Evolution 54, 651–656.Google Scholar
Schubert, M., Holland, L. Z., Holland, N. D. and Jacobs, D.K. (2000) A phylogenetic tree of the Wnt genes based on all available full-length sequences, including five from the cephalochordate amphioxus. Molecular Biology and Evolution 17, 1896–1903.Google Scholar
Sulaiman, I. M., Anderson, M., Khristova, M., Tang, K., Sulaiman, N., Phifer, E., Simpson, S. and Kerdahi, K. (2011) Development of a PCR-restriction fragment length polymorphism protocol for rapid detection and differentiation of four cockroach vectors (Group I “Dirty 22” species) responsible for food contamination and spreading of foodborne pathogens: public health importance. Journal of Food Protection 74, 1883–1890. doi: 10.4315/0362-028X.JFP-11-242.Google Scholar
Sulaiman, I. M., Anderson, M., Oi, D. H., Simpson, S. and Kerdahi, K. (2012) Multilocus genetic characterization of two ant vectors (Group II “Dirty 22” species) known to contaminate food and food products and spread foodborne pathogens. Journal of Food Protection 75, 1447–1452. doi: 10.4315/0362-028X.JFP-12-098.CrossRefGoogle ScholarPubMed
Sulaiman, I. M., Fayer, R., Bern, C., Gilman, R. H., Trout, J.M., Schantz, P.M., Das, P., Lal, A. A. and Xiao, L. (2003 a) Triosephosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis . Emerging Infectious Diseases 9, 1444–1452.CrossRefGoogle ScholarPubMed
Sulaiman, I. M., Fayer, R., Lal, A. A., Trout, J. M., Schaefer, F. W. III and Xiao, L. (2003 b) Molecular characterization of microsporidia indicates that wild mammals harbor host-adapted Enterocytozoon spp. as well as human-pathogenic Enterocytozoon bieneusi . Applied and Environmental Microbiology 69, 4495–4501. doi: 10.1128/AEM.69.8.4495-4501.2003.Google Scholar
Sulaiman, I. M., Jacobs, E., Simpson, S. and Kerdahi, K. (2014) Molecular identification of isolated fungi from unopened containers of Greek yorgurt by DNA sequencing of internal transcribed spacer region. Pathogens 3, 499–509. doi:10.3390/pathogens3030499.Google Scholar
Sulaiman, I. M., Lal, A. A. and Xiao, L. (2001) A population genetic study of the Cryptosporidium parvum human genotype parasites. Journal of Eukaryotic Microbiology (Suppl. 1), 24S–27S.Google Scholar
Sulaiman, I. M., Lal, A. A. and Xiao, L. (2002) Molecular phylogeny and evolutionary relationships of Cryptosporidium parasites at the actin locus. Journal of Parasitology 88, 388–394.Google Scholar
Sulaiman, I. M., Torres, P., Simpson, S., Kerdahi, K. and Ortega, Y. (2013) Sequence characterization of heat shock protein gene of Cyclospora cayetanensis isolates from Nepal, Mexico, and Peru. Journal of Parasitology 99, 379–382. doi: 10.1645/GE-3114.1.Google Scholar
Varadínová, Z., Wang, Y. J., Kučerová, Z., Stejskal, V., Opit, G., Cao, Y., Li, F. J. and Li, Z. (2015) COI barcode based species-specific primers for identification of five species of stored-product pests from genus Cryptolestes (Coleoptera: Laemophloeidae). Bulletin of Entomological Research 105, 202–209.Google Scholar
von Beeren, C., Stoeckle, M. Y., Xia, J., Burke, G. and Kronauer, D. J. (2014) Interbreeding among deeply divergent mitochondrial lineages in the American cockroach (Periplaneta americana). Scientific Reports 5, 8297. doi:10.1038/srep08297.Google Scholar
Yue, Q., Wu, K., Qiu, D., Hu, J., Liu, D., Wei, X., Chen, J. and Cook, C. E. (2014) A formal re-description of the cockroach Hebardina concinna anchored on DNA Barcodes confirms wing polymorphism and identifies morphological characters for field identification. PLoS ONE 9(9): e106789. doi: 10.1371/journal.pone.0106789.Google Scholar