期刊论文详细信息
Particle and Fibre Toxicology
Rhodnius prolixus interaction with Trypanosoma rangeli: modulation of the immune system and microbiota population
Patrícia Azambuja2  Eloi S Garcia2  Daniele P Castro2  Fabio F da Mota2  Marcia Gumiel1  Marcela B Figueiredo1  Jayme M Santangelo3  Peter J Waniek1  Débora P Mattos1  Cecilia S Vieira1 
[1] Laboratório de Bioquímica e Fisiologia de Insetos, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz (IOC/FIOCRUZ), Rio de Janeiro, RJ, Brazil;Departamento de Entomologia Molecular, Instituto Nacional de Entomologia Molecular (INCT-EM), Rio de Janeiro, RJ, Brazil;Departamento de Ciências Ambientais, Instituto de Florestas, Universidade Federal Rural do Rio de Janeiro (UFRRJ), Seropédica, RJ, Brazil
关键词: Antimicrobial peptide;    Prophenoloxidase;    Immune system;    Trypanosoma rangeli;    Rhodnius prolixus;   
Others  :  1146801
DOI  :  10.1186/s13071-015-0736-2
 received in 2014-11-10, accepted in 2015-02-13,  发布年份 2015
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【 摘 要 】

Background

Trypanosoma rangeli is a protozoan that infects a variety of mammalian hosts, including humans. Its main insect vector is Rhodnius prolixus and is found in several Latin American countries. The R. prolixus vector competence depends on the T. rangeli strain and the molecular interactions, as well as the insect’s immune responses in the gut and haemocoel. This work focuses on the modulation of the humoral immune responses of the midgut of R. prolixus infected with T. rangeli Macias strain, considering the influence of the parasite on the intestinal microbiota.

Methods

The population density of T. rangeli Macias strain was analysed in different R. prolixus midgut compartments in long and short-term experiments. Cultivable and non-cultivable midgut bacteria were investigated by colony forming unit (CFU) assays and by 454 pyrosequencing of the 16S rRNA gene, respectively. The modulation of R. prolixus immune responses was studied by analysis of the antimicrobial activity in vitro against different bacteria using turbidimetric tests, the abundance of mRNAs encoding antimicrobial peptides (AMPs) defensin (DefA, DefB, DefC), prolixicin (Prol) and lysozymes (LysA, LysB) by RT-PCR and analysis of the phenoloxidase (PO) activity.

Results

Our results showed that T. rangeli successfully colonized R. prolixus midgut altering the microbiota population and the immune responses as follows: 1 - reduced cultivable midgut bacteria; 2 - decreased the number of sequences of the Enterococcaceae but increased those of the Burkholderiaceae family; the families Nocardiaceae, Enterobacteriaceae and Mycobacteriaceae encountered in control and infected insects remained the same; 3 - enhanced midgut antibacterial activities against Serratia marcescens and Staphylococcus aureus; 4 - down-regulated LysB and Prol mRNA levels; altered DefB, DefC and LysA depending on the infection (short and long-term); 5 - decreased POactivity.

Conclusion

Our findings suggest that T. rangeli Macias strain modulates R. prolixus immune system and modifies the natural microbiota composition.

【 授权许可】

   
2015 Vieira et al.; licensee BioMed Central.

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【 参考文献 】
  • [1]Watkins R. Histology of Rhodnius prolixus infected with Trypanosoma rangeli. J Invertebr Pathol. 1971; 17:59-66.
  • [2]Hoare CA. The trypanosomes of mammals: a zoological monograph. Blackwell Scientific Publications, Oxford; 1972.
  • [3]Tobie EJ. Observations on development of Trypanosoma rangeli in hemocoel of Rhodnius prolixus. J Invertebr Pathol. 1970; 15:118-25.
  • [4]Guhl F, Vallejo GA. Trypanosoma (Herpetosoma) rangeli Tejera, 1920 - An updated review. Mem Inst Oswaldo Cruz. 2003; 98:435-42.
  • [5]Hecker H, Schwarzenbach M, Rudin W. Development and interactions of Trypanosoma rangeli in and with the reduviid bug Rhodnius prolixus. Parasitol Res. 1990; 76:311-8.
  • [6]Garcia ES, Mello CB, Azambuja P, Ribeiro JMC. Rhodnius prolixus - salivary antihemostatic components decrease with Trypanosoma rangeli infection. Exp Parasitol. 1994; 78:287-93.
  • [7]Azambuja P, Garcia ES. Trypanosoma rangeli interactions within the vector Rhodnius prolixus: a mini review. Mem Inst Oswaldo Cruz. 2005; 100:567-72.
  • [8]Garcia ES, Castro DP, Figueiredo MB, Azambuja P. Parasite mediated interactions within the insect vector: Trypanosoma rangeli strategies. Parasit Vectors. 2012; 5:105. BioMed Central Full Text
  • [9]Garcia ES, Ratcliffe NA, Whitten MM, Gonzalez MS, Azambuja P. Exploring the role of insect host factors in the dynamics of Trypanosoma cruzi-Rhodnius prolixus interactions. J Insect Physiol. 2007; 53:11-21.
  • [10]Garcia ES, Castro DP, Figueiredo MB, Genta FA, Azambuja P. Trypanosoma rangeli: a new perspective for studying the modulation of immune reactions of Rhodnius prolixus. Parasit Vectors. 2009; 2:33. BioMed Central Full Text
  • [11]Figueiredo MB, Genta FA, Garcia ES, Azambuja P. Lipid mediators and vector infection: Trypanosoma rangeli inhibits Rhodnius prolixus hemocyte phagocytosis by modulation of phospholipase A2 and PAF-acetylhydrolase activities. J Insect Physiol. 2008; 54:1528-37.
  • [12]Azambuja P, Feder D, Garcia ES. Isolation of Serratia marcescens in the midgut of Rhodnius prolixus: impact on the establishment of the parasite Trypanosoma cruzi in the vector. Exp Parasitol. 2004; 107:89-96.
  • [13]Azambuja P, Garcia ES, Ratcliffe NA. Gut microbiota and parasite transmission by insect vectors. Trends Parasitol. 2005; 21:568-72.
  • [14]Azambuja PG, Guimarães JA, Garcia ES. Haemolytic factor from the crop of Rhodnius prolixus: evidence and partial characterization. J Insect Physiol. 1983; 29:5.
  • [15]Pulido XC, Perez G, Vallejo GA. Preliminary characterization of a Rhodnius prolixus hemolymph trypanolytic protein, this being a determinant of Trypanosoma rangeli KP1(+) and KP1(−) subpopulations vectorial ability. Mem Inst Oswaldo Cruz. 2008; 103:172-9.
  • [16]Mello CB, Nigam Y, Garcia ES, Azambuja P, Newton RP, Ratcliffe NA. Studies on a haemolymph lectin isolated from Rhodnius prolixus and its interaction with Trypanosoma rangeli. Exp Parasitol. 1999; 91:289-96.
  • [17]Castro DP, Moraes C, Gonzalez M, Ratcliffe N, Azambuja P, Garcia E. Trypanosoma cruzi immune response modulation decreases microbiota in Rhodnius prolixus gut and is crucial for parasite survival and development. PLoS One. 2012; 7:e36591.
  • [18]Waniek PJ, Castro HC, Sathler PC, Miceli L, Jansen AM, Araujo CAC. Two novel defensin-encoding genes of the Chagas disease vector Triatoma brasiliensis (Reduviidae, Triatominae): gene expression and peptide-structure modeling. J Insect Physiol. 2009; 55:840-8.
  • [19]Ursic-Bedoya R, Buchhop J, Joy JB, Durvasula R, Lowenberger C. Prolixicin: a novel antimicrobial peptide isolated from Rhodnius prolixus with differential activity against bacteria and Trypanosoma cruzi. Insect Mol Biol. 2011; 20:775-86.
  • [20]Whitten M, Sun F, Tew I, Schaub G, Soukou C, Nappi A et al.. Differential modulation of Rhodnius prolixus nitric oxide activities following challenge with Trypanosoma rangeli, T. cruzi and bacterial cell wall components. Insect Biochem Mol Biol. 2007; 37:440-52.
  • [21]Garcia ES, Machado EM, Azambuja P. Inhibition of hemocyte microaggregation reactions in Rhodnius prolixus larvae orally infected with Trypanosoma rangeli. Exp Parasitol. 2004; 107:31-8.
  • [22]Garcia ES, Machado EM, Azambuja P. Effects of eicosanoid biosynthesis inhibitors on the prophenoloxidase-activating system and microaggregation reactions in the hemolymph of Rhodnius prolixus infected with Trypanosoma rangeli. J Insect Physiol. 2004; 50:157-65.
  • [23]Sociedade Brasileira de Ciências de Animais em Laboratório. COBEA. http://www.cobea.org.br. (2014). Accessed 10 Oct 2014.
  • [24]Schottelius J. Neuraminidase fluorescence test for the differentiation of Trypanosoma cruzi and Trypanosoma rangeli. Trop Med Parasitol. 1987; 38:323-7.
  • [25]Grisard EC, Steindel M, Guarneri AA, Eger-Mangrich I, Campbell DA, Romanha AJ. Characterization of Trypanosoma rangeli strains isolated in Central and South America: an overview. Mem Inst Oswaldo Cruz. 1999; 94:203-9.
  • [26]Vallejo GA, Guhl F, Carranza JC, Lozano LE, Sanchez JL, Jaramillo JC et al.. kDNA markers define two major Trypanosoma rangeli lineages in Latin-America. Acta Trop. 2002; 81:77-82.
  • [27]Azambuja P, Garcia ES. Care and maintenance of triatomine colonies. In: Molecular biology of insect disease vectors: a methods manual. Crampton JM, Beard CB, Louis C, editors. Chapman and Hall, London; 1997: p.56-64.
  • [28]Bexfield A, Nigam Y, Thomas S, Ratcliffe NA. Detection and partial characterisation of two antibacterial factors from the excretions/secretions of the medicinal maggot Lucilia sericata and their activity against methicillin resistant Staphylococcus aureus (MRSA). Microbes Infect. 2004; 6:1297-304.
  • [29]Ferrand J, Patron K, Legrand-Frossi C, Frippiat JP, Merlin C, Alauzet C et al.. Comparison of seven methods for extraction of bacterial DNA from fecal and cecal samples of mice. J Microbiol Methods. 2014; 105:180-5.
  • [30]Andersson AF, Lindberg M, Jakobsson H, Backhed F, Nyren P, Engstrand L. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS One. 2008; 3:e2836.
  • [31]National Institute of Health Common Fund Human Microbiome Project (HMP) http://www.hmpdacc.org. (2014). Accessed 15 Sept 14.
  • [32]Nawrocki EP, Eddy SR. Query-dependent banding (QDB) for faster RNA similarity searches. PLoS Comput Biol. 2007; 3:e56.
  • [33]Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011; 27:2194-200.
  • [34]Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007; 73:5261-7.
  • [35]Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ et al.. The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 2009; 37:D141-5.
  • [36]Vieira CS, Waniek PJ, Mattos DP, Castro DP, Mello CB, Ratcliffe NA et al.. Humoral responses in Rhodnius prolixus: bacterial feeding induces differential patterns of antibacterial activity and enhances mRNA levels of antimicrobial peptides in the midgut. Parasit Vectors. 2014; 7:232. BioMed Central Full Text
  • [37]Lopez L, Morales G, Ursic R, Wolff M, Lowenberger C. Isolation and characterization of a novel insect defensin from Rhodnius prolixus, a vector of Chagas disease. Insect Biochem Mol Biol. 2003; 33:439-47.
  • [38]Ursic-Bedoya RJ, Nazzari H, Cooper D, Triana O, Wolff M, Lowenberger C. Identification and characterization of two novel lysozymes from Rhodnius prolixus, a vector of Chagas disease. J Insect Physiol. 2008; 54:593-603.
  • [39]Genta FA, Souza RS, Garcia ES, Azambuja P. Phenol oxidases from Rhodnius prolixus: temporal and tissue expression pattern and regulation by ecdysone. J Insect Physiol. 2010; 56:1253-9.
  • [40]Machado PE, Eger-Mangrich I, Rosa G, Koerich LB, Grisard EC, Steindel M. Differential susceptibility of triatomines of the genus Rhodnius to Trypanosoma rangeli strains from different geographical origins. Int J Parasitol. 2001; 31:632-4.
  • [41]Urrea DA, Carranza JC, Cuba CA, Gurgel-Goncalves R, Guhl F, Schofield CJ et al.. Molecular characterisation of Trypanosoma rangeli strains isolated from Rhodnius ecuadoriensis in Peru, R. colombiensis in Colombia and R. pallescens in Panama, supports a co-evolutionary association between parasites and vectors. Infect Genet Evol. 2005; 5:123-9.
  • [42]Whitten MM, Mello CB, Gomes SA, Nigam Y, Azambuja P, Garcia ES et al.. Role of superoxide and reactive nitrogen intermediates in Rhodnius prolixus (Reduviidae)/Trypanosoma rangeli interactions. Exp Parasitol. 2001; 98:44-57.
  • [43]Vallejo GA, Guhl F, Carranza JC, Triana O, Perez G, Ortiz PA et al.. Trypanosoma rangeli parasite-vector-vertebrate interactions and their relationship to the systematics and epidemiology of American trypanosomiasis. Biomedica. 2007; 27 Suppl 1:110-8.
  • [44]Vallejo GA, Guhl F, Schaub GA. Triatominae-Trypanosoma cruzi/T. rangeli. Vector-parasite interactions. Acta Trop. 2009; 110:137-47.
  • [45]Tchioffo MT, Boissiere A, Churcher TS, Abate L, Gimonneau G, Nsango SE et al.. Modulation of malaria infection in Anopheles gambiae mosquitoes exposed to natural midgut bacteria. PLoS One. 2013; 8:e81663.
  • [46]Weiss BL, Wang J, Maltz MA, Wu Y, Aksoy S. Trypanosome infection establishment in the tsetse fly gut is influenced by microbiome regulated host immune barriers. PLoS Pathog. 2013; 9:e1003318.
  • [47]Clayton AM, Dong Y, Dimopoulos G. The Anopheles innate immune system in the defense against malaria infection. J Innate Immun. 2014; 6:169-81.
  • [48]Sant'Anna MR, Diaz-Albiter H, Aguiar-Martins K, Al Salem WS, Cavalcante RR, Dillon VM et al.. Colonisation resistance in the sand fly gut: Leishmania protects Lutzomyia longipalpis from bacterial infection. Parasit Vectors. 2014; 7:329. BioMed Central Full Text
  • [49]Kollien AH, Schaub GA. The development of Trypanosoma cruzi in triatominae. Parasitol Today. 2000; 16:381-7.
  • [50]Carvalho-Moreira CJ, Spata MC, Coura JR, Garcia ES, Azambuja P, Gonzalez MS et al.. In vivo and in vitro metacyclogenesis tests of two strains of Trypanosoma cruzi in the triatomine vectors Triatoma pseudomaculata and Rhodnius neglectus: short/long-term and comparative study. Exp Parasitol. 2003; 103:102-11.
  • [51]Cortez MR, Provencano A, Silva CE, Mello CB, Zimmermann LT, Schaub GA et al.. Trypanosoma cruzi: effects of azadirachtin and ecdysone on the dynamic development in Rhodnius prolixus larvae. Exp Parasitol. 2012; 131:363-71.
  • [52]Araujo CAC, Waniek PJ, Jansen AM. TcI/TcII co-infection can enhance Trypanosoma cruzi growth in Rhodnius prolixus. Parasit Vectors. 2014; 7:94. BioMed Central Full Text
  • [53]Terra WR. Evolution of digestive system of insects – review. Annu Rev Entomol. 1990; 35:181-200.
  • [54]Kollien AH, Gonçalves TC, De Azambuja P, Garcia ES, Schaub GA. The effect of azadirachtin on fresh isolates of Trypanosoma cruzi in different species of triatomines. Parasitol Res. 1998; 84:286-90.
  • [55]Garcia ES, Genta FA, de Azambuja P, Schaub GA. Interactions between intestinal compounds of triatomines and Trypanosoma cruzi. Trends Parasitol. 2010; 26:499-505.
  • [56]Waniek PJ, Pacheco Costa JE, Jansen AM, Costa J, Araujo CAC. Cathepsin L of Triatoma brasiliensis (Reduviidae, Triatominae): sequence characterization, expression pattern and zymography. J Insect Physiol. 2012; 58:178-87.
  • [57]Lee WJ. Bacterial-modulated signaling pathways in gut homeostasis. Sci Signal. 2008; 1:pe24.
  • [58]Ha EM, Lee KA, Seo YY, Kim SH, Lim JH, Oh BH et al.. Coordination of multiple dual oxidase regulatory pathways in responses to commensal and infectious microbes in drosophila gut. Nat Immunol. 2009; 10:949-57.
  • [59]Geiger A, Fardeau ML, Njiokou F, Ollivier B. Glossina spp. gut bacterial flora and their putative role in fly-hosted trypanosome development. Front Cell Infect Microbiol. 2013; 3:34.
  • [60]Gendrin M, Christophides G. The Anopheles mosquito microbiota and their impact on pathogen transmission. Anopheles mosquitoes - New insights into malaria vectors. Manguin S, editor. InTech, Croatia; 2013. doi:10. 5772/55107
  • [61]Wigglesworth VB. ymbiotic bacteria in a blood-sucking insect, Rhodnius prolixus Stal (Hemiptera, Triatomidae). Parasitology. 1936; 28:284-9.
  • [62]da Mota FF, Marinho LP, Moreira CJ, Lima MM, Mello CB, Garcia ES et al.. Cultivation-independent methods reveal differences among bacterial gut microbiota in triatomine vectors of Chagas disease. PLoS Negl Trop Dis. 2012; 6:e1631.
  • [63]Eichler S, Schaub GA. Development of symbionts in triatomine bugs and the effects of infections with trypanosomatids. Exp Parasitol. 2002; 100:17-27.
  • [64]Castro DP, Moraes CS, Garcia ES, Azambuja P. Inhibitory effects of d-mannose on trypanosomatid lysis induced by Serratia marcescens. Exp Parasitol. 2007; 115:200-4.
  • [65]Castro DP, Seabra SH, Garcia ES, de Souza W, Azambuja P. Trypanosoma cruzi: ultrastructural studies of adhesion, lysis and biofilm formation by Serratia marcescens. Exp Parasitol. 2007; 117:201-7.
  • [66]Thomson NR, Crow MA, McGowan SJ, Cox A, Salmond GP. Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol Microbiol. 2000; 36:539-56.
  • [67]Dillon RJ, Dillon VM. The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol. 2004; 49:71-92.
  • [68]Leulier F, Royet J. Maintaining immune homeostasis in fly gut. Nat Immunol. 2009; 10:936-8.
  • [69]Schaub GA. Interactions of Trypanosomatids and Triatomines. Adv Insect Phys. 2009; 37:177-242.
  • [70]Nehme NT, Liegeois S, Kele B, Giammarinaro P, Pradel E, Hoffmann JA et al.. A model of bacterial intestinal infections in Drosophila melanogaster. PLoS Pathog. 2007; 3:e173.
  • [71]Ryu JH, Kim SH, Lee HY, Bai JY, Nam YD, Bae JW et al.. Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science. 2008; 319:777-82.
  • [72]Marmaras VJ, Lampropoulou M. Regulators and signalling in insect haemocyte immunity. Cell Signal. 2009; 21:186-95.
  • [73]Zasloff M. Antimicrobial peptides of multicellular organisms. Nature. 2002; 415:389-95.
  • [74]Bulet P, Stocklin R. Insect antimicrobial peptides: structures, properties and gene regulation. Protein PepT Lett. 2005; 12:3-11.
  • [75]Ferrandon D, Imler JL, Hetru C, Hoffmann JA. The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat Rev Immunol. 2007; 7:862-74.
  • [76]Bulet P, Cociancich S, Reuland M, Sauber F, Bischoff R, Hegy G et al.. A novel insect defensin mediates the inducible antibacterial activity in larvae of the dragonfly Aeschna cyanea (Paleoptera, Odonata). Eur J Biochem. 1992; 209:977-84.
  • [77]Lamberty M, Ades S, Uttenweiler-Joseph S, Brookhart G, Bushey D, Hoffmann JA et al.. Insect immunity. Isolation from the lepidopteran Heliothis virescens of a novel insect defensin with potent antifungal activity. J Biol Chem. 1999; 274:9320-6.
  • [78]Shahabuddin M, Fields I, Bulet P, Hoffmann JA, Miller LH. Plasmodium gallinaceum: differential killing of some mosquito stages of the parasite by insect defensin. Exp Parasitol. 1998; 89:103-12.
  • [79]Vizioli J, Richman AM, Uttenweiler-Joseph S, Blass C, Bulet P. The defensin peptide of the malaria vector mosquito Anopheles gambiae: antimicrobial activities and expression in adult mosquitoes. Insect Biochem Mol Biol. 2001; 31:241-8.
  • [80]McGwire BS, Olson CL, Tack BF, Engman DM. Killing of African trypanosomes by antimicrobial peptides. J Infect Dis. 2003; 188:146-52.
  • [81]Kleschenko YE, Karpenko LP, Villalta F. Effects of human defensin-α1 on Trypanosoma cruzi trypomastigotes in vitro. Bull Exp Biol Med. 2010; 149:731-3.
  • [82]Waniek PJ, Jansen AM, Araujo CAC. Trypanosoma cruzi infection modulates the expression of Triatoma brasiliensisdef1 in the midgut. Vector Borne Zoonotic Dis. 2011; 11:845-7.
  • [83]Gomes SA, Feder D, Thomas NE, Garcia ES, Azambuja P. Rhodnius prolixus infected with Trypanosoma rangeli: In vivo and in vitro experiments. J Invertebr Pathol. 1999; 73:289-93.
  • [84]Gomes SA, Feder D, Garcia ES, Azambuja P. Suppression of the prophenoloxidase system in Rhodnius prolixus orally infected with Trypanosoma rangeli. J Insect Physiol. 2003; 49:829-37.
  • [85]Machado EM, Azambuja P, Garcia ES. WEB 2086, a platelet-activating factor antagonist, inhibits prophenoloxidase-activating system and hemocyte microaggregation reactions induced by Trypanosoma rangeli infection in Rhodnius prolixus hemolymph. J Insect Physiol. 2006; 52:685-92.
  • [86]Gregorio EA, Ratcliffe NA. The prophenoloxidase system and in vitro interaction of Trypanosoma rangeli with Rhodnius prolixus and Triatoma infestans haemolymph. Parasite Immunol. 1991; 13:551-64.
  • [87]Ascenzi P, Gradoni L. Nitric oxide limits parasite development in vectors and in invertebrate intermediate hosts. IUBMB Life. 2002; 53:121-3.
  • [88]Rivero A. Nitric oxide: an antiparasitic molecule of invertebrates. Trends Parasitol. 2006; 22:219-25.
  • [89]Cosentino-Gomes D, Rocco-Machado N, Meyer-Fernandes JR. Rhodnius prolixus: Modulation of antioxidant defenses by Trypanosoma rangeli. Exp Parasitol. 2014; 145:118-24.
  • [90]Cirimotich CM, Dong Y, Clayton AM, Sandiford SL, Souza-Neto JA, Mulenga M et al.. Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science. 2011; 332:855-8.
  • [91]Ramirez JL, Souza-Neto J, Torres Cosme R, Rovira J, Ortiz A, Pascale JM et al.. Reciprocal tripartite interactions between the Aedes aegypti midgut microbiota, innate immune system and dengue virus influences vector competence. PLoS Negl Trop Dis. 2012; 6:e1561.
  • [92]Weiss B, Aksoy S. Microbiome influences on insect host vector competence. Trends Parasitol. 2011; 27:514-22.
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