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Coinfection by Trypanosoma cruzi and a fungal pathogen increases survival of Chagasic bugs: advice against a fungal control strategy

Published online by Cambridge University Press:  06 November 2019

A. Laura Flores-Villegas ,
Margarita Cabrera-Bravo ,
José A. De Fuentes-Vicente ,
J. Guillermo Jiménez-Cortés ,
Paz María Salazar-Schettino ,
Martha Irene Bucio-Torres  and
Alex Córdoba-Aguilar Open the ORCID record for Alex Córdoba-Aguilar [Opens in a new window]
A. Laura Flores-Villegas
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, Mexico City, Mexico
Margarita Cabrera-Bravo*
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, Mexico City, Mexico
José A. De Fuentes-Vicente
Affiliation:
Instituto de Ciencias Biológicas, Universidad de Ciencias y Artes de Chiapas, Libramiento Norte Poniente 1150, CP 29029. Tuxtla Gutiérrez, Chiapas, Mexico
J. Guillermo Jiménez-Cortés
Affiliation:
Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, Apdo. P. 70-275, Circuito Exterior, Ciudad Universitaria, 04510 Coyoacán, Mexico City, Mexico
Paz María Salazar-Schettino
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, Mexico City, Mexico
Martha Irene Bucio-Torres
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, Mexico City, Mexico
Alex Córdoba-Aguilar*
Affiliation:
Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, Apdo. P. 70-275, Circuito Exterior, Ciudad Universitaria, 04510 Coyoacán, Mexico City, Mexico
*
Author for correspondence: Margarita Cabrera-Bravo, E-mail: imay@unam.mx; Alex Córdoba-Aguilar, E-mail: acordoba@iecologia.unam.mx
Author for correspondence: Margarita Cabrera-Bravo, E-mail: imay@unam.mx; Alex Córdoba-Aguilar, E-mail: acordoba@iecologia.unam.mx
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Abstract

Triatomine bugs carry the parasitic protozoa Trypanosoma cruzi, the causal agent of Chagas disease. It is known that both the parasite and entomopathogenic fungi can decrease bug survival, but the combined effect of both pathogens is not known, which is relevant for biological control purposes. Herein, the survival of the triatomine Meccus pallidipennis (Stal, 1872) was compared when it was coinfected with the fungus Metarhizium anisopliae (Metschnikoff) and T. cruzi, and when both pathogens acted separately. The immune response of the insect was also studied, using phenoloxidase activity in the bug gut and hemolymph, to understand our survival results. Contrary to expectations, triatomine survival was higher in multiple than in single challenges, even though the immune response was lower in cases of multiple infection. We postulate that T. cruzi exerts a protective effect and/or that the insect reduced the resources allocated to defend itself against both pathogens. Based on the present results, the use of M. anisopliae as a control agent should be re-considered.

Keywords

BiocontrolMeccus pallidipennisMetarhizium anisopliaemultiple infectionTrypanosoma cruzi
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 3 , June 2020 , pp. 363 - 369
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Copyright
Copyright © Cambridge University Press 2019

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References

Alizon, S, de Roode, JC and Michalakis, Y (2013) Multiple infections and the evolution of virulence. Ecology Letters 16, 556–567.Google ScholarPubMed
Azambuja, P, Feder, D, Mello, CB, Gomes, SAO and Garcia, ES (1999) Immunity in Rhodnius prolixus: Trypanosomatid–vector interactions. Memorias do Instituto Oswaldo Cruz 94, 219–222.CrossRefGoogle ScholarPubMed
Bautista, NL, Rojas, G, De Haro, I, Bucio, M and Salazar-Schettino, PM (2001) Comportamiento biológico de Triatoma pallidipennis (Hemiptera: Reduvidae) en el estado de Morelos, México. Boletín Chileno de Parasitología 57, 22–27.Google Scholar
Benelli, G (2018) Managing mosquitoes and ticks in a rapidly changing world – facts and trends. Saudi Journal of Biological Sciences 26, 921–929.CrossRefGoogle Scholar
Bordes, F and Morand, S (2011) The impact of multiple infections on wild animal hosts: a review. Infection, Ecology and Epidemiology 1, 7346.Google ScholarPubMed
Botto-Mahan, C, Cattan, PE and Medel, R (2006) Chagas disease parasite induces behavioural changes in the kissing bug Mepraia spinolai. Acta Tropica 98, 219–223.CrossRefGoogle ScholarPubMed
Brunner-Mendoza, C, Reyes-Montes, MR, Moonjely, S, Bidochka, MJ and Toriello, C (2019) A review on the genus Metarhizium as an entomopathogenic microbial biocontrol agent with emphasis on its use and utility in Mexico. Biocontrol Science and Technology 29, 83–102.CrossRefGoogle Scholar
Choisy, M and de Roode, JC (2010) Mixed infections and the evolution of virulence: effects of resource competition, parasite plasticity, and impaired host immunity. American Naturalist 175, E105–E118.Google ScholarPubMed
Cordero-Montoya, G, Flores-Villegas, AL, Salazar-Schettino, PM, Vences-Blanco, MO, Rocha-Ortega, M, Gutiérrez-Cabrera, AE, Rojas-Ortega, E and Córdoba-Aguilar, A (2019) The cost of being a killer´s accomplice: Trypanosoma cruzi impairs the fitness of kissing bug. Parasitology Research 118, 2523–2529.CrossRefGoogle Scholar
Daquinag, AC, Nakamura, S, Takao, T, Shimonishi, Y and Tsukamoto, T (1995) Primary structure of a potent endogenous DOPA-containing inhibitor of phenol oxidase from Musca domestica. Proceedings of the National Academy of Sciences of the United States of America 92, 2964–2968.CrossRefGoogle ScholarPubMed
De Fuentes-Vicente, JA, Cabrera-Bravo, M, Enríquez-Vara, JN, Bucio-Torres, M, Gutiérrez-Cabrera, AE, Vidal-López, DG, Martínez-Ibarra, JA, Salazar-Schettino, PM and Córdoba-Aguilar, A (2016) Relationships between altitude, triatomine (Triatoma dimidiata) immune response and virulence of Trypanosoma cruzi, the causal agent of Chagas’ disease. Medical Veterinary and Entomology 31, 63–71.CrossRefGoogle ScholarPubMed
De Fuentes-Vicente, JA, Gutiérrez-Cabrera, AE, Flores-Villegas, AL, Lowenberger, C, Benelli, G, Salazar-Schettino, PM and Cordoba-Aguilar, A (2018) What makes an effective Chagas disease vector? Factors underlying Trypanosoma cruzi-triatomine interactions. Acta Tropica 183, 23–31.CrossRefGoogle ScholarPubMed
De Oliveira, ABB, Alevi, KCC, Imperador, CHL, Madeira, FF and de Azeredo-Oliveira, MTV (2018) Parasite–vector interaction of Chagas disease: a mini review. American Journal of Tropical Medicine and Hygiene 98, 653–655.CrossRefGoogle ScholarPubMed
Elliot, SL, Rodrigues, JDO, Lorenzo, MG, Martins-Filho, OA and Guarneri, AA (2015) Trypanosoma cruzi, etiological agent of Chagas disease, is virulent to its triatomine vector Rhodnius prolixus in a temperature-dependent manner. PLoS Neglected Tropical Diseases 9, e0003646.CrossRefGoogle Scholar
Favila-Ruiz, G, Jiménez-Cortés, JG, Córdoba-Aguilar, A, Salazar-Schettino, PM, Gutiérrez-Cabrera, AE, Pérez-Torres, A, De Fuentes-Vicente, JA, Vences-Blanco, MO, Bucio-Torres, MI, Flores-Villegas, AL and Cabrera-Bravo, M (2018) Effects of Trypanosoma cruzi on the phenoloxidase and prophenoloxidase activity in the vector Meccus pallidipennis (Hemiptera:Reduviidae). Parasites & Vectors 11, 434.CrossRefGoogle Scholar
Fellet, MR, Lorenzo, MG, Elliot, SL, Carrasco, D and Guarneri, AA (2014) Effects of infection by Trypanosoma cruzi and Trypanosoma rangeli on the reproductive performance of the vector Rhodnius prolixus. PLoS ONE 9, e105255.CrossRefGoogle ScholarPubMed
Flores-Villegas, AL, Salazar-Schettino, PM, Córdoba-Aguilar, A, Gutiérrez-Cabrera, AE, Rojas-Wastavino, GE, Bucio-Torres, MI and Cabrera-Bravo, M (2015) Immune defence mechanisms of triatomines against bacteria, viruses, fungi and parasites. Bulletin of Entomological Research 5, 523–532.CrossRefGoogle Scholar
Flores-Villegas, AL, Cabrera-Bravo, M, Toriello, C, Bucio-Torres, MI, Salazar-Schettino, PM and Córdoba-Aguilar, A (2016) Survival and immune response of the Chagas vector Meccus pallidipennis (Hemiptera: Reduviidae) against two entomopathogenic fungi, Metarhizium anisopliae and Isaria fumosorosea. Parasites & Vectors 9, 176.CrossRefGoogle ScholarPubMed
Flores-Villegas, AL, Cabrera-Bravo, M, Pérez-Torres, A, Córdoba-Aguilar, A, Salazar-Schettino, PM, Hernández-Velázquez, VM and Toriello, C (2018) Effects on Meccus pallidipennis (Hemiptera: Reduviidae) eggs exposed to entomopathogenic fungi: exploring alternatives to control Chagas disease. Journal of Medical Entomology 56, 284–290.CrossRefGoogle Scholar
Garcia, AR, de Paula Rocha, A, Moreira, CC, Rocha, SL, Guarneri, AA and Elliot, SL (2016) Screening of fungi for biological control of a triatomine vector of Chagas disease: temperature and trypanosome infection as factors. PLoS Neglected Tropical Diseases 10, e0005128.CrossRefGoogle ScholarPubMed
González-Santoyo, I and Córdoba-Aguilar, A (2012) Phenoloxidase: a key component of the insect immune system. Entomologia Experimentalis et Applicata 142, 1–16.CrossRefGoogle Scholar
Herbison, R, Lagrue, C and Poulin, R (2018) The missing link in parasite manipulation of host behaviour. Parasites & Vectors 11, 222.CrossRefGoogle ScholarPubMed
Hinestroza, G, Ortiz, MI and Molina, J (2016) Behavioral fever response in Rhodnius prolixus (Reduviidae: Triatominae) to intracoelomic inoculation of Trypanosoma cruzi. Revista da Sociedade Brasileira de Medicina Tropical 49, 425–432.CrossRefGoogle ScholarPubMed
Hurd, H (2003) Manipulation of medically important insect vectors by their parasites. Annual Review of Entomology 48, 141–161.CrossRefGoogle ScholarPubMed
Kamiya, T, Mideo, N and Alizon, S (2018) Coevolution of virulence and immunosuppression in multiple infections. Journal of Evolutionary Biology 31, 995–1005.CrossRefGoogle ScholarPubMed
López-Villavicencio, M, Courjol, F, Gibson, AK, Hood, ME, Jonot, O, Shykoff, JA and Giraud, T (2011) Competition, cooperation among kin, and virulence in multiple infections. Evolution 65, 1357–1366.CrossRefGoogle ScholarPubMed
Lorono-Pino, MA, Cropp, CB, Farfan, JA, Vorndam, AV, Rodríguez-Angulo, EM, Rosado-Paredes, EP, Flores-Flores, LF, Beaty, BJ and Gubler, DJ (1999) Common occurrence of concurrent infections by multiple dengue virus serotypes. The American Journal of Tropical Medicine and Hygiene 61, 725–730.CrossRefGoogle ScholarPubMed
Mahmud, R, Lim, YAL and Amir, A (2018) Medical Parasitology: A Textbook. Gewerbestrasse, Switzerland: Springer.Google Scholar
Martínez-Ibarra, JA and Katthain-Duchateau, G (1999) Biology of Triatoma pallidipennis Stal 1945 (Hemiptera: Reduviidae: Triatominae) under laboratory conditions. Memórias do Instituto Oswaldo Cruz 94, 837–839.CrossRefGoogle Scholar
Martínez-Ibarra, JA, García-Benavidez, G, Vargas-Llamas, V, Bustos-Saldaña, R and Montañez-Valdes, OD (2012) Bionomics of populations on Meccus pallidipennis (Stal), 1872 (Hemiptera: Reduviidae from Mexico. Journal of Vector Ecology 37, 474–477.CrossRefGoogle ScholarPubMed
Marliére, NP, Latorre-Estivalis, JM, Lorenzo, MG, Carrasco, D, Alves-Silva, J, de Rodrigues, JO, de Ferreira, LL, de Lara, LM, Lowenberger, C and Guarneri, AA (2015) Trypanosomes modify the behavior of their insect hosts: effects on locomotion and on the expression of a related gene. PLoS Neglected Tropical Diseases 9, e0003973.CrossRefGoogle ScholarPubMed
McClure, CD, Zhong, W, Hunt, VL, Chapman, FM, Hill, FV and Priest, NK (2014) Hormesis results in trade-offs with immunity. Evolution 68, 2225–2233.Google ScholarPubMed
Peterson, JK, Graham, AL, Elliott, RJ, Dobson, AP and Chávez, OT (2016) Trypanosoma cruzi–Trypanosoma rangeli co-infection ameliorates negative effects of single trypanosome infections in experimentally infected Rhodnius prolixus. Parasitology 143, 1157–1167.CrossRefGoogle ScholarPubMed
Poinar, GO (2018) Nematodes for Biological Control of Insects. Miami, Florida: CRC Press.CrossRefGoogle Scholar
Pollitt, LC, Bram, JT, Blanford, S, Jones, MJ and Read, AF (2015) Existing infection facilitates establishment and density of malaria parasites in their mosquito vector. PLoS Pathogens 11, e1005003.CrossRefGoogle ScholarPubMed
Read, FA (1994) The evolution of virulence. Trends in Microbiology 2, 73–76.CrossRefGoogle ScholarPubMed
Rechcigl, JE and Rechcigl, NA (2016) Insect Pest Management: Techniques for Environmental Protection. London: CRC Press.CrossRefGoogle Scholar
Ribeiro, JCM, Genta, FA, Sorgine, MHF, Logullo, R, Mesquita, RD, Paiva-Silva, GO, Majerowicz, D, Medeiros, M, Koerich, L, Terra, WR, Ferreira, C, Pimentel, AC, Bisch, PM, Leite, DC, Diniz, MMP, Lídio da, SGV, Junior, J, Da Silva, ML, Araujo, RN, Caroline, A, Gandara, P, Brosson, S, Salmon, D, Bousbata, S, González-Caballero, N, Silber, AM, Alves-Bezerra, M, Gondim, KC, Silva-Neto, MAC, Atella, GC, Araujo, H, Dias, FA, Polycarpo, C, Vionette-Amaral, RJ, Fampa, P, Melo, ACA, Tanaka, AS, Balczun, C, Oliveira, JHM, Gonçalves, RLS, Lazoski, C, Rivera-Pomar, R, Diambra, L, Schaub, GA, Garcia, ES, Azambuja, P, Braz, GRC and Oliveira, PL (2014) An insight into the transcriptome of the digestive tract of the bloodsucking bug, Rhodnius prolixus. PloS Neglected Tropical Diseases 8, e2594.CrossRefGoogle ScholarPubMed
Rückert, C, Weger-Lucarelli, J, Garcia-Luna, SM, Young, MC, Byas, AD, Murrieta, RA, Fauver, JR and Ebel, GD (2017) Impact of simultaneous exposure to arboviruses on infection and transmission by Aedes aegypti mosquitoes. Nature Communications 8, 15412.CrossRefGoogle ScholarPubMed
Schmid-Hempel, P (2011) Evolutionary Parasitology: The Integrated Study of Infections, Immunology, Ecology, and Genetics. New York, NY: Oxford University Press.Google Scholar
Toriello, C (2003) Bioseguridad de Metharhizium anisopliae (Metschnikoff) Sorokin (Hyphomycete). Vedalia 10, 107–113.Google Scholar
Toriello, C, Pérez-Torres, A, Burciaga-Díaz, A, Navarro-Barranco, H, Pérez-Mejía, A, Lorenzana-Jiménez, M and Mier, T (2006) Lack of acute pathogenicity and toxicity in mice of an isolate of Metarhizium anisopliae var. anisopliae from spittlebugs. Ecotoxicology and Environmental Safety 65, 278–287.CrossRefGoogle ScholarPubMed
Toriello, C, Montoya-Sansón, E, Zavala-Ramírez, M, Navarro-Barranco, H, Basilio-Hernández, D, Hernández-Velázquez, V and Mier, T (2008) Virulencia y termotolerancia de cultivos monospóricos de Metarhizium anisopliae var. Anisopliae de la mosca pinta (Hemiptera: Cercopidae). Revista Mexicana de Micología 28, 57–66.Google Scholar
Vieira, CS, Waniek, PJ, Mattos, DP, Castro, DP, Mello, CB, Ratcliffe, NA, Garcia, ES and Azambuja, P (2014) Humoral responses in Rhodnius prolixus: bacterial feeding induces differential patterns of antibacterial activity and enhances mRNA levels of antimicrobial peptides in the midgut. Parasites and Vectors 7, 1–13.CrossRefGoogle ScholarPubMed
Whitten, MMA, Mello, CB, Gomes, SAO, Nigam, Y, Azambuja, P, Garcia, ES and Ratcliffe, NA (2001) Role of superoxide and reactive nitrogen intermediates in Rhodnius prolixus (Reduviidae)/Trypanosoma rangeli interactions. Experimental Parasitology 98, 44–57.CrossRefGoogle ScholarPubMed
Whitten, M, Sun, F, Tew, I, Schaub, G, Soukou, C, Nappi, A and Ratcliffe, N (2007) Differential modulation of Rhodnius prolixus nitric oxide activities following challenge with Trypanosoma rangeli, T. cruzi and bacterial cell wall components. Insect Biochemistry and Molecular Biology 37, 440–452.CrossRefGoogle ScholarPubMed
WHO Expert Committee on the Control of Chagas Disease (2000: Brasilia, Brazil) & World Health Organization (2002) Control of Chagas disease: second report of the WHO expert committee. Geneva: World Health Organization. http://www.who.int/iris/handle/10665/42443.Google Scholar