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

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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.

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References

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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

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

    Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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.

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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).

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Authors and Affiliations

  1. Departamento de Ciências Fisiológicas, Instituto de Biologia, Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ, Brazil

    Vinícius Menezes Tunholi-Alves, Victor Menezes Tunholi Alves & Jairo Pinheiro da Silva

  2. Departamento de Química, Instituto de Ciências Exatas, Universidade Federal Rural do Rio de Janeiro, BR 465, Km 7, 23890-000, Seropédica, RJ, Brazil

    Rosane Nora Castro & Fernanda Barbosa Salgueiro

  3. Universidade Federal do Recôncavo da Bahia, Centro de Ciências Agrárias, Ambientais e Biológicas, Cruz das Almas, BA, Brazil

    Wendell Marcelo de Souza Perinotto

  4. Departamento de Parasitologia Animal, Instituto de Veterinária, Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ, Brazil

    Patrícia Silva Gôlo, Mariana Guedes Camargo & Vânia Rita Elias Pinheiro Bittencourt

  5. Departamento de Epidemiologia e Saúde Pública, Instituto de Veterinária, Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ, Brazil

    Isabele da Costa Angelo

Authors
  1. Vinícius Menezes Tunholi-Alves
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  2. Victor Menezes Tunholi Alves
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  3. Jairo Pinheiro da Silva
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  4. Rosane Nora Castro
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  5. Fernanda Barbosa Salgueiro
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  6. Wendell Marcelo de Souza Perinotto
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  7. Patrícia Silva Gôlo
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  8. Mariana Guedes Camargo
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  9. Isabele da Costa Angelo
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  10. Vânia Rita Elias Pinheiro Bittencourt
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Correspondence to Vinícius Menezes Tunholi-Alves.

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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

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  • DOI: https://doi.org/10.1007/s00436-016-5180-5

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