Skip to main content
SpringerLink
Log in

A metagenomic assessment of the bacteria associated with Lucilia sericata and Lucilia cuprina (Diptera: Calliphoridae)

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Lucilia Robineau-Desvoidy (Diptera: Calliphoridae) is a blow fly genus of forensic, medical, veterinary, and agricultural importance. This genus is also famous because of its beneficial uses in maggot debridement therapy (MDT). Although the genus is of considerable economic importance, our knowledge about microbes associated with these flies and how these bacteria are horizontally and trans-generationally transmitted is limited. In this study, we characterized bacteria associated with different life stages of Lucilia sericata (Meigen) and Lucilia cuprina (Wiedemann) and in the salivary gland of L. sericata by using 16S rDNA 454 pyrosequencing. Bacteria associated with the salivary gland of L. sericata were also characterized using light and transmission electron microscopy (TEM). Results from this study suggest that the majority of bacteria associated with these flies belong to phyla Proteobacteria, Firmicutes, and Bacteroidetes, and most bacteria are maintained intragenerationally, with a considerable degree of turnover from generation to generation. In both species, second-generation eggs exhibited the highest bacterial phylum diversity (20 % genetic distance) than other life stages. The Lucilia sister species shared the majority of their classified genera. Of the shared bacterial genera, Providencia, Ignatzschineria, Lactobacillus, Lactococcus, Vagococcus, Morganella, and Myroides were present at relatively high abundances. Lactobacillus, Proteus, Diaphorobacter, and Morganella were the dominant bacterial genera associated with a survey of the salivary gland of L. sericata. TEM analysis showed a sparse distribution of both Gram-positive and Gram-negative bacteria in the salivary gland of L. sericata. There was more evidence for horizontal transmission of bacteria than there was for trans-generational inheritance. Several pathogenic genera were either amplified or reduced by the larval feeding on decomposing liver as a resource. Overall, this study provides information on bacterial communities associated with different life stages of Lucilia and their horizontal and trans-generational transmission, which may help in the development of better vector-borne disease management and MDT methods.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Amendt J, Campobasso CP, Gaudry E, Reiter C, LeBlanc HN, Hall MJ, Entomology EAFE (2007) Best practice in forensic entomology—standards and guidelines. Int J Legal Med 121:90–104

    Article  PubMed  Google Scholar 

  • Anderson GS (2000) Minimum and maximum development rates of some forensically important Calliphoridae (Diptera). J Forensic Sci 45:824–832

    Article  CAS  PubMed  Google Scholar 

  • Arora S, Baptista C, Lim CS (2011) Maggot metabolites and their combinatory effects with antibiotic on Staphylococcus aureus. Ann Clin Microb Anti 10:6, 10.1186/1476-0711-10-6

    Article  Google Scholar 

  • Ashworth JR, Wall R (1994) Responses of the sheep blowflies Lucilia sericata and L. cuprina to odour and the development of semiochemical baits. Med Vet Entomol 8:303–309

    Article  CAS  PubMed  Google Scholar 

  • Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI (2005) Host-bacterial mutualism in the human intestine. Science 307:1915–1920

    Article  PubMed  Google Scholar 

  • Bexfield A, Bond AE, Morgan C, Wagstaff J, Newton RP, Ratcliffe NA, Dudley E, Nigam Y (2010) Amino acid derivatives from Lucilia sericata excretions/secretions may contribute to the beneficial effects of maggot therapy via increased angiogenesis. Br J Dermatol 162:554–562

    Article  CAS  PubMed  Google Scholar 

  • Cazander G, van Veen KE, Bernards AT, Jukema GN (2009a) Do maggots have an influence on bacterial growth? A study on the susceptibility of strains of six different bacterial species to maggots of Lucilia sericata and their excretions/secretions. J Tissue Viability 18:80–87

    Article  CAS  PubMed  Google Scholar 

  • Cazander G, van Veen KE, Bouwman LH, Bernards AT, Jukema GN (2009b) The influence of maggot excretions on PAO1 biofilm formation on different biomaterials. Clin Orthop Relat Res 467:536–545

    Article  PubMed  Google Scholar 

  • Cazander G, Veerdonk M, Vandenbroucke-Grauls CJE, Schreurs MJ, Jukema G (2010) Maggot excretions inhibit biofilm formation on biomaterials. Clin Orthop Relat Res 468:2789–2796

    Article  PubMed  PubMed Central  Google Scholar 

  • Cazander G, Pritchard DI, Nigam Y, Jung W, Nibbering PH (2013) Multiple actions of Lucilia sericata larvae in hard-to-heal wounds: larval secretions contain molecules that accelerate wound healing, reduce chronic inflammation and inhibit bacterial infection. Bioessays 35:1083–1092

    Article  CAS  PubMed  Google Scholar 

  • Chao A, Bunge J (2002) Estimating the number of species in a stochastic abundance model. Biometrics 58:531–539

    Article  PubMed  Google Scholar 

  • Clark K, Evans L, Wall R (2006) Growth rates of the blowfly, Lucilia sericata, on different body tissues. Forensic Sci Int 156:145–149

    Article  CAS  PubMed  Google Scholar 

  • Cole JR, Wang Q, Cardenas E (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–145

    Article  CAS  PubMed  Google Scholar 

  • Dharne MS, Gupta AK, Rangrez AY, Ghate HV, Patole MS, Shouche YS (2008) Antibacterial activities of multi drug resistant Myroides odoratimimus bacteria isolated from adult flesh flies (Diptera: sarcophagidae) are independent of metallo beta-lactamase gene. Braz J Microbiol 39:397–404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dowd S, Callaway T, Wolcott R, Sun Y, McKeehan T, Hagevoort R, Edrington T (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8:125

    Article  PubMed  PubMed Central  Google Scholar 

  • Fischer OA, Matlova L, Dvorska L, Svastova P, Bartl J, Weston RT, Pavlik I (2004) Blowflies Calliphora vicina and Lucilia sericata as passive vectors of Mycobacterium avium subsp. avium, M. a. paratuberculosis and M. a. hominissuis. Med Vet Entomol 18:116–122

    Article  CAS  PubMed  Google Scholar 

  • Fleischmann W (2004) Maggot debridement. In: Banwell P, Ziegler U, Téot L (eds) Surgery in wounds. Springer, Berlin Heidelberg, pp 125–128. doi:10.1007/978-3-642-59307-9_13

    Chapter  Google Scholar 

  • Garrity G, Bell J, Lilburn T (2004) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, New York

    Google Scholar 

  • Grassberger M, Reiter C (2001) Effect of temperature on Lucilia sericata (Diptera: Calliphoridae) development with special reference to the isomegalen- and isomorphen-diagram. Forensic Sci Int 120:32–36

    Article  CAS  PubMed  Google Scholar 

  • Greenberg B (1968) Model for destruction of bacteria in the midgut of blow fly maggots. J Med Entomol 5:31–38

    Article  CAS  PubMed  Google Scholar 

  • Greenberg B (1973) Biology and disease transmission vol volume 2. Flies and disease. Princeton University Press, Princeton

    Google Scholar 

  • Gupta AK, Nayduch D, Verma P, Shah B, Ghate HV, Patole MS, Shouche YS (2012) Phylogenetic characterization of bacteria in the gut of house flies (Musca domestica L.). FEMS Microbiol Ecol 79:581–593

    Article  CAS  PubMed  Google Scholar 

  • Gupta AK, Rastogi G, Nayduch D, Sawant SS, Bhonde RR, Shouche YS (2014) Molecular phylogenetic profiling of gut-associated bacteria in larvae and adults of flesh flies Med Vet Entomol doi:10.1111/mve.12054

  • Hall RD (2005) Entomology and the law—flies as forensic indicators. J Med Entomol 42:922–922

    Google Scholar 

  • Hamady M, Lozupone C, Knight R (2009) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data ISME J 4:17–27 doi:http://www.nature.com/ismej/journal/v4/n1/suppinfo/ismej200997s1.html

  • Han M, Zmasek C (2009) PhyloXML: XML for evolutionary biology and comparative genomics. BMC Bioinformatics 10:356

    Article  PubMed  PubMed Central  Google Scholar 

  • Harris LG, Bexfield A, Nigam Y, Rohde H, Ratcliffe NA, Mack D (2009) Disruption of Staphylococcus epidermidis biofilms by medicinal maggot Lucilia sericata excretions/secretions. Int J Artif Organs 32:555–564

    CAS  PubMed  Google Scholar 

  • Henry S, DeMaria A Jr, McCabe WR (1983) Bacteremia due to Fusobacterium species. Am J Med 75:225–231

    Article  CAS  PubMed  Google Scholar 

  • Hilker M, Meiners T (2002) Chemoecology of insect eggs and egg deposition. Blackwell Publishing, Berlin

    Google Scholar 

  • Hurst GD, Jiggins FM (2000) Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerg Infect Dis 6:329–336

    Article  CAS  PubMed  PubMed Central  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  PubMed  Google Scholar 

  • Kerridge A, Lappin-Scott H, Stevens JR (2005) Antibacterial properties of larval secretions of the blowfly. Lucilia sericata Med Vet Entomol 19:333–337

    Article  CAS  PubMed  Google Scholar 

  • Lam K, Babor D, Duthie B, Babor EM, Moore M, Gries G (2007) Proliferating bacterial symbionts on house fly eggs affect oviposition behaviour of adult flies. Anim Behav 74:81–92

    Article  Google Scholar 

  • Li F, Wantuch HA, Linger RJ, Belikoff EJ, Scott MJ (2014) Transgenic sexing system for genetic control of the Australian sheep blow fly Lucilia cuprina Insect Biochem Mol Biol doi:10.1016/j.ibmb.2014.06.001

  • Liu Y, Yang Y, Zhao F, Fan X, Zhong W, Qiao D, Cao Y (2013) Multi-drug resistant Gram-negative enteric bacteria isolated from flies at Chengdu airport, China. Southeast Asian J Trop Med Public Health 44:988–996

    CAS  PubMed  Google Scholar 

  • Ma J, Benson AK, Kachman SD, Hu Z, Harshman LG (2012a) Drosophila melanogaster selection for survival of Bacillus cereus infection: life history trait indirect responses Int J Evol Biol 2012:935970 doi:10.1155/2012/935970

  • Ma Q, Fonseca A, Liu W, Fields AT, Pimsler ML, Spindola AF, Tarone AM, Crippen TL, Tomberlin JK, Wood TK (2012b) Proteus mirabilis interkingdom swarming signals attract blow flies. ISME J 6:1356–1366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahajan GB, Balachandran L (2012) Antibacterial agents from actinomycetes—a review. Front Biosci (Elite Ed) 4:240–253

    Article  Google Scholar 

  • Maldonado MA, Centeno N (2003) Quantifying the potential pathogens transmission of the blowflies (Diptera: Calliphoridae). Mem Inst Oswaldo Cruz 98:213–216

    Article  PubMed  Google Scholar 

  • Martin B, Chadwick W, Yi T, Park SS, Lu D, Ni B, Gadkaree S, Farhang K, Becker KG, Maudsley S (2012) VENNTURE—a novel Venn diagram investigational tool for multiple pharmacological dataset analysis. PLoS ONE 7:e36911. doi:10.1371/journal.pone.0036911PONE-D-11-21759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mollenhauer HH (1964) Plastic embedding mixtures for use in electron-microscopy Stain Technol:111–114

  • Mowlavi G, Nateghpour M, Teimoori S, Amin A, Noohi F, Kargar F (2011) Fatal nosocomial myiasis caused by Lucilia sericata. J Hosp Infect 78:338–339

    Article  PubMed  Google Scholar 

  • Mumcuoglu KY (2001) Clinical applications for maggots in wound care. Am J Clin Dermatol 2:219–227

    Article  CAS  PubMed  Google Scholar 

  • Mumcuoglu KY, Miller J, Mumcuoglu M, Friger M, Tarshis M (2001) Destruction of bacteria in the digestive tract of the maggot of Lucilia sericata (Diptera: Calliphoridae). J Med Entomol 38:161–166

    Article  CAS  PubMed  Google Scholar 

  • Nawrocki E, Eddy S (2007) Query-dependent banding (QDB) for faster RNA similarity searches. PLOS Comput Biol 3:0540–0554

    Article  CAS  Google Scholar 

  • Nawrocki E, Kolbe D, Eddy S (2009) Infernal 1.0: inference of RNA alignments. Bioinformatics 25:1335–1337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nigam Y, Bexfield A, Thomas S, Ratcliffe NA (2006) Maggot therapy: the science and implication for CAM part II—maggots combat infection. eCAM 3:303–308. doi:10.1093/ecam/nel022

    PubMed  PubMed Central  Google Scholar 

  • Niu BF, Fu LM, Sun SL, Li WZ (2010) Artificial and natural duplicates in pyrosequencing reads of metagenomic data. BMC Bioinforma 11:187. doi:10.1186/1471-2105-11-187

    Article  Google Scholar 

  • Ponnusamy L, Xu N, Nojima S, Wesson DM, Schal C, Apperson CS (2008) Identification of bacteria and bacteria-associated chemical cues that mediate oviposition site preferences by Aedes aegypti. Proc Natl Acad Sci USA 105:9262–9267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490

    Article  PubMed  PubMed Central  Google Scholar 

  • Raghava Rao KV, Siva Kumar K, Rao DB, Raghava Rao T (2012) Isolation and characterization of antagonistic actinobacteria from mangrove soil. J Biochem Technol 3:361–365

    Google Scholar 

  • Raj A, Kumar S, Singh SK, Kumar M (2013) Characterization of a new Providencia sp. Strain X1 producing multiple xylanases on wheat bran Scientific World Journal doi:10.1155/2013/386769

  • R Development Core Team (2006) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sanford MR, Whitworth TL, Phatak DR (2014) Human wound colonization by Lucilia eximia and Chrysomya rufifacies (Diptera: Calliphoridae): myiasis, perimortem, or postmortem colonization? J Med Entomol 51:716–719

    Article  PubMed  Google Scholar 

  • Schröder R, Hilker M (2008) The relevance of background odor in resource location by insects: a behavioral approach. BioSci 58:308–316

    Article  Google Scholar 

  • Shannon CE (1948) A mathematical theory of communication. Bell System Tech J 27:379–423

    Article  Google Scholar 

  • Sherman RA (2009) Maggot therapy takes us back to the future of wound care: new and improved maggot therapy for the 21st century. J Diabetes Sci Technol 3:336–344

    Article  PubMed  PubMed Central  Google Scholar 

  • Sherman RA, Pechter EA (1988) Maggot therapy: a review of the therapeutic applications of fly larvae in human medicine, especially for treating osteomyelitis. Med Vet Entomol 2:225–230

    Article  CAS  PubMed  Google Scholar 

  • Sherman OA, Tran JMT (1994) A simple, sterile food source for rearing the larvae of Lucilia sericata (Diptera: Calliphoridae). Med Vet Entomol 9:393–398

    Article  Google Scholar 

  • Sherman RA, Hall MJ, Thomas S (2000) Medicinal maggots: an ancient remedy for some contemporary afflictions. Annu Rev Entomol 45:55–81

    Article  CAS  PubMed  Google Scholar 

  • Singh B, Wells JD (2013) Molecular systematics of the Calliphoridae (Diptera: Oestroidea): evidence from one mitochondrial and three nuclear genes. J Med Entomol 50:15–23

    Article  CAS  PubMed  Google Scholar 

  • Spiteller D, Dettner K, Boland W (2000) Gut bacteria may be involved in interactions between plants, herbivores and their predators: microbial biosynthesis of N-acylglutamine surfactants as elicitors of plant volatiles. Biol Chem 381:755–762

    Article  CAS  PubMed  Google Scholar 

  • Steenvoorde P, Buddingh TJ, van Engeland A, Oskam J (2005) Maggot therapy and the “yuk” factor: an issue for the patient? Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society 13:350–352 doi:10.1111/j.1067-1927.2005.130319.x

  • Stevens J, Wall R (1996) Species, sub-species and hybrid populations of the blowflies Lucilia cuprina and Lucilia sericata (Diptera:Calliphoridae). Proc Biol Sci 263:1335–1341

    Article  CAS  PubMed  Google Scholar 

  • Swofford D (2003) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4 edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Sze SH, Dunham JP, Carey B, Chang PL, Li F, Edman RM, Fjeldsted C, Scott MJ, Nuzhdin SV, Tarone AM (2012) A de novo transcriptome assembly of Lucilia sericata (Diptera: Calliphoridae) with predicted alternative splices, single nucleotide polymorphisms and transcript expression estimates. Insect Mol Biol 21:205–221

    Article  CAS  PubMed  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  PubMed  PubMed Central  Google Scholar 

  • Tarone AM (2007) Lucilia Sericata development: plasticity, population differences, and gene expression. Michigan State University

  • Tarone AM, Foran DR (2006) Components of developmental plasticity in a Michigan population of Lucilia sericata (Diptera: Calliphoridae). J Med Entomol 43:1023–1033

    Article  PubMed  Google Scholar 

  • Tarone AM, Foran DR (2008) Generalized additive models and Lucilia sericata growth: assessing confidence intervals and error rates in forensic entomology. J Forensic Sci 53:942–948

    Article  PubMed  Google Scholar 

  • Tarone AM, Jennings KC, Foran DR (2007) Aging blow fly eggs using gene expression: a feasibility study. J Forensic Sci 52:1350–1354

    Article  CAS  PubMed  Google Scholar 

  • Tarone AM, Picard CJ, Spiegleman C, Foran DR (2011) Population and temperature effects on Lucilia sericata (Diptera: Calliphoridae) body size and minimum development time. J Med Entomol 48:1062–1068

    Article  CAS  PubMed  Google Scholar 

  • Tomberlin JK, Mohr R, Benbow ME, Tarone AM, VanLaerhoven S (2011) A roadmap for bridging basic and applied research in forensic entomology. Annu Rev Entomol 56:401–421

    Article  CAS  PubMed  Google Scholar 

  • Tomberlin JK, Crippen TL, Tarone AM, Singh B, Adams K, Rezenom YH, Benbow ME, Flores M, Longnecker M, Pechal JL, Russel DH, Beier RC, Wood TK (2012) Interkingdom responses of flies to bacteria mediated by fly physiology and bacterial quorum sensing. Anim Behav 84:1449–1456

    Article  Google Scholar 

  • Toth E, Kovacs G, Schumann P, Kovacs AL, Steiner U, Halbritter A, Marialigeti 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

    Article  CAS  PubMed  Google Scholar 

  • van der Plas MJ, Jukema GN, Wai SW, Dogterom-Ballering HC, Lagendijk EL, van Gulpen C, van Dissel JT, Bloemberg GV, Nibbering PH (2008) Maggot excretions/secretions are differentially effective against biofilms of Staphylococcus aureus and Pseudomonas aeruginosa. J Antimicrob Chemother 61:117–122

    Article  PubMed  Google Scholar 

  • van der Plas MJ, Baldry M, van Dissel JT, Jukema GN, Nibbering PH (2009) Maggot secretions suppress pro-inflammatory responses of human monocytes through elevation of cyclic AMP. Diabetologia 52:1962–1970

    Article  PubMed  PubMed Central  Google Scholar 

  • Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, Xie G, Haft DH, Sait M, Badger J, Barabote RD, Bradley B, Brettin TS, Brinkac LM, Bruce D, Creasy T, Daugherty SC, Davidsen TM, DeBoy RT, Detter JC, Dodson RJ, Durkin AS, Ganapathy A, Gwinn-Giglio M, Han CS, Khouri H, Kiss H, Kothari SP, Madupu R, Nelson KE, Nelson WC, Paulsen I, Penn K, Ren Q, Rosovitz MJ, Selengut JD, Shrivastava S, Sullivan SA, Tapia R, Thompson LS, Watkins KL, Yang Q, Yu C, Zafar N, Zhou L, Kuske CR (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75:2046–2056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei T, Miyanaga K, Tanji Y (2014a) Persistence of antibiotic-resistant and -sensitive Proteus mirabilis strains in the digestive tract of the housefly (Musca domestica) and green bottle flies (Calliphoridae). Appl Microbiol Biotechnol 98:8357–8366

    Article  CAS  PubMed  Google Scholar 

  • Wei T, Ishida R, Miyanaga K, Tanji Y (2014b) Seasonal variations in bacterial communities and antibiotic-resistant strains associated with green bottle flies (Diptera: Calliphoridae). Appl Microbiol Biotechnol 98:4197–4208

    Article  CAS  PubMed  Google Scholar 

  • Whitworth T (2006) Keys to the genera and species of blow flies (Diptera : Calliphoridae) of America North of Mexico. Proc Entomol Soc Wash 108:689–725

    Google Scholar 

  • Wright ES, Yilmaz LS, Noguera DR (2012) DECIPHER, a search-based approach to chimera identification for 16S rRNA sequences. Appl Environ Microbiol 78:717–725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng L, Crippen TL, Singh B, Tarone AM, Dowd S, Yu Z, Wood TK, Tomberlin JK (2013) A survey of bacterial diversity from successive life stages of black soldier fly (Diptera: Stratiomyidae) by using 16S rDNA pyrosequencing. J Med Entomol 50:647–658

    Article  CAS  PubMed  Google Scholar 

  • Zurek L, Ghosh A (2014) Insect represent a link between food animal farms and the urban environment for antibiotic resistant trait. Appl Environ Microbiol 80:3562–3567

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Dr. Robert Droleskey for his assistance with transmission electron microscopy of the salivary gland. Funding for B.S., A.M.T., L.Z., A.T.F., M.F., and J.K.T. was provided partially by the Texas Agrilife Research and the College of Agriculture and Life Sciences at Texas A&M University, College Station, TX. Additional funding for B.S., A.M.T., T.L.C., and J.K.T. was provided by the National Institute of Justice, Office of Justice Programs, U.S. Department of Justice through Grant 2010-DN-BX-K243. B.S. was also supported by a start up fund from the College of Humanities and Sciences of Virginia Commonwealth University, Richmond, VA. We also thank anonymous reviewers for their suggestions that improved this article substantially. Points of view in this document are those of the authors and do not necessarily represent the official position or policies of the U.S. Department of Justice, Department of the Army, Department of Defense, or U.S. Government. Mention of trade names, companies, or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement of the products by the U.S. Department of Agriculture.

Conflict of interest

The authors have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Entomology, Texas A&M University, College Station, TX, USA

    Baneshwar Singh, Longyu Zheng, Andrew T. Fields, Micah Flores, Jeffery K. Tomberlin & Aaron M. Tarone

  2. Department of Forensic Science, Virginia Commonwealth University, 1015 Floyd Avenue, Richmond, VA, 23284, USA

    Baneshwar Singh

  3. Southern Plains Agricultural Research Center, Agricultural Research Service, USDA, College Station, TX, USA

    Tawni L. Crippen & Longyu Zheng

  4. State Key Laboratory of Agricultural Microbiology, National Engineering Research Center of Microbe Pesticide, Huazhong Agricultural University, Wuhan, China

    Longyu Zheng & Ziniu Yu

  5. School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY, USA

    Andrew T. Fields

  6. Tianjin Institute of Industrial Biotechnology, Chinese Academy of Science, Tianjin, China

    Qun Ma

  7. Department of Chemical Engineering, The Pennsylvania State University, University Park, PA, USA

    Thomas K. Wood

  8. MR DNA Molecular Research LP, Shallowater, TX, USA

    Scot E. Dowd

  9. Walter Reed Army Institute of Research, Silver Spring, MD, USA

    Micah Flores

Authors
  1. Baneshwar Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tawni L. Crippen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Longyu Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andrew T. Fields
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ziniu Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qun Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Thomas K. Wood
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Scot E. Dowd
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Micah Flores
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jeffery K. Tomberlin
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Aaron M. Tarone
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Baneshwar Singh.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 2227 kb)

ESM 2

(XLSX 35 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Singh, B., Crippen, T.L., Zheng, L. et al. A metagenomic assessment of the bacteria associated with Lucilia sericata and Lucilia cuprina (Diptera: Calliphoridae). Appl Microbiol Biotechnol 99, 869–883 (2015). https://doi.org/10.1007/s00253-014-6115-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-014-6115-7

Keywords

Search

Navigation