Aerobic Bacterial Community of American Cockroach Periplaneta americana,a Step toward Finding Suitable Paratransgenesis Candidates
AbstractBackground: Cockroaches mechanically spread pathogenic agents, however, little is known about their gut microbiota. Identification of midgut microbial community helps targeting novel biological control strategies such as paratransgenesis. Here the bacterial microbiota of Periplaneta americana midgut, were identified and evaluated for finding proper paratransgenesis candidate.Methods: Midgut of specimens were dissected and cultivated in different media. The bacterial isolates were then identified using the phenotypic and 16S-rRNA sequencing methods.Results: The analytical profile index (API) kit showed presence of 11 bacterial species including: Escherichia coli, Shigella flexineri, Citrobacter freundii, E. vulneris, Enterobacter cloacae, Yersinia pseudotuberculosis, Y.intermedia, Leclericia adecarboxylata, Klebsiella oxytoca, K. planticola, and Rahnella aquatilis in the cockroach midguts. The first three species are potentially symbiotic whereas others are transient. The conventional platingmethod revealed presence of only four isolates of Salmonella, E. coli, and Proteus which in three cases mismatched with API and 16S-rRNA genotyping. The API correctly identified the four isolates as Shigella flexneri, Citrobacter freundii, and E. coli (n= 2). 16S-rRNA sequence analysis confirmed the API results; however the C. freundii sequencewas identical with C. murliniae indicating lack of genetic variation in the gene between these two closely related species.Conclusion: A low number of potentially symbiotic bacteria were found in the American cockroach midguts. Among them Enterobacter cloacae is a potential candidate for paratransgenesis approach whereas other bacteria are pathogens and are not useful for the approach. Data analysis showed that identification levels increase from the conventional to API and to genotyping respectively.
Allotey J, Mpuchane S, Gashe BA, Simpanya M, Matsheka I (2009) Trapping of Blattella germanica (L) populations in human dwellings in Gaborone, Bot- swana. J Appl Zoo Res. 20(2): 175–188.
Arlian LG (2002) Arthropod allergens and human health. Annu Rev Entomol. 47:395–433.
Arruda LK, Vailes LD, Ferriani VPL, Santos ABR, Pomes A, Chapman MD (2001) Cockroach allergens and asthma. J Allergy Clin Immunol. 107: 419–428.
Badger JL, Stins MF, Kim KS (1999) Citrobacter freundii invades and repli- cates in human brain microvascular endothelial cells. Infect Immun. 67(8):4208–4215.
Barney M, Volgyi A, Navarro A, Ryder D (2001) Riboprinting and 16S rRNA gene sequencing for identification of brewery Pediococcus isolates. Appl Environ Microbiol. 67(2): 553–560.
Bell WJ, Roth LM, Nalepa CA (2007) Microbes: Unseen influence. In: Bell WJ, Roth LM, Nalepa CA (Eds): Cock- roaches: ecology, behavior, and natural history, The Johns Hopkins University Press, Baltimore, pp. 76–88.
Bignell DE (1977) Some observations on the distribution of gut flora in the american cockroach, Periplaneta americana. J Invertebr Pathol. 29: 338–343.
Blaiotta G, Fusco V, Ercolini D, Pepe O, Coppola S (2010) Diversity of Staphyl- coccus species strains based on partial kat (catalase) gene sequences and de- sign of a PCR-restriction fragment length polymorphism assay for identi- fication and differentiation of coagulase- positive species (S. aureus, S. delphini, S. hyicus, S. schleiferi subsep. coagulans). J Clin Microbiol. 48: 192–201.
Bosshard PP, Zbinden R, Abels S, Böddinghaus B, Altwegg M, Böttger EC (2006) 16S rRNA gene sequencing versus the API 20 NE system and the Vitek 2 ID-GNB card for identification of nonfermenting gram-negative bac- teria in the clinical laboratory. J Clin Microbiol. 44: 1359–1366.
Bracke JW, Cruden DL, Markovetz AJ (1979) Intestinal microbial flora of the American cockroach. Appl Environ Microbiol. 38: 945–955.
Burgess NRH, McDermott SN, Whiting J (1973) Aerobic bacteria occurring in the hind-gut of the cockroach, Blatta orientalis. J Hyg (Lond). 71: 1–7.
Cruden DL, Markovetz AJ (1984) Microbial aspects of the cockroach hindgut. Arch Microbiol. 138: 131–139.
Cruden DL, Markovetz AJ (1987) Microbial ecology of the cockroach gut. Annu Rev Microbiol. 41: 617–643.
Chavshin AR, Oshaghi MA, Vatandoost H, Pourmand MR, Raeisi A, Enayati AA, Mardani N, Ghoorchian S (2012) Iden- tification of bacterial microflora in the midgut of the larvae and adult of wild caught Anopheles stephensi: a step toward finding suitable paratransgenesis candidates. Acta Trop. 121(2): 129–134.
Chavshin AR, Oshaghi MA, Vatandoost H, Raeisi A, Zarenejad F (2013) Escherichia coli expressing a green fluo- rescent protein (GFP) in Anopheles stephensi: a preliminary model for paratransgenesis. Symbiosis. 60(1):17–24.
Clarridge JE (2004) Impact of 16S rRNA gene sequence analysis for identifi- cation of bacteria on clinical micro- biology and infectious diseases. Clin Microbiol Rev. 17(4): 840–862.
Cloud JL, Conville PS, Croft A, Harmsen D, Witebsky FG, Carroll KC (2004) Eval- uation of partial 16S ribosomal DNA sequencing for identification of Nocardia species by using the MicroSeq 500 system with an expanded database. J Clin Microbiol. 42: 578–584.
Eisenstein BI (1990) New molecular tech- niques for microbial epidemiology and the diagnosis of infectious diseases. J Infect Dis.161: 595–602.
Enayati AA, Motevalli Haghi F (2007) Bi- ochemistry of pyrethroid resistance in German cockroach (Dictyoptera, Bla- tellidae) from hospitals of Sari, Iran. Iran Biomed J. 11(4): 251–258.
Erme F, Certel M, Karakas B (2009) Identi- fication of Bacillus species isolated from ropey breads both with classical methods and API identification kits. J Pharm Bioallied Sci . 22(2): 201–210.
Farber JM (1996) An introduction to the hows and whys of molecular typing. J Food Prot. 59: 1091–1101.
Geraghty L, Booth M, Rowan N, Fogarty A (2013) Investigations on the efficacy of routinely used phenotypic methods compared to genotypic approaches for the identification of staphylococcal species isolated from companion an- imals in Irish veterinary hospitals. Ir Vet J. 66(1): 7.
Gouveia C, Asensi MD, Zahner V, Rangel EF, Oliveira SM (2008) Study on the bacterial midgut microbiota associated to different Brazilian populations of Lutzomyia longipalpis (Lutz and Neiva) (Diptera: Psychodidae). Neotrop Ento- mol. 37(5): 597–601.
Grant KA, Kroll RG (1993) Molecular biol- ogy techniques for the rapid detection and characterisation of food borne bac- teria. Food Sci Techno1 Today. 7: 80–88.
Hall L, Doerr KA, Wohlfiel SL, Roberts GD (2003) Evaluation of the MicroSeq sys- tem for identification of mycobacteria by 16S ribosomal DNA sequencing and its integration into a routine clin- ical mycobacteriology laboratory. J Clin Microbiol. 41: 1447–1453.
Hashemi-Aghdam SS, Oshaghi MA (2013) A checklist of Iranian cockroaches (Blattodea) with description of Poly- phaga sp as a new species in Iran. J Arthropod-Borne Dis. (In press)Harmsen D, Karch H (2004) 16S rDNA for diagnosing pathogens: a living tree. ASM News. 70: 19–24.
Hillesland H, Read A, Subhadra B, Hurwitz I, McKelvey R, Ghosh K, Das P, Durvasula R (2008) Identification of aerobic gut bacteria from the kala azar vector, Phlebotomus argentipes: a plat- form for potential paratransgenic ma- nipulation of sand flies. Am J Trop Med Hyg. 79(6): 881–886.
Hurwitz I, Fieck A, Read A, Hillesland H, Klein N, Kang A, Durvasula R (2011) Paratransgenic control of vector borne diseases. Int J Biol Sci. 7(9): 1334–1344.
Husseneder C, Grace JK (2005) Genetically engineered termite gut bacteria (En- terobacter cloacae) deliver and spread foreign genes in termite colonies. Appl Microbiol Biotechnol. 68: 360–367.
Janda JM, Abbott SL (2007) 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. J Clin Microbiol.45(9): 2761–2764.
Jiang H, Zhang JM, Wang JP, Yang B, Liu CF, Lu J, Hu YY (2007) Genetic en- gineering of Periplaneta fuliginosa densovirus as an improved biopesticide. Arch Virol. 52(2): 383–394.
Kane MD, Breznak JA (1991) Effect of host diet on production of organic acids and methane by cockroach gut bacteria. Appl Environ Microbiol. 57(9): 2628–2634.
Karimian F, Sedaghat MM, Oshaghi MA, Mohtarami F, Sanei Dehkordi A, Koosha M, Akbari S, Hashemi Aghdam SS (2011) Utility of filter paper for pre- serving insects, bacteria, and host res- ervoir DNA for molecular testing. Iran J Arthropod-Borne Dis. 5(2): 42–50.
Keller R, Pedroso MZ, Ritchmann R, Silva RM (1998) Occurrence of virulence- associated properties in Enterobacter cloacae. Infect Immun. 66 (2): 645–649.
Krishna NK, Cunnion KM (2012) Role of molecular diagnostics in the management of infectious disease emergencies. Med Clin North Am. 96(6): 1067–1078.
LaClaire LL, Facklam RR (2000) Compar- ison of three commercial rapid iden- tification systems for the unusual gram-positive cocci Dolosigranulum pigrum, Ignavigranum ruoffiae, and Facklamia Species. J Clin Microbiol.38(6): 2037–2042.
Limoee M, Enayati AA, Ladonni H, Vatandoost H, Baseri H, Oshaghi MA (2006) Various mechanisms responsi- ble for permethrin metabolic resistance in seven field-collected strains of the German cockroach from Iran, Blattella germanica (L.) (Dictyoptera: Blatte- llidae). Pestic Biochem Physiol. 87:138–146.
Litonjua AA, Cary VJ, Burge HA, Weiss ST, Gold DR (2001) Exposure to cock- roach allergen in the home is associ- ated with incident doctor-diagnosed asthma and recurrent wheezing. J Allergy Clin Immunol. 107: 41–7.
Maleki-Ravasan N, Oshaghi MA, Hajikhani S, Saeidi Z, Akhavan AA, Gerami- Shoar M, Shirazi MH, Yakhchali B, Rassi Y, Afshar D (2013) Aerobic mi- crobial community of insectary pop- ulation of Phlebotomus papatasi. J Arthropod Borne Dis. 8(1): 69–81.
Maleki-Ravasan N, Oshaghi MA, Afshar D, Arandian MH, Hajikhani S, Akhavan AA, Yakhchali B, Shirazi MH, Jafari R, Aminian K, Fazeli-Varzaneh RA (2014) Aerobic Bacterial flora of bi- otic and abiotic compartments of a hyperendemic Zoonotic Cutaneous Leishmaniasis (ZCL) focus. Acta Trop, (In press).
Maslow JN, Mulligan ME, Arbeit RD (1993) Molecular epidemiology: application of contemporary techniques to the typing of microorganisms. Clin Infect Dis. 17: 153–164.
Mellmann A, Cloud JL, Andrees S, Black- wood K, Carroll KC, Kabani A, Roth A, Harmsen D (2003) Evaluation of RIDOM, MicroSeq, and GenBank services in the molecular identification of Nocardia species. Int J Med Microbiol. 293: 359–370.
Mignard S, Flandrois JP (2006) 16S rRNA sequencing in routine bacterial identi- fication: a 30-month experiment. J Microbiol Methods. 67: 574–581.
Mille P, Peters B (2004) Overview of the public health implications of cockroaches and their management. N S W Public Health Bull. 15(12): 208–211.
Mukhopadhyay J, Braig HR, Rowton ED, Ghosh K (2012) Naturally occurring culturable aerobic gut flora of adult Phlebotomus papatasi, vector of Leishmania major in the Old World. PLoS One. 7(5): e35748.
Nagy E, Urbán E, Sóki J, Terhes G, Nagy K (2006) The place of molecular genetic methods in the diagnostics of human pathogenic anaerobic bacteria. A mini- review. Acta Microbiol Immunol Hung.53(2): 183–194.
Nazarowec-White M, Farber JM (1999) Phe- notypic and genotypic typing of food and clinical isolates of Enterobacter sakazakii. J Med Microbiol. 48: 559–567.
Niyogi SK (2005) Shigellosis. J Microbiol.43(2): 133–143.
Pai HH, Chen WC, Peng CF (2005) Isolation of bacteria with antibiotic resistance from household cockroaches (Peri- planeta americana and Blattella ger- manica). Acta Trop. 93(3): 259–265.
Schauer C, Thompson CL, Brune A (2012) The bacterial community in the gut of the cockroach Shelfordella lateralis reflects the close evolutionary related- ness of cockroaches and termites. Appl Environ Microbiol. 78(8): 2758–2767.
Sibley CD, Peirano G, Church DL (2012) Molecular methods for pathogen and microbial community detection and characterization: current and potential application in diagnostic microbiology. Infect Genet Evol. 12(3): 505–521.
Sneath PHA (1984) Endospore forming gram-positive rods and cocci. In: Sneath PHA (Ed): Bergey’s Manual of Systematic Bacteriology. Vol. 2. Williams and Wilkins, Baltimore, pp.1104–1139.
Speers DJ (2006) Clinical applications of molecular biology for infectious dis- eases. Clin Biochem Rev. 27(1): 39–51.
Springer B, Stockman L, Teschner K, Roberts GD, Bottger EC (1995) Two- laboratory collaborative study on iden- tification of mycobacteria: molecular versus phenotypic methods. J Clin Microbiol. 34(2): 296–303.
Tachbele E, Erku W, Gebre-Michael T, Ashenafi M (2006) Cockroach-asso- ciated food borne bacterial pathogens from some hospitals and restaurants in Addis Ababa, Ethiopia: Distribution and antibiograms. J Rural Trop Public Health. 5: 34–41.
Vahabi A, Rafinejad J, Mohammadi P, Biglarian F (2007) Regional evaluation of bacterial contamination in hospital environment cockroaches. Iran J En- viron Health Sci Eng. 4: 57–60.
Vinokurov K, Taranushenko Y, Krishnan N, Sehnal F (2007) Proteinase, amylase, and proteinase-inhibitor activities in the gut of six cockroach species. J Insect Physiol. 53: 794–802.
Wang S, Jacobs-Lorena M (2013) Genetic approaches to interfere with malaria transmission by vector mosquitoes. Trends Biotechnol. 31(3): 185–193.
Watanabe K, Abe K, Sato M (2000) Biolog- ical control of an insect pest by gut- colonizing Enterobacter cloacae trans- formed with ice nucleation gene. J Appl Microbiol 88:90-97.
Weile J, Knabbe C (2009) Current appli- cations and future trends of molecular diagnostics in clinical bacteriolog. Anal Bioanal Chem. 394(3): 731–742.
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol. 173(2): 697–703.
Woo PC, Ng KH, Lau SK, Yip KT, Fung AM, Leung KW, Tam DM, Que TL, Yuen KY (2003) Usefulness of the MicroSeq (500) 16S ribosomal DNA based bacterial identification system for identification of clinically signif- icant bacterial isolates with ambiguous biochemical profiles. J Clin Microbiol.41: 1996–2001.
Woo PC, Lau SK, Teng JL, Tse H, Yuen KY (2008) Then and now: use of 16S rDNA gene sequencing for bacterial identification and discovery of novel bacteria in clinical microbiology labor- atories. Clin Microbiol Infect. 14(10):908–934.
Zarchi AA, Vatani H (2009) A survey on species and prevalence rate of bacterial agents isolated from cockroaches in three hospitals. Vector Borne Zoonotic Dis. 9(2): 197–200.
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