Microbiomes of North American Triatominae: The Grounds for Chagas Disease Epidemiology

. 2018 ; 9 () : 1167. [epub] 20180613

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid29951039

Insect microbiomes influence many fundamental host traits, including functions of practical significance such as their capacity as vectors to transmit parasites and pathogens. The knowledge on the diversity and development of the gut microbiomes in various blood feeding insects is thus crucial not only for theoretical purposes, but also for the development of better disease control strategies. In Triatominae (Heteroptera: Reduviidae), the blood feeding vectors of Chagas disease in South America and parts of North America, the investigation of the microbiomes is in its infancy. The few studies done on microbiomes of South American Triatominae species indicate a relatively low taxonomic diversity and a high host specificity. We designed a comparative survey to serve several purposes: (I) to obtain a better insight into the overall microbiome diversity in different species, (II) to check the long term stability of the interspecific differences, (III) to describe the ontogenetic changes of the microbiome, and (IV) to determine the potential correlation between microbiome composition and presence of Trypanosoma cruzi, the causative agent of Chagas disease. Using 16S amplicons of two abundant species from the southern US, and four laboratory reared colonies, we showed that the microbiome composition is determined by host species, rather than locality or environment. The OTUs (Operational Taxonomic Units) determination confirms a low microbiome diversity, with 12-17 main OTUs detected in wild populations of T. sanguisuga and T. protracta. Among the dominant bacterial taxa are Acinetobacter and Proteiniphilum but also the symbiotic bacterium Arsenophonus triatominarum, previously believed to only live intracellularly. The possibility of ontogenetic microbiome changes was evaluated in all six developmental stages and feces of the laboratory reared model Rhodnius prolixus. We detected considerable changes along the host's ontogeny, including clear trends in the abundance variation of the three dominant bacteria, namely Enterococcus, Acinetobacter, and Arsenophonus. Finally, we screened the samples for the presence of Trypanosoma cruzi. Comparing the parasite presence with the microbiome composition, we assessed the possible significance of the latter in the epidemiology of the disease. Particularly, we found a trend toward more diverse microbiomes in Trypanosoma cruzi positive T. protracta specimens.

Zobrazit více v PubMed

Aksoy E., Telleria E. L., Echodu R., Wu Y., Okedi L. M., Weiss B. L., et al. . (2014). Analysis of multiple Tsetse fly populations in Uganda reveals limited diversity and species-specific gut microbiota. Appl. Environ. Microbiol. 80, 4301–4312. 10.1128/AEM.00079-14 PubMed DOI PMC

Amino R., Porto R. M., Chammas R., Egami M. I., Schenkman S. (1998). Identification and characterization of a sialidase released by the salivary gland of the hematophagous insect Triatoma infestans. J. Biol. Chem. 273, 24575–24582. 10.1074/jbc.273.38.24575 PubMed DOI

Azambuja P., Feder D., Garcia E. S. (2004). Isolation of Serratia marcescens in the midgut of Rhodnius prolixus: impact on the establishment of the parasite Trypanosoma cruzi in the vector. Exp. Parasitol. 107, 89–96. 10.1016/j.exppara.2004.04.007 PubMed DOI

Azambuja P., Garcia E. S., Ratcliffe N. A. (2005). Gut microbiota and parasite transmission by insect vectors. Trends Parasitol. 21, 568–572. 10.1016/j.pt.2005.09.011 PubMed DOI

Bern C., Kjos S., Yabsley M. J., Montgomery S. P. (2011). Trypanosoma cruzi and Chagas' disease in the United States. Clin. Microbiol. Rev. 24, 655–681. 10.1128/CMR.00005-11 PubMed DOI PMC

Bokulich N. A., Subramanian S., Faith J. J., Gevers D., Gordon J. I., Knight R., et al. . (2013). Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods 10, 57–59. 10.1038/nmeth.2276 PubMed DOI PMC

Camacho C., Coulouris G., Avagyan V., Ma N., Papadopoulos J., Bealer K., et al. . (2009). BLAST+: architecture and applications. BMC Bioinformatics 10:421. 10.1186/1471-2105-10-421 PubMed DOI PMC

Caporaso J. G., Bittinger K., Bushman F. D., DeSantis T. Z., Andersen G. L., Knight R. (2010a). PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266–267. 10.1093/bioinformatics/btp636 PubMed DOI PMC

Caporaso J. G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F. D., Costello E. K., et al. . (2010b). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336. 10.1038/nmeth.f.303 PubMed DOI PMC

Cirimotich C. M., Ramirez J. L., Dimopoulos G. (2011). Native microbiota shape insect vector competence for human pathogens. Cell Host Microbe 10, 307–310. 10.1016/j.chom.2011.09.006 PubMed DOI PMC

Crotti E., Balloi A., Hamdi C., Sansonno L., Marzorati M., Gonella E., et al. . (2012). Microbial symbionts: a resource for the management of insect-related problems. Microb. Biotechnol. 5, 307–317. 10.1111/j.1751-7915.2011.00312.x PubMed DOI PMC

Curtis-Robles R., Hamer S. A., Lane S., Levy M. Z., Hamer G. L. (2017a). Bionomics and spatial distribution of triatomine vectors of Trypanosoma cruzi in Texas and other southern states, USA. Am. J. Trop. Med. Hyg. 98, 113–121. 10.4269/ajtmh.17-0526 PubMed DOI PMC

Curtis-Robles R., Snowden K. F., Dominguez B., Dinges L., Rodgers S., Mays G., et al. . (2017b). Epidemiology and molecular typing of Trypanosoma cruzi in naturally-infected hound dogs and associated triatomine vectors in Texas, USA. PLoS Negl. Trop. Dis. 11:e0005298. 10.1371/journal.pntd.0005298 PubMed DOI PMC

Curtis-Robles R., Wozniak E. J., Auckland L. D., Hamer G. L., Hamer S. A. (2015). Combining public health education and disease ecology research: using citizen science to assess Chagas disease entomological risk in Texas. PLoS Negl. Trop. Dis. 9:e0004235. 10.1371/journal.pntd.0004235 PubMed DOI PMC

da Mota F. F., Marinho L. P., Moreira C. J., Lima M. M., Mello C. B., Garcia E. S., et al. . (2012). Cultivation-independent methods reveal differences among bacterial gut microbiota in triatomine vectors of Chagas disease. PLoS Negl. Trop. Dis. 6:e1631. 10.1371/journal.pntd.0001631 PubMed DOI PMC

de Fuentes-Vicente J. A., Gutiérrez-Cabrera A. E., Flores-Villegas A. L., Lowenberger C., Benelli G., Salazar-Schettino P. M., et al. . (2018). What makes an effective Chagas disease vector? Factors underlying Trypanosoma cruzi-triatomine interactions. Acta Trop. 183, 23–31. 10.1016/j.actatropica.2018.04.008 PubMed DOI

Díaz S., Villavicencio B., Correia N., Costa J., Haag K. L. (2016). Triatomine bugs, their microbiota and Trypanosoma cruzi: asymmetric responses of bacteria to an infected blood meal. Parasit. Vectors 9:636. 10.1186/s13071-016-1926-2 PubMed DOI PMC

Duguma D., Hall M. W., Rugman-Jones P., Stouthamer R., Terenius O., Neufeld J. D., et al. . (2015). Developmental succession of the microbiome of Culex mosquitoes. BMC Microbiol. 15:140. 10.1186/s12866-015-0475-8 PubMed DOI PMC

Edgar R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998. 10.1038/nmeth.2604 PubMed DOI

Edwards M. S., Stimpert K. K., Montgomery S. P. (2017). Addressing the challenges of Chagas disease: an emerging health concern in the United States. Infect. Dis. Clin. Pract. 25:118 10.1097/IPC.0000000000000512 PubMed DOI PMC

Fox J., Weisberg S. (2011). An R Companion to Applied Regression, 2nd Edn. Thousand Oaks, CA: Sage Publications; Available online at: http://socserv.socsci.mcmaster.ca/jfox/Books/Companion.

Galvão C., Carcavallo R., Rocha D. D. S., Jurberg J. (2003). A checklist of the current valid species of the subfamily Triatominae Jeannel, 1919 (Hemiptera, Reduviidae) and their geographical distribution, with nomenclatural and taxonomic notes. Zootaxa 202, 1–36. 10.11646/zootaxa.202.1.1 DOI

Garcia E. S., Castro D. P., Figueiredo M. B., Azambuja P. (2010). Immune homeostasis to microorganisms in the guts of triatomines (Reduviidae): a review. Mem. Inst. Oswaldo Cruz 105, 605–610. 10.1590/S0074-02762010000500001 PubMed DOI

Garcia M. N., Burroughs H., Gorchakov R., Gunter S. M., Dumonteil E., Murray K. O., et al. . (2017). Molecular identification and genotyping of Trypanosoma cruzi DNA in autochthonous Chagas disease patients from Texas, USA. Infect. Genet. Evol. 49, 151–156. 10.1016/j.meegid.2017.01.016 PubMed DOI

Gimonneau G., Tchioffo M. T., Abate L., Boissière A., Awono-Ambéné P. H., Nsango S. E., et al. . (2014). Composition of Anopheles coluzzii and Anopheles gambiae microbiota from larval to adult stages. Infect. Genet. Evol. 28, 715–724. 10.1016/j.meegid.2014.09.029 PubMed DOI

Gourbière S., Dorn P., Tripet F., Dumonteil E. (2012). Genetics and evolution of triatomines: from phylogeny to vector control. Heredity 108, 190–202. 10.1038/hdy.2011.71 PubMed DOI PMC

Guindon S., Dufayard J. F., Lefort V., Anisimova M., Hordijk W., Gascuel O. (2010). New Algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321. 10.1093/sysbio/syq010 PubMed DOI

Gumiel M., da Mota F. F., Rizzo Vde S., Sarquis O., de Castro D. P., Lima M. M., et al. . (2015). Characterization of the microbiota in the guts of Triatoma brasiliensis and Triatoma pseudomaculata infected by Trypanosoma cruzi in natural conditions using culture independent methods. Parasit. Vectors 8:245. 10.1186/s13071-015-0836-z PubMed DOI PMC

Gunter S. M., Murray K. O., Gorchakov R., Beddard R., Rossmann S. N., Montgomery S. P., et al. . (2017). Likely autochthonous transmission of Trypanosoma cruzi to humans, south central Texas, USA. Emerg. Infect. Dis. 23, 500–503. 10.3201/eid2303.161157 PubMed DOI PMC

Hafner M. S., Sudman P. D., Villablanca F. X., Spradling T. A., Demastes J. W., Nadler S. A. (1994). Disparate rates of molecular evolution in cospeciating hosts and parasites. Science 265, 1087–1090. 10.1126/science.8066445 PubMed DOI

Hegde S., Rasgon J. L., Hughes G. L. (2015). The microbiome modulates arbovirus transmission in mosquitoes. Curr. Opin. Virol. 15, 97–102. 10.1016/j.coviro.2015.08.011 PubMed DOI PMC

Hernández C., Salazar C., Brochero H., Teherán A., Buitrago L. S., Vera M., et al. . (2016). Untangling the transmission dynamics of primary and secondary vectors of Trypanosoma cruzi in Colombia: parasite infection, feeding sources and discrete typing units. Parasit. Vectors 9:620. 10.1186/s13071-016-1907-5 PubMed DOI PMC

Husseneder C., Park J. S., Howells A., Tikhe C. V., Davis J. A. (2017). Bacteria associated with Piezodorus guildinii (Hemiptera: Pentatomidae), with special reference to those transmitted by feeding. Environ. Entomol. 46, 159–166. 10.1093/ee/nvw112 PubMed DOI

Hypša V. (1993). Endosytobionts of Triatoma infestans: distribution and transmission. J. Invertebr. Pathol. 61, 32–38. 10.1006/jipa.1993.1006 DOI

Hypša V., Aksoy S. (2003). Phylogenetic characterization of two transovarially transmitted endosymbionts of the bedbug Cimex lectularius (Heteroptera: Cimicidae). Insect Mol. Biol. 6, 301–304. 10.1046/j.1365-2583.1997.00178.x PubMed DOI

Jupatanakul N., Sim S., Dimopoulos G. (2014). The insect microbiome modulates vector competence for arboviruses. Viruses 6, 4294–4313. 10.3390/v6114294 PubMed DOI PMC

Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., et al. . (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649. 10.1093/bioinformatics/bts199 PubMed DOI PMC

Klepzig K. D., Adams A. S., Handelsman J., Raffa K. F. (2009). Symbioses: a key driver of insect physiological processes, ecological interactions, evolutionary diversification, and impacts on humans. Environ. Entomol. 38, 67–77. 10.1603/022.038.0109 PubMed DOI

Kruskal W. H., Wallis W. A. (1952). Use of ranks in one-criterion variance analysis. J. Am. Stat. Assoc. 47, 583–621. 10.1080/01621459.1952.10483441 DOI

Kwong W. K., Engel P., Koch H., Moran N. A. (2014). Genomics and host specialization of honey bee and bumble bee gut symbionts. Proc. Natl. Acad. Sci. U.S.A. 111, 11509–11514. 10.1073/pnas.1405838111 PubMed DOI PMC

Leonhardt S. D., Kaltenpoth M. (2014). Microbial communities of three sympatric Australian stingless bee species. PLoS ONE 9:e10571 10.1371/journal.pone.0105718 PubMed DOI PMC

McPhatter L., Roachell W., Mahmood F., Hoffman L., Lockwood N., Osuna A., et al. . (2012). Vector surveillance to determine species composition and occurrence of Trypanosoma cruzi at three military installations in San Antonio, Texas. US Army Med. Dep. J. 3–12, 12–21. PubMed

Mesquita R. D., Vionette-Amaral R. J., Lowenberger C., Rivera-Pomar R., Monteiro F. A., Minx P., et al. . (2015). Genome of Rhodnius prolixus, an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection. Proc. Natl. Acad. Sci. U.S.A. 112, 14936–14941. 10.1073/pnas.1506226112 PubMed DOI PMC

Minard G., Mavingui P., Moro C. V. (2013). Diversity and function of bacterial microbiota in the mosquito holobiont. Parasit. Vectors 6:146. 10.1186/1756-3305-6-146 PubMed DOI PMC

Minchin P. R. (1987). An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio 69, 89–107. 10.1007/BF00038690 DOI

Montgomery S. P., Starr M. C., Cantey P. T., Edwards M. S., Meymandi S. K. (2014). Neglected parasitic infections in the United States: Chagas disease. Am. J. Trop. Med. Hyg. 90, 814–818. 10.4269/ajtmh.13-0726 PubMed DOI PMC

Moser D. R., Kirchhoff L. V., Donelson J. E. (1989). Detection of Trypanosoma cruzi by DNA amplification using the polymerase chain reaction. J. Clin. Microbiol. 27, 1477–1482. PubMed PMC

Nikoh N., Hosokawa T., Moriyama M., Oshima K., Hattori M., Fukatsu T. (2014). Evolutionary origin of insect–Wolbachia nutritional mutualism. Proc. Nat. Acad. Sci. U.S.A. 111, 10257–10262. 10.1073/pnas.1409284111 PubMed DOI PMC

Nováková E., Husník F., Šochová E., Hypša V. (2015). Arsenophonus and Sodalis symbionts in louse flies: an analogy to the Wigglesworthia and Sodalis system in tsetse flies. Appl. Environ. Microbiol. 81, 6189–6199. 10.1128/AEM.01487-15 PubMed DOI PMC

Nováková E., Hypša V., Nguyen P., Husník F., Darby A. C. (2016). Genome sequence of Candidatus Arsenophonus lipopteni, the exclusive symbiont of a blood sucking fly Lipoptena cervi (Diptera: Hippoboscidae). Stand. Genomic Sci. 11:72. 10.1186/s40793-016-0195-1 PubMed DOI PMC

Novakova E., Woodhams D. C., Rodríguez-Ruano S. M., Brucker R. M., Leff J. W., Maharaj A., et al. . (2017). Mosquito microbiome dynamics, a background for prevalence and seasonality of West Nile Virus. Front. Microbiol. 8:526. 10.3389/fmicb.2017.00526 PubMed DOI PMC

Nunes-da-Fonseca R., Berni M., Tobias-Santos V., Pane A., Araujo H. M. (2017). Rhodnius prolixus: from classical physiology to modern developmental biology. Genesis 55:e22995. 10.1002/dvg.22995 PubMed DOI

Núñez J. A., Lazzari C. R. (1990). Rearing of Triatoma infestans Klug (Het., Reduviidae) in the absence of a live host. J. Appl. Entomol. 109, 87–92. 10.1111/j.1439-0418.1990.tb00023.x DOI

Oksanen J., Blanchet F. G., Kindt R., Legendre P., Minchin P. R., O'Hara R. B., et al. (2013). Vegan: Community Ecology Package. The Comprehensive R Archive Network (CRAN) Available online at: http://CRAN.R-project.org/package=vegan.

Oliver K. M., Martinez A. J. (2014). How resident microbes modulate ecologically-important traits of insects. Curr. Opin. Insect Sci. 4, 1–7. 10.1016/j.cois.2014.08.001 PubMed DOI

Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., et al. . (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596. 10.1093/nar/gks1219 PubMed DOI PMC

R Development Core Team (2014). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing Vienna; Available online at: http://www.R-project.org/

Saldaña M. A., Hegde S., Hughes G. L. (2017). Microbial control of arthropod-borne disease. Mem. Inst. Oswaldo Cruz 112, 81–93. 10.1590/0074-02760160373 PubMed DOI PMC

Sorfová P., Skeríková A., Hypsa V. (2008). An effect of 16S rRNA intercistronic variability on coevolutionary analysis in symbiotic bacteria: molecular phylogeny of Arsenophonus triatominarum. Syst. Appl. Microbiol. 31, 88–100. 10.1016/j.syapm.2008.02.004 PubMed DOI

Sudakaran S., Salem H., Kost C., Kaltenpoth M. (2012). Geographical and ecological stability of the symbiotic mid-gut microbiota in European firebugs, Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae). Mol. Ecol. 21, 6134–6151. 10.1111/mec.12027 PubMed DOI

Taracena M. L., Oliveira P. L., Almendares O., Umaña C., Lowenberger C., Dotson E. M., et al. . (2015). Genetically modifying the insect gut microbiota to control Chagas disease vectors through systemic RNAi. PLoS Negl. Trop. Dis. 9:e0003358. 10.1371/journal.pntd.0003358 PubMed DOI PMC

Weiss B., Aksoy S. (2011). Microbiome influences on insect host vector competence. Trends Parasitol. 27, 514–522. 10.1016/j.pt.2011.05.001 PubMed DOI PMC

Weiss S., Xu Z. Z., Peddada S., Amir A., Bittinger K., Gonzalez A., et al. . (2017). Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 5:27. 10.1186/s40168-017-0237-y PubMed DOI PMC

WHO (2015). Chagas disease in Latin America: an epidemiological update based on 2010 estimates. Releve Epidemiol. Hebd. 90, 33–43. PubMed

Wickham H. (2009). Ggplot2: Elegant Graphics for Data Analysis. New York, NY: Springer-Verlag; Available online at: http://ggplot2.org.

Wilkes T. E., Duron O., Darby A. C., Hypša V., Nováková E., Hurst G. D. D. (2011). The genus Arsenophonus, in Manipulative Tenants: Bacteria Associated With Arthropods, eds Zchori-Fein E., Bourtzis K. (Boca Raton, FL: CRC Press; ), 520–528.

Wozniak E. J., Lawrence G., Gorchakov R., Alamgir H., Dotson E., Sissel B., et al. . (2015). The biology of the Triatomine bugs native to south central Texas and assessment of the risk they pose for autochthonous Chagas disease exposure. J. Parasitol. 101, 520–528. 10.1645/15-748 PubMed DOI

Zhang G., Browne P., Zhen G., Johnston A., Cadillo-Quiroz H., Franz N. (2017). Endosymbiont diversity and evolution across the weevil tree of life. bioRxiv, 171181 10.1101/171181 DOI

Zolnik C. P., Prill R. J., Falco R. C., Daniels T. J., Kolokotronis S. O. (2016). Microbiome changes through ontogeny of a tick pathogen vector. Mol. Ecol. 25, 4963–4977. 10.1111/mec.13832 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...