Aerobic Microbial Community of Insectary Population of Phlebotomus papatasi
-
Naseh Maleki-Ravasan
,
Mohammad Ali Oshaghi
,
Sara Hajikhani
,
Zahra Saeidi
,
Amir Ahmad Akhavan
,
Mohsen Gerami-Shoar
,
Mohammad Hasan Shirazi
,
Bagher Yakhchali
,
Yavar Rassi
,
Davoud Afshar
Abstract
Background: Microbes particularly bacteria presenting in the gut of haematophagous insects may have an important role in the epidemiology of human infectious disease.
Methods: The microbial flora of gut and surrounding environmental of a laboratory strain of Phlebotomus papatasi, the main vector of Zoonotic Cutaneous Leishmaniasis (ZCL) in the old world, was investigated. Biochemical reac- tions and 16s rDNA sequencing of the isolated bacteria against 24 sugars and amino acids were used for bacteria species identification. Common mycological media used for fungi identification as well.
Results: Most isolates belonged to the Enterobacteriaceae, a large, heterogeneous group of gram-negative rods whose natural habitat is the intestinal tract of humans and animals. Enterobacteriaceae groups included Edwardsiella, Enterobacter, Escherichia, Klebsiella, Kluyvera, Leminorella, Pantoea, Proteus, Providencia, Rahnella, Serratia, Shigella, Tatumella, and Yersinia and non Enterobacteriaceae groups included Bacillus, Staphylococcus and Pseu- domonas. The most prevalent isolates were Proteus mirabilis and P. vulgaris. These saprophytic and swarming mo- tile bacteria were isolated from all immature, pupae, and mature fed or unfed male or female sand flies as well as from larval and adult food sources. Five fungi species were also isolated from sand flies, their food sources and colo- nization materials where Candida sp. was common in all mentioned sources.
Conclusion: Midgut microbiota are increasingly seen as an important factor for modulating vector competence in insect vectors so their possible effects of the mirobiota on the biology of P. papatasi and their roles in the sandfly- Leishmania interaction are discussed.
Aksoy S, Weiss B, Attardo G (2008) Paratransgenesis applied for control of tsetse transmitted sleeping sickness. Adv Exp Med Biol. 627: 35–48.
Al-bayati NY, Al-Ubaidi AS, Al-Ubaidi IK (2011) Risks associated with cockroach Periplaneta americana as a transmitter of pathogen agents. Diyala J Med. 1:91–97.
Alexander B, Maroli M (2003) Control of phlebotomine sandflies. Med Vet En- tomol. 17(1): 1–18.
Bates PA (2008) Leishmania sandfly inter- action: progress and challenges. Curr Opin Microbiol. 11(4): 340–344.
Bates PA (2007) Transmission of Leishmania metacyclic promastigotes by phlebo- tomine sandflies. Int J Parasitol. 37 (10): 1097–1106.
Baumann P, Moran NA, Baumann L (2000) Bacteriocyte-associated endosymbionts of insects. In: Dworkin M (ed): The Pro- karyotes. Springer-Verlag, New York.
Beard CB, Doston EM, Pennington PM, Eichler S, Cordon-Rosales C, Durvasula RV (2001) Bacterial symbiosis and paratransgenic control of vector-borne Chagas disease. Int J Parasitol. 31:621–627.
Bolaños-Herrera R (1959) Frecuencia de Sal- monella y Shigella em moscas domésticas em la ciudade de San José. Rev Biol Trop. 7(2): 207–210.
Boulanger N, Lowenberger C, Volf P, Ursic R, Sigutova L, Sabatier L, Svobodova M, Beverley SM, Spath G, Brun R, Pesson B, Bulet P (2004) Characterization of a defensin from the sand fly Phlebo- tomus duboscqi induced by challenge with bacteria or the protozoan parasite Leishmania major. Infect Immun. 72:7140–7146.
Bourtzis K, Miller TA (2003) Insect Symbi- osis. CRC Press, Boca Raton, FL.Bucher GE (1963) Transmission of bacterial pathogens by the ovipositor of a hymenopterous parasite. J Insect Pathol.5: 277–283.
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.
Butler JF, Garcia-Maruniak A, Meek F, Maruniak JE (2010) Wild Florida house flies (Musca domestica) as car- riers of pathogenic bacteria. Fla En- tomol. 93(2): 218–223.
Cameron MM, Milligan PJ, Llanos-Cuentas A, Davies CR (1995) An association between phlebotomine sandflies and aphids in the Peruvian Andes. Med Vet Entomol. 9: 127–132.
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 to- ward finding suitable paratransgenesis candidates. Acta Trop. 121(2): 129–134.
Chavshin AR, Oshaghi MA, Vatandoost H, Yakhchali B., Raeisi A, Zarenejad F (2013) Escherichia coli expressing a green fluorescent protein (GFP) in Anopheles stephensi: a preliminary model for paratransgenesis. Symbiosis 60: 17–24.
Cirimotich CM, Dong Y, Clayton AM, Sandiford SL, Souza-Neto JA, Mulenga M, Dimopoulos G (2011) Natural mi- crobe-mediated refractoriness to Plas- modium infection in Anopheles gambiae. Science. 332: 855–858.
Dillon RJ, Dillon VM (2004) The gut bac- teria of insects: nonpathogenic inter- actions. Annu Rev Entomol. 49: 71–92.
Dillon RJ, Charnley K (2002) Mutualism between the desert locust Schistocerca gregaria and its gut microbiota. Res Microbiol.153(8): 503–509.
Dillon RJ, ElKordy E, Shehata M, Lane RP (1996) The prevalence of a microbiota in the digestive tract of Phlebotomus papatasi. Ann Trop Med Parasitol.90(6): 669–673.
Dong Y, Manfredini F, Dimopoulos G (2009) Implication of the Mosquito Midgut Microbiota in the Defense against Ma- laria Parasites. PLoS Pathog. 5(5): e1000423.
Erdmann GR (1987) Antibacterial action of myiasis-causing flies. Parasitol Today.3(7): 214–216.
Erdmann GR, Khalil SKW (1986) Isolation and identification of two antibacterial agents produced by a strain of Proteus mirabilis isolated from larvae of the screwworm (Cochliomya hominivorax) (Diptera: Calliphoridae). J Med En- tomol. 23(2): 208–211.
Feliciangeli MD (2004) Natural breeding places of phlebotomine sand flies. Med Vet Entomol. 18(1): 71–80.
Fleischmann W, Grassberger M, Sherman R (2004) Maggot Therapy: A Handbook of Maggot-Assisted Wound Healing. Stuttgart Georg Thieme.
Foster TJ (2005) Immune evasion by staph- ylococci. Nat Rev Microbiol. 3(12):948–958.
Galac MR. Lazzaro BP (2011) Comparative pathology of bacteria in the genus Providencia to a natural host, Dro- sophila melanogaster. Microbes In- fect. 13(7): 673–683.
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 En- tomol. 37: 597–601.
Greenberg B (1959) Persistence of bacteria in the developmental stages of the house fly .II. Quantitative study of the host- contaminant relationship in flies breeding under natural conditions. Am J Trop Med Hyg. 8: 412–416.
Greenberg B (1968) Model for destruction of bacteria in the midgut of blow fly maggots. J Med Entomol. 5(1): 31–38. Greenberg B, Kowalski JA, Klowden MJ (1970) Factors affecting the transmission of Salmonella by flies. Natural re- sistance to colonization and bacterial in- terference. Infect Immun. 2(6): 800–809.
Guentzel MN (1991) Escherichia, Klebsiella, Enterobacter, Serratia, Citrobacter and Proteus. In: Baron S (Ed): Medical Mi- crobiology. New York, Churchill Living- stone, pp. 377–387.
Guernaoui S, Garcia D, Gazanion E, Ouhdouch Y, Boumezzough A, Pesson B, Fontenille D, Sereno D (2011) Bac- terial flora as indicated by PCR-tem- perature gradient gel electrophoresis (TGGE) of 16S rDNA gene fragments from isolated guts of phlebotomine sand flies (Diptera: Psychodidae). J Vector Ecol. 36: 144–147.
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 platform for potential paratransgenic manipulation of sand flies. Am J Trop Med Hyg. 79(6): 881–886.
Hinnebusch BJ (2005) The Evolution of Flea- borne Transmission in Yersinia pestis. Curr Issues Mol Biol. 7(2): 197–212.
Hollis DG, Hickman FW, Fanning GR, Farmer JJ, Weaver RE, Brenner DJ (1981) Tatumella ptyseos gen. nov., sp. nov., a member of the family Enterobacteriaceae found in clinical specimens. J Clin Microbiol. 14: 79e88.
Kamhawi S (2006) Phlebotomine sand flies and Leishmania parasites: friends or foes? Trends Parasitol. 22(9): 439–445.
Khampang P, Luxananil P, Tanapongpipat S,Chungjatupornchai W, Panyim S (2001) Recombinant Enterobacter amnigenus highly toxic to Anopheles dirus mos- quito larvae. Curr Microbiol. 43(6):448–451.
Killick-Kendrick R, Killick-Kendrick M (1987) Honeydew of aphids as a source of sugar for Phlebotomus ariasi. Med Vet Entomol. 1(3): 297–302.
Koch H, Schmid-Hempel P (2011) Socially transmitted gut microbiota protect bum- ble bees against an intestinal parasite. PNAS. 108(48): 19288–19292.
Kuzina LV, Miller ED, Ge BX, Miller TA (2002) Transformation of Enterobacter gergoviae isolated from pink bollworm (Lepidoptera: Gelechiidae) gut with Ba- cillus thuringiensis toxin. Curr Mic- robiol. 44: 1–4.
Lacey LA, Unruh TR, Simkins H, Thomsen- Archer K (2007) Gut bacteria associ- ated with the Pacific Coast wireworm, Limonius canus, inferred from16S rDNA sequences and the triplications forcontrol. Phytoparasit 35: 479–489.
Ma Q, Fonseca A, Liu W, Fields AT, Pimsler ML, Spindola AF, Tarone AM, Crippen TL, Tomberlin JK, Wood TK (2012) Proteus mirabilis interkingdom swarm- ing signals attract blow flies. ISME J.6(7): 1356–66.
Marín-Cevada V, Caballero-Mellado J, Bustillos-Cristales R, Muñoz-Rojas J, Mascarúa-Esparza MA, Castañeda-Lucio M, López-Reyes L, Martínez-Aguilar L, Fuentes-Ramírez LE (2010) Tatumella ptyseos, an unrevealed causative agent of pink disease in pineapple. J Phy- topathol. 158(2): 93–99.
McCoy AJ, Liu H, Falla TJ, Gunn JS (2001) Identification of Proteus mirabilis mu- tants with increased sensitivity to an- timicrobial peptides. Antimicrob Agents Chemother. 45(7): 2030–2037.
Meister S, Kanzok SM, Zheng XL, Luna C, Li TR, Hoa NT, Clayton JR, White KP, Kafatos FC, Christophides GK, Zheng L (2005) Immune signaling path- ways regulating bacterial and malaria parasite infection of the mosquito Anopheles gambiae. Proc Natl Acad Sci USA. 102: 11420–11425.
Modi GB, Tesh RB (1983) A simple tech- nique for mass rearing Lutzomyia longipalpis and Phlebotomus papatasi (Diptera: Psychodidae) in the labora- tory. J Med Entomol. 20: 568–569.
Mohd Masri S, Nazni WA, Lee HL, Tengku Rogayah TAR, Subramaniam S (2005) Sterilization of Lucilia cuprina (Wiedemann) maggots used in therapy of intractable wounds. Trop Biomed.22(2): 185–189.
Mukhopadhyay J, Braig HR, Rowton ED, Ghosh K (2012) Naturally occurring culturable aerobic gut flora of adult Phlebotomus papatasi, Vector of Leish- mania major in the old world. PLoS ONE. 7(5): e35748.
Muniaraj M, Dinesh D, Sinha P, Das P, Bhattacharya S (2008) Dual culture method to determine the relationship of gut bacteria of sand fly (Phlebotomus argentipes) with promastigotes of Leish- mania donovani. J Commun Dis. 40 (2): 133–138.
Muratoğlu H, Sezen K, Demirbağ Z (2011) Determination and pathogenicity of the bacterial flora associated with the spruce bark beetle, Ips typographus (L.) (Cole- optera: Curculionidae: Scolytinae) Turk J Biol. 35: 9–20.
Nguyen NH, Suh SO, Blackwell M (2007) "Five novel Candida species in insect- associated yeast clades isolated from Neuroptera and other insects". My- cologia. 99(6): 842–858.
O’Neill SL, Hoffmann AA, Werren JH (1997) Influential Passengers. Oxford Univer- sity Press, Oxford.
Oshaghi MA, Maleki Ravasan N, Javadian E, Rassi Y, Sadraei J, Enayati AA, Vatandoost H, Zare Z, Emami SN (2009) Ap- plication of predictive degree day mod- el for field development of sand fly vec- tors of visceral leishmaniasis in north- west of Iran. J Vector Borne Dis. 46:1–8.
Panizzi AR, Parra JRP (1991) Ecologia nut- ricional de insetos e suas implicações no manejo de pragas. São Paulo, Manole/ Brasilia: CNPq.
Pontes MH, Dale C (2011) Lambda Red- mediated genetic modification of the insect endosymbiont Sodalis glossini- dius. Appl Environ Microbiol. 77:1918–1920.
Pumpuni CB, Demaio J, Kent M, Davis JR, Beier JC (1996) Bacterial population dynamics in three Anopheline species: the impact on Plasmodium sporogonic development. Am J Trop Med Hyg. 54 (2): 214–218.
Radjame K, Srinivasan R, Dhanda V (1997) Oviposition response of phlebotomid sandfly Phlebotomus papatasi to soil bacteria isolated from natural breeding habitats. Indian J Exp Biol. 35: 59–61.
Rajendran P, Modi GB (1982) Bacterial flora of Sandfly gut (Diptera: Psychodidae) Indian J Public Health. 26(1): 49–52.
Rani A, Sharma A, Rajagopal R, Adak T, Bhatnagar RK (2009) Bacterial diver- sity analysis of larvae and adult midgut microflora using culture-dependent and culture-independent methods in lab- reared and field-collected Anopheles stephensi-an Asian malarial vector. BMC Microbiol. 9: 96.
Rio RV, Hu Y, Aksoy S (2004) Strategies of the home-team: symbioses exploited for vector-borne disease control. Trends Microbiol. 12(7): 325–336.
Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C (2011) Hemocyte dif- ferentiation mediates innate immune memory in Anopheles gambiae mos- quitoes. Science. 329(5997): 1353–1355.
Rozalski A, Sidorczyk Z, Kotelko K (1997) Potential virulence factors of Proteus bacilli. Microbiol molec Biol Rev. 61 (1): 65–89.
Salehzadeh A, Tavacol P, Mahjub H (2007) Bacterial, fungal and parasitic contam- ination of cockroaches in public hospi- tals of Hamadan, Iran. J Vect Borne Dis.44: 105–110.
Sanchez-Gonzalez M, Blanco-Gamez A, Es- calante A, Valladares AG, Olvera C, Roberto P (2011) Isolation and charac- terization of new facultative alkaphilic Bacillus flexus strains from maize pro- cessing waste water (nejayote) Lett Appl Microbiol. 52(4): 413–419.
Santander J, Xin W, Yang Z, Curtiss R (2010) The Aspartate-Semialdehyde Dehydrogenase of Edwardsiella ictaluri and its use as balanced-lethal system in fish vaccinology. PloS ONE. 5(12): e15944.
Schlein Y, Polacheck I, Yuva B (1985) My- coses, bacterial infections and anti- bacterial activity in sandflies (Psy- chodidae) and their possible role in the transmission of leishmaniasis. Parasitol.90: 57–66.
Schlein Y, Yuval B (1987) Leishmaniasis in the Jordan Valley. IV. Attraction of Phlebotomus papatasi (Diptera: Psy- chodidae) to plants in the field. J Med Entomol. 24(1): 87–90.
Sevim E, Celebi O, Sevim A (2012) Deter- mination of the bacterial flora as a mi- crobial control agent of Toxoptera aurantii (Homoptera: Aphididae). Bio- logia. 67(2): 397–404.
Silby MW, Winstanley C, Godfrey SAC, Levy SB, Jackson RW (2011) Pseudomonas genomes: diverse and adaptable. FEMS Microbiol Rev. 35(4): 652–680.
Singh RP, Mantri VA, Reddy CRK, Jha B (2011) Isolation of seaweed associated bacteria and their morphogenesis-in- ducing capability in axenic cultures of the green alga Ulva fasciata. Aquat Biol. 12: 13–21.
Suh SO, Nguyen NH, Blackwell M (2008) Yeasts isolated from plant-associated beetles and other insects: seven novel Candida species near Candida albicans". FEMS. Yeast Res. 8(1): 88–102.
Tay BY, Lokesh BE, Lee CY, Sudesh K (2010) Polyhydroxyalkanoate (PHA) accumulating bacteria from the gut of higher termite Macrotermes carbonarius (Blattodea: Termitidae). World J Mic- robiol Biotechnol. 26(6): 1015–1024.
Thaochan N, Drew RAI, Hughes JM, Vijaysegaran S, Chinajariyawong A (2010) Alimentary tract bacteria iso- lated and identified with API-20E and molecular cloning techniques from Aus- tralian tropical fruit flies, Bactrocera cacuminata and B. tryoni. J Insect Sci.10:131.
Toth-Prestia C, Hirshfield IN (1988) Iso-lation of plasmid-harboring Serratia plymuthica from facultative gut microflora of the tobacco hornworm, Manduca sexta. Appl Environ Microbiol. 54(7): 1855–1857.
Vasanthakumar A, Delalibera I, Handelsman J, Klepzig KD, Schloss PD, Raffa KF (2006) Characterization of gut-associ- ated microorganisms in larvae and adults of the southern pine beetle, Dendroctonus frontalis Zimmerman. En- viron Entomol. 35: 1710–1717.
Volf P, Kiewegova A, Nemec A (2002) Bac- terial colonisation in the gut of Phlebo- tomus duboscqi (Diptera Psychodidae): transtadial passage and the role of fe- male diet. Folia Parasitol. 49: 73–77.
Wang S, Ghosh AK, Bongio N, Stebbings KA, Lampe DJ, Jacobs-Lorena M (2012) Fighting malaria with engineered sym- biotic bacteria from vector mosquitoes. Proc Natl Acad Sci USA. 109(31):12734–12739.
Warburg A (1991) Entomopathogens of phlebotomine sand flies: laboratory experiments and natural infections. J Invertebr Pathol. 58(2): 189–202.
Wasserberg G, Rowton ED (2011) Sub-ad- ditive effect of conspecific eggs and frass on oviposition rate of Lutzomyia longipalpis and Phlebotomus papatasi. J Vector Ecol. 36(1): S138–S143.
Weisberg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplfication for ylogenetic study. J Bacteriol. 173(2): 697–703.
Weiss B, Aksoy S (2011) Microbiome influ- ences on insect host vector competence. Trends Parasitol. 27: 514–522.
Wermelinger ED, Zanuncio JC (2001) Dev- elopment of Lutzomyia intermedia and Lutzomyia longipalpis (Diptera: Psy- chodidae: Phlebotominae) larvae in dif- ferent diets. Braz J Biol. 61(3): 405–408.
Xi Z, Ramirez JL, Dimopoulos G (2008) The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog.4(7): e1000098.
Young CJ, Turner DP, Killick-Kendrick R, Rioux JA, Leaney AJ (1980) Fructose in wild-caught Phlebotomus ariasi and the possible relevance of sugars taken by sand flies to the transmission of leishmaniasis. Trans R Soc Trop Med Hyg. 74(3): 363–366.
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