Abstract
Zika virus (ZIKV), a mosquito-borne flavivirus, poses a serious threat to public health worldwide, and Aedes albopictus is one of its vectors. To evaluate the potential of the entomopathogenic fungus Beauveria bassiana for ZIKV vector control, we compared the vectorial capacity of Ae. albopictus females blood-fed with ZIKV with or without exposure to Beauveria bassiana. We found that fungal infection significantly decreased the amount of ZIKV by 3.6-, 12.3- and 7.8-fold in mosquito midguts, heads and salivary glands, respectively. Similarly, fungal infection also reduced the rates of ZIKV dissemination, potential transmission and potential population transmission for mosquitoes by 26.8%, 38.4% and 35.2%, respectively. On the other hand, the median survival time and fecundity of fungus-infected mosquitoes were reduced by 84.2% and 39.8% in comparison with those of the non-fungus-infected mosquitoes. The first gonotrophic cycle length was increased by 15.3% because of fungal infection. This study revealed that B. bassiana infection significantly reduced the vectorial capacity of A. albopictus for ZIKV, which suggested that B. bassiana could be broadly and efficiently used in the field for the control of Zika vectors.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Almeida AP, Baptista SS, Sousa CA et al (2005) Bioecology and vectorial capacity of Aedes albopictus (Diptera: Culicidae) in Macao, China, in relation to dengue virus transmission. J Med Entomol 42:419–428
Araujo LM, Ferreira ML, Nascimento OJ (2016) Guillain–Barre syndrome associated with the Zika virus outbreak in Brazil. Arq Neuropsiquiatr 74:253–255. https://doi.org/10.1590/0004-282x20160035
Baronti C, Piorkowski G, Charrel RN, Boubis L, Leparc-Goffart I, de Lamballerie X (2014) Complete coding sequence of Zika virus from a French Polynesia outbreak in 2013. Genome Announc. https://doi.org/10.1128/genomea.00500-14
Blanford S, Chan BH, Jenkins N, Sim D, Turner RJ, Read AF, Thomas MB (2005) Fungal pathogen reduces potential for malaria transmission. Science 308:1638–1641. https://doi.org/10.1126/science.1108423
Bogoch II, Brady OJ, Kraemer MUG et al (2016) Anticipating the international spread of Zika virus from Brazil. Lancet 387:335–336. https://doi.org/10.1016/s0140-6736(16)00080-5
Bukhari T, Takken W, Koenraadt CJ (2011) Development of Metarhizium anisopliae and Beauveria bassiana formulations for control of malaria mosquito larvae. Parasit Vectors 4:23. https://doi.org/10.1186/1756-3305-4-23
Cao-Lormeau VM, Blake A, Mons S et al (2016) Guillain–Barre syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet 387:1531–1539. https://doi.org/10.1016/s0140-6736(16)00562-6
CDC (2018) World map of areas with risk of Zika. Centers for disease control and prevention. https://wwwnc.cdc.gov/travel/page/world-map-areas-with-zika. Accessed 25 July 2018
Ciota AT, Bialosuknia SM, Ehrbar DJ, Kramer LD (2017) Vertical Transmission of Zika virus by Aedes aegypti and Ae. albopictus mosquitoes. Emerg Infect Dis 23:880–882. https://doi.org/10.3201/eid2305.162041
Clark TB, Kellen WR, Fukuda T, Lindegren JE (1968) Field and laboratory studies on the pathogenicity of the fungus Beauveria bassiana to three genera of mosquitoes. J Invertebr Pathol 11:1–7
Darbro JM, Johnson PH, Thomas MB, Ritchie SA, Kay BH, Ryan PA (2012) Effects of Beauveria bassiana on survival, blood-feeding success, and fecundity of Aedes aegypti in laboratory and semi-field conditions. Am J Trop Med Hyg 86:656–664. https://doi.org/10.4269/ajtmh.2012.11-0455
de Paula AR (2008) Susceptibility of adult Aedes aegypti (Diptera: Culicidae) to infection by Metarhizium anisopliae and Beauveria bassiana: prospects for Dengue vector control. Biocontrol Sci Technol 18:1017–1025
Deng SQ, Cai QD, Deng MZ, Huang Q, Peng HJ (2017) Scorpion neurotoxin AaIT-expressing Beauveria bassiana enhances the virulence against Aedes albopictus mosquitoes. AMB Express 7:121. https://doi.org/10.1186/s13568-017-0422-1
Dong Y, Morton JC Jr, Ramirez JL, Souza-Neto JA, Dimopoulos G (2012) The entomopathogenic fungus Beauveria bassiana activate toll and JAK-STAT pathway-controlled effector genes and anti-dengue activity in Aedes aegypti. Insect Biochem Mol Biol 42:126–132. https://doi.org/10.1016/j.ibmb.2011.11.005
Duffy MR, Chen TH, Hancock WT et al (2009) Zika virus outbreak on Yap Island, Federated States of Micronesia. N Engl J Med 360:2536–2543. https://doi.org/10.1056/NEJMoa0805715
Fang W, St Leger RJ (2012) Enhanced UV resistance and improved killing of malaria mosquitoes by photolyase transgenic entomopathogenic fungi. PLoS ONE 7:e43069
Farenhorst M, Farina D, Scholte EJ, Takken W, Hunt RH, Coetzee M, Knols BG (2008) African water storage pots for the delivery of the entomopathogenic fungus Metarhizium anisopliae to the malaria vectors Anopheles gambiae s.s. and Anopheles funestus. Am J Trop Med Hyg 78:910–916
Farenhorst M, Hilhorst A, Thomas MB, Knols BG (2011) Development of fungal applications on netting substrates for malaria vector control. J Med Entomol 48:305–313
Franz AW, Kantor AM, Passarelli AL, Clem RJ (2015) Tissue barriers to arbovirus infection in mosquitoes. Viruses 7:3741–3767. https://doi.org/10.3390/v7072795
Garza-Hernandez JA, Rodriguez-Perez MA, Salazar MI, Russell TL, Adeleke MA, de Luna-Santillana EJ, Reyes-Villanueva F (2013) Vectorial capacity of Aedes aegypti for dengue virus type 2 is reduced with co-infection of Metarhizium anisopliae. PLoS Negl Trop Dis 7:e2013. https://doi.org/10.1371/journal.pntd.0002013
Grard G, Caron M, Mombo IM et al (2014) Zika virus in Gabon (Central Africa)–2007: a new threat from Aedes albopictus? PLoS Negl Trop Dis 8:e2681. https://doi.org/10.1371/journal.pntd.0002681
Guzzetta G, Poletti P, Montarsi F et al (2016) Assessing the potential risk of Zika virus epidemics in temperate areas with established Aedes albopictus populations. Euro Surveill. https://doi.org/10.2807/1560-7917.es.2016.21.15.30199
Hurd H (2001) Host fecundity reduction: a strategy for damage limitation? Trends Parasitol 17:363–368
Hurd H (2009) Evolutionary drivers of parasite-induced changes in insect life-history traits from theory to underlying mechanisms. Adv Parasitol 68:85–110. https://doi.org/10.1016/s0065-308x(08)00604-0
Jaronski ST (2010) Ecological factors in the inundative use of fungal entomopathogens. Biocontrol 55:159–185
Kamareddine L, Fan Y, Osta MA, Keyhani NO (2013) Expression of trypsin modulating oostatic factor (TMOF) in an entomopathogenic fungus increases its virulence towards Anopheles gambiae and reduces fecundity in the target mosquito. Parasit Vectors 6:22
Kauffman EB, Kramer LD (2017) Zika virus mosquito vectors: competence, biology, and vector control. J Infect Dis 216:S976–S990. https://doi.org/10.1093/infdis/jix405
Knols BG, Bukhari T, Farenhorst M (2010) Entomopathogenic fungi as the next-generation control agents against malaria mosquitoes. Future Microbiol 5:339–341. https://doi.org/10.2217/fmb.10.11
Lanciotti RS, Kosoy OL, Laven JJ et al (2008) Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg Infect Dis 14:1232–1239. https://doi.org/10.3201/eid1408.080287
Leta S, Beyene TJ, De Clercq EM, Amenu K, Revie C (2017) Global risk mapping for major diseases transmitted by Aedes aegypti and Aedes albopictus. Int J Infect Dis. https://doi.org/10.1016/j.ijid.2017.11.026
Li Y, Xu J, Zhong D et al (2018) Evidence for multiple-insecticide resistance in urban Aedes albopictus populations in southern China. Parasit Vectors 11:4. https://doi.org/10.1186/s13071-017-2581-y
Liu Y, Liu J, Du S et al (2017a) Evolutionary enhancement of Zika virus infectivity in Aedes aegypti mosquitoes. Nature 545:482–486. https://doi.org/10.1038/nature22365
Liu Z, Zhou T, Lai Z et al (2017b) Competence of Aedes aegypti, Ae. albopictus, and Culex quinquefasciatus Mosquitoes as Zika virus vectors, China. Emerg Infect Dis 23:1085–1091. https://doi.org/10.3201/eid2307.161528
Lord JC (2005) From Metchnikoff to Monsanto and beyond: the path of microbial control. J Invertebr Pathol 89:19–29. https://doi.org/10.1016/j.jip.2005.04.006
Moyes CL, Vontas J, Martins AJ et al (2017) Contemporary status of insecticide resistance in the major Aedes vectors of arboviruses infecting humans. PLoS Negl Trop Dis 11:e0005625. https://doi.org/10.1371/journal.pntd.0005625
Padilla-Guerrero IE, Barelli L, Gonzalez-Hernandez GA, Torres-Guzman JC, Bidochka MJ (2011) Flexible metabolism in Metarhizium anisopliae and Beauveria bassiana: role of the glyoxylate cycle during insect pathogenesis. Microbiology 157:199–208. https://doi.org/10.1099/mic.0.042697-0
Paixao ES, Barreto F, Teixeira Mda G, Costa Mda C, Rodrigues LC (2016) History, epidemiology, and clinical manifestations of Zika: a systematic review. Am J Public Health 106:606–612. https://doi.org/10.2105/ajph.2016.303112
Paula AR, Carolino AT, Silva CP, Pereira CR, Samuels RI (2013a) Testing fungus impregnated cloths for the control of adult Aedes aegypti under natural conditions. Parasit Vectors 6:256. https://doi.org/10.1186/1756-3305-6-256
Paula AR, Carolino AT, Silva CP, Samuels RI (2013b) Efficiency of fungus-impregnated black cloths combined with imidacloprid for the control of adult Aedes aegypti (Diptera: Culicidae). Lett Appl Microbiol 57:157–163
Pedrini N, Ortiz-Urquiza A, Huarte-Bonnet C, Zhang S, Keyhani NO (2013) Targeting of insect epicuticular lipids by the entomopathogenic fungus Beauveria bassiana: hydrocarbon oxidation within the context of a host-pathogen interaction. Front Microbiol 4:24. https://doi.org/10.3389/fmicb.2013.00024
Pla S, St Leger RJ, Wu LP (2007) Fungal peptide Destruxin A plays a specific role in suppressing the innate immune response in Drosophila melanogaster. J Biol Chem 282:8969
Rasmussen SA, Jamieson DJ, Honein MA, Petersen LR (2016) Zika virus and birth defects-reviewing the evidence for causality. N Engl J Med 374:1981–1987. https://doi.org/10.1056/nejmsr1604338
Rath A, Mohanty I, Hazra RK (2017) Insecticide susceptibility status of invasive Aedes albopictus across dengue endemic districts of Odisha. Pest Manag Sci, India. https://doi.org/10.1002/ps.4827
Scholte EJ, Knols BG, Samson RA, Takken W (2004) Entomopathogenic fungi for mosquito control: a review. J Insect Sci 4:19
Smith DL, Battle KE, Hay SI, Barker CM, Scott TW, McKenzie FE (2012) Ross, macdonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Pathog 8:e1002588. https://doi.org/10.1371/journal.ppat.1002588
Smith LB, Kasai S, Scott JG (2016) Pyrethroid resistance in Aedes aegypti and Aedes albopictus: important mosquito vectors of human diseases. Pestic Biochem Physiol 133:1–12. https://doi.org/10.1016/j.pestbp.2016.03.005
Tognarelli J, Ulloa S, Villagra E et al (2016) A report on the outbreak of Zika virus on Easter Island, South Pacific, 2014. Arch Virol 161:665–668. https://doi.org/10.1007/s00705-015-2695-5
Toopaang W, Phonghanpot S, Punya S et al (2017) Targeted disruption of the polyketide synthase gene pks15 affects virulence against insects and phagocytic survival in the fungus Beauveria bassiana. Fungal Biol 121:664–675. https://doi.org/10.1016/j.funbio.2017.04.007
Wang C, St Leger RJ (2007) A scorpion neurotoxin increases the potency of a fungal insecticide. Nat Biotechnol 25:1455–1456. https://doi.org/10.1038/nbt1357
Weaver SC, Costa F, Garcia-Blanco MA et al (2016) Zika virus: history emergence biology and prospects for control. Antivir Res 130:69–80. https://doi.org/10.1016/j.antiviral.2016.03.010
Wei G, Lai Y, Wang G, Chen H, Li F, Wang S (2017) Insect pathogenic fungus interacts with the gut microbiota to accelerate mosquito mortality. Proc Natl Acad Sci USA 114:5994–5999. https://doi.org/10.1073/pnas.1703546114
Zhang M, Zheng X, Wu Y et al (2010) Quantitative analysis of replication and tropisms of Dengue virus type 2 in Aedes albopictus. Am J Trop Med Hyg 83:700–707. https://doi.org/10.4269/ajtmh.2010.10-0193
Acknowledgements
We thank Dr. Changwen Ke for kindly providing Zika virus strain Z16006 to conduct this study. This research was supported by National Key R&D Program of China (2017YFD0500400), National Natural Science Foundation of China (81772217, 20180907, 81572012), Guangdong Provincial Natural Science Foundation Project (2016A030311025, 2017A030313694), Science and Technology Planning Project of Guangdong Province (2018A050506038) and Guangzhou health and medical collaborative innovation major special project (201604020011) to HJP.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
Our only experimental animal is Aedes albopictus, which does not involve animal ethical issues.
Additional information
Communicated by E. Quesada-Moraga.
Rights and permissions
About this article
Cite this article
Deng, S., Huang, Q., Wei, H. et al. Beauveria bassiana infection reduces the vectorial capacity of Aedes albopictus for the Zika virus. J Pest Sci 92, 781–789 (2019). https://doi.org/10.1007/s10340-019-01081-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-019-01081-0