Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Unveiling the oxidative metabolism of Rhipicephalus microplus (Acari: Ixodidae) experimentally exposed to entomopathogenic fungi

Abstract

Rhipicephalus microplus is an important tick in tropical regions due to the high economic losses caused by its parasitism. Metarhizium anisopliae and Beauveria bassiana are well-known entomopathogenic fungi that can afflict R. microplus ticks. The development of new targets and strategies to control this parasite can be driven by studies of this tick’s physiology. Recently, it was reported that when exposed to adverse physiological conditions, ticks can activate fermentative pathways, indicating transition from aerobic to anaerobic metabolism. Nevertheless, the precise mechanism by which entomopathogenic fungi influence R. microplus metabolism has not been clarified, limiting understanding of the tick-fungus association. Thus, the present study aimed to evaluate the effect of infection of ticks by M. anisopliae and B. bassiana on the amount of selected carboxylic acids present in the hemolymph, enabling increased understanding of changes previously reported. The results showed preservation in the concentrations of oxalic, lactic, and pyruvic acids in the hemolymph 24 and 48 h after dropping from cattle; while there were variations in the concentration of these carboxylic acids after infection of female ticks to M. anisopliae and B. bassiana. Significant increases were observed in the concentration of oxalic and lactic acids and significant reduction of pyruvic acid for both observation times (24 and 48 h) after infection by entomopathogenic fungi. These results indicate that B. bassiana and M. anisopliae infection alters the basal metabolism of R. microplus females, resulting in the activation of fermentative pathways.

This is a preview of subscription content, log in to check access.

Fig. 1

References

  1. Alves SB (1998) Controle Microbiano de Insetos, 2ªth edn. FEALQ, Piracicaba, p 1163

  2. Angelo IC, Fernandes EK, Bahiense TC, Perinotto WMS, Moraes APR, Terra ALM, Bittencourt VREP (2010a) Efficiency of Lecanicillium lecanii to control the tick Rhipicephalus microplus. Vet Parasitol 172:317–322

  3. Angelo IC, Fernandes EKK, Bahiense TC, Perinotto WMS, Gôlo PS, Moraes APR, Bittencourt VREP (2012) Virulence of Isaria sp. and Purpureocillium lilacinum to Rhipicephalus microplus tick under laboratory conditions. Parasitol Res 111:1473–1480

  4. Angelo IC, Golo PS, Camargo MG, Kluck GEG, Folly E, Bittencourt VREP (2010b) Haemolymph protein and lipid profile of Rhipicephalus (Boophilus) microplus infected by fungi. Transbound Emerg Dis 57:79–83

  5. Angelo IC, Tunholi-Alves VM, Tunholi VM, Perinotto WMS, Gôlo PS, Camargo MG, Quinelato S, Pinheiro J, Bittencourt VREP (2015) Physiological changes in Rhipicephalus microplus (Acari: Ixodidae) experimentally infected with entomopathogenic fungi. Parasitol Res 114:219–225

  6. Bezerra JCB, Becker W, Zelck EU (1997) A comparative study of the organic acid content of the hemolymph of Schistosoma mansoni-resistant and susceptible strains of Biomphalaria glabrata. Mem Inst Oswaldo Cruz 92:421–425

  7. Camargo MG, Marciano AF, Sá FA, Perinotto WMS, Quinelato S, Gôlo PS, Angelo IC, Prata MCA, Bittencourt VREP (2014) Commercial formulation of Metarhizium anisopliae for the control of Rhipicephalus microplus in a pen study. Vet Parasitol 205:271–276

  8. Camargo MG, Nogueira MRS, Marciano AF, Perinotto WMS, Coutinho-Rodrigues CJB, Scott FB, Angelo IC, Prata MCA, Bittencourt VREP (2016) Metarhzium anisopliae for controlling Rhipicephalus microplus ticks under field conditions. Vet Parasitol 223:38–42

  9. FAO (2004) Resistance management and integrated parasite control in ruminants. Guidelines. Animal Production and Health Division, FAO, pp 25–77pp

  10. Fernandes EKK, Bittencourt VREP (2008) Entomopathogenic fungi against South American tick species. Exp Appl Acarol 46:71–93

  11. Fernandes ÉKK, Bittencourt VREP, Roberts DW (2012) Perspectives on the potential of entomopathogenic fungi in biological control of ticks. Exp Parasitol 130:300–305

  12. Fraga A, Ribeiro L, Lobato M, Santos V, Silva JR, Gomes H, Moraes JLC, Menezes JS, Logullo CJ, Campos E, Fonseca RN (2013) Glycogen and glucose metabolism are essential for early embryonic development of the red flour beetle Tribolium castaneum. Plos one 8:e65125

  13. Grisi L, Leite RC, Martins JRS, Barros ATM, Andreotti R, Cançado PHD, León AAP, Pereira JB, Villela HS (2014) Reassessment of the potential economic impact of cattle parasites in Brazil. Braz J Vet Parasitol 23:150–156

  14. Luz C, Tigano MS, Silva IG, Cordeiro CMT, Aljanabi SM (1998) Selection of Beauveria bassiana and Metarhizium anisopliae isolates to control Triatoma infestans. Mem I Oswaldo Cruz 93:839–846

  15. Massa DR, Chejlava MJ, Fried B, Sherma J (2007) High performance column liquid chromatographic analysis of selected carboxylic acids in Biomphalaria glabrata patently infected with Schistosoma mansoni. Parasitol Res 101:925–928

  16. Moraes J, Campos E, Logullo C (2012) Metabolismo energético durante a embriogênese do carrapato bovino Rhipicephalus microplus. Tópicos avançados em Entomologia molecular. Instituto Nacional de Ciências e Tecnologia em Entomologia molecular.

  17. Moraes J, Galina A, Alvarenga PH, Rezende GL, Masuda A, Vaz IS, Logullo C (2007) Glucose metabolism during embryogenesis of the hard tick Boophilus microplus. Comp Biochem Physiol 146:528–533

  18. Ostfeld RS, Price A, Hornbostel VL, Benjamin MA, Keesing F (2006) Controlling ticks and tick-borne zoonoses with biological and chemical agents. Bioscience 56:383–394

  19. Perinotto WSM, Angelo IC, Golo PS, Quinelato S, Camargo MG, Sá FA, Bittencourt VREP (2012) Susceptibility of difference populations of ticks to entomopathogenic fungi. Exp Parasitol 130:257–260

  20. Rajput ZI, Hu S, Chen W, Arijo A, Xiao C (2006) Importance of ticks and their chemical and immunological control in livestock. J Zhejiang Univ Sci B 7:912–921

  21. Samson RA (1974) Paecilomyces and some allied hyphomycetes. Stud Mycol 6:1–119

  22. St Leger RJ, Nelson JO, Screen SE (1999) The entomopathogenic fungus Metarhizium anisopliae alters ambient pH, allowing extracellular protease production and activity. Microbiology 145:2691–2699

  23. Sun M, Ren Q, Guan G, Liu Z, Ma M, Gou H, Chen Z, Li Y, Liu A, Niu Q, Yang J, Yin H, Luo J (2011) Virulence of Beauveria bassiana, Metarhizium anisopliae and Paecilomyces lilacinus to the engorged female Hyalomma anatolicum anatolicum tick (Acari: Ixodidae). Vet Parasitol 180:389–393

  24. Tunholi VM, Tunholi-Alves VM, Lustrino D, Castro R, Sant’ana L, Garcia J, A M Jr, Rodrigues MLA, Pinheiro J (2013) Aerobic to anaerobic transition in Biomphalaria glabrata (Say, 1818) infected with different miracidial doses of Echinostoma paraensei (Lie and Basch, 1967) by high performance liquid chromatography. Exp Parasitol 133:403–410

  25. Tunholi-Alves VM, Tunholi VMA, Castro RN, Sant’ana L, Garcia J, Thiengo SC, Pinheiro J, A M Jr (2014) Activation of anaerobic metabolism in Biomphalaria glabrata (Mollusca: Gastropoda) experimentally infected by Angyostrongylus cantonensis (Nematoda, Metastrongylidae) by highperformance liquid chromatography. Parasitol Int 63:64–68

Download references

Acknowledgments

This study was supported in part by the Conselho Nacional para o Desenvolvimento Científico e Tecnológico (CNPq) and Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ).

Author information

Correspondence to Vinícius Menezes Tunholi-Alves.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tunholi-Alves, V.M., Tunholi Alves, V.M., da Silva, J.P. et al. Unveiling the oxidative metabolism of Rhipicephalus microplus (Acari: Ixodidae) experimentally exposed to entomopathogenic fungi. Parasitol Res 115, 3683–3688 (2016). https://doi.org/10.1007/s00436-016-5180-5

Download citation

Keywords

  • Metarhizium anisopliae
  • Beauveria bassiana
  • Lactic acids
  • Pyruvic acid
  • Oxalic acids