Microbiomes of North American Triatominae: The Grounds for Chagas Disease Epidemiology
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
29951039
PubMed Central
PMC6008411
DOI
10.3389/fmicb.2018.01167
Knihovny.cz E-zdroje
- Klíčová slova
- Rhodnius prolixus, Triatominae, Trypanosoma cruzi, microbiome, ontogeny,
- Publikační typ
- časopisecké články MeSH
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.
Biology Centre of ASCR Institute of Parasitology Ceske Budejovice Czechia
Department of Entomology Southwestern Biological Institute Tucson AZ United States
Faculty of Science University of South Bohemia Ceske Budejovice Czechia
US Army Public Health Command Central JBSA Fort Sam Houston Houston TX United States
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
Microbiome of pear psyllids: A tale about closely related species sharing their endosymbionts
Methodological Insight Into Mosquito Microbiome Studies