Environmental Science and Pollution Research

, Volume 24, Issue 31, pp 24714–24724 | Cite as

Evaluation of Beauveria bassiana infection in the hemolymph serum proteins of the housefly, Musca domestica L. (Diptera: Muscidae)

  • Sapna MishraEmail author
  • Peeyush Kumar
  • Anushree Malik
Short Research and Discussion Article


Beauveria bassiana plays a prominent role in biocontrol of houseflies, Musca domestica (L.). Thus, a deeper insight into immune response of M. domestica during B. bassiana infection was warranted to assist the production of more efficient mycoinsecticides. The present study investigates changes in protein profile of M. domestica hemolymph serum post B. bassiana infection using two-dimensional difference gel electrophoresis (2D-DIGE) followed by identification of selected proteins by matrix-assisted laser desorption/ionization-time of flight mass spectrometry (MALDI-TOF MS). The non-infected or control group of flies showed an expression of 54 proteins, while M. domestica infected with B. bassiana expressed a total of 68 hemolymph serum proteins. Thirty three proteins were expressed in both groups of houseflies, whereas 35 proteins were exclusively expressed in infected flies and 21 proteins were exclusively expressed in control flies. Among the 33 proteins which were expressed in both groups of houseflies, 17 proteins showed downregulation, while16 proteins were upregulated in the infected flies compared to the non-infected ones. The results from this study are expected to facilitate better understanding of insect’s immune response mechanism.


Musca domestica Entomopathogen Beauveria bassiana Hemolymph Immune response Protein expression 



This paper is dedicated to the memory of Late, Padma Bhusahn, Dr. V. P. Sharma, Founder Director of National Institute of Malaria Research (India) and Former Additional Director General, Indian Council of Medical Research, who inspired the authors constantly with valuable suggestions on insect pest/vector control. Financial support by Indian Council of Medical Research (IRIS_ID No. 2010-07860), India and CSIR Research Associateship (09/086 (1191)/2014-EMR-I) to one of the author (SM) is gratefully acknowledged. The authors also acknowledge Mr. Satendar Singh (IIT Delhi, India) for his help in experimental work.

Supplementary material

11356_2017_193_MOESM1_ESM.docx (354 kb)
ESM 1 (DOCX 353 kb)


  1. Dowsey AW, Morris JS, Gutstein HB, Yang GZ (2010) Informatics and statistics for analyzing 2-d gel electrophoresis images. Proteome Bioinform 604:239–255CrossRefGoogle Scholar
  2. El-Sadawy HA, El-Dobal SKA (2009) Changes in hemolymph serum proteins pattern of Hyalomma dromedarii ticks infected with entomopathogenic nematodes. Glob Vet 3:441–446Google Scholar
  3. Gul HT, Saeed S, Khan FZ (2014) Entomopathogenic fungi as effective insect pest management tactic: a review. Appl Sci Bus Econ 1(1):10–18Google Scholar
  4. Horvath CM (2000) STAT proteins and transcriptional responses to extracellular signals. Trends Biochem Sci 25(10):496–502CrossRefGoogle Scholar
  5. Levy F, Bulet P, Sabatier LE (2004) Proteomic analysis of the systemic immune response of Drosophila. Cell Mol Proteom 3:156–166CrossRefGoogle Scholar
  6. Liang Y, Wang J-X, Zhao X-F, Du X-J, Xue J-F (2006) Molecular cloning and characterization of cecropin from the housefly (Musca domestica), and its expression in Escherichia coli. Dev Comp Immunol 30:249–257CrossRefGoogle Scholar
  7. Liu N, Zhang L, Li M, Reid W (2012) Transcriptome of adult Musca domestica launches a platform for comparative housefly gene expression and characterization of differential gene expression among resistant and susceptible houseflies. Submitted to the EMBL/Gen Bank/DDBJ databasesGoogle Scholar
  8. Malik A, Singh N, Satya S (2007) Housefly (Musca domestica): a review of control strategies for a challenging pest. J Environ Sci Health Part B 42(4):453–469CrossRefGoogle Scholar
  9. McCaffrey R, St Johnston D, González-Reyes A (2006) Drosophila mus 301/spindle-C encodes a helicase with an essential role in double-strand DNA break repair and meiotic progression. Genetics 174(3):1273–1285CrossRefGoogle Scholar
  10. McDonald CE, Chen LL (1965) The lowry modification of the folin reagent for determination of proteinase activity. Anal Biochem 10(1):175–177CrossRefGoogle Scholar
  11. Meylaers K, Clynen E, Daloze D, DeLoof A, Schoofs L (2004) Identification of 1-lysophosphatidylethanolamine (C16, 1) as an antimicrobial compound in the housefly, Musca domestica. Insect Biochem Mol Biol 34:43–49CrossRefGoogle Scholar
  12. Mishra S, Malik A (2012) Nutritional optimization of a native Beauveria bassiana isolate (HQ917687) pathogenic to housefly, Musca domestica L. J Parasit Dis 37(2):199–207CrossRefGoogle Scholar
  13. Mishra S, Kumar P, Malik A, Satya S (2011) Adulticidal and larvicidal activity of Beauveria bassiana and Metarhizium anisopliae against housefly, Musca domestica (Diptera:Muscidae) in laboratory and simulated field bioassays. Parasitol Res 108:1483–1492CrossRefGoogle Scholar
  14. Mishra S, Kumar P, Malik A (2015) The effect of Beauveria bassiana infection on cell mediated and humoral immune response in house fly, Musca domestica L. Environ Sci Pollut Res 22:15171–15178CrossRefGoogle Scholar
  15. Mustelin T, Alonso A, Bottini N, Huynh H, Rahmouni S, Nika K, Louis-dit-Sully C, Tautz L, Togo SH, Bruckner S, Mena-Duran AV (2004) Protein tyrosine phosphatases in T cell physiology. Mol Immunol 41(6):687–700CrossRefGoogle Scholar
  16. Mustelin T, Vang T, Bottini N (2005) Protein tyrosine phosphatases and the immune response. Nature Rev Immunol 5(1):43–57CrossRefGoogle Scholar
  17. Reichhart JM, Gubb D, Leclerc V (2011) The Drosophila serpins: multiple functions in immunity and morphogenesis. Methods Enzymol 499:205–225CrossRefGoogle Scholar
  18. Reis M, Sousa-Guimarães S, Vieira CP, Sunkel CE, Vieira J (2011) Drosophila genes that affect meiosis duration are among the meiosis related genes that are more often found duplicated. PLoS One 6:1–16Google Scholar
  19. Ren Q, Zhao X, Wang J (2009) Molecular characterization and expression analysis of a chicken-type lysozyme gene from housefly (Musca domestica). J Genet Genomics 36:7–16CrossRefGoogle Scholar
  20. Riley CP, Gough ES, He J, Jandhyala SS, Kennedy B, Orcun S, Ouzzani M, Buck C, Roumani AM, Zhang X (2010) The proteome discovery pipeline-a data analysis pipeline for mass spectrometry-based differential proteomics discovery. Open Proteomics J 3:8–19Google Scholar
  21. Scott JG, Warren WC, Beukeboom LW, Bopp D, Clark AG, Giers SD, Hediger M, Jones AK, Kasai S, Leichter CA, Li M (2014) Genome of the house fly, Musca domestica L., a global vector of diseases with adaptations to a septic environment. Genome Biol 15(10):1–7CrossRefGoogle Scholar
  22. Shang Y, Feng P, Wang C (2015) Fungi that infect insects: altering host behavior and beyond. PLoS Pathog 11(8):1–6CrossRefGoogle Scholar
  23. Shono T, Scott JG (2003) Spinosad resistance in the house fly, Musca domestica, is due to a recessive factor on autosome 1. Pestic Biochem Physiol 75:1–7CrossRefGoogle Scholar
  24. Sopko R, Perrimon N (2013) Receptor tyrosine kinases in drosophila development. Cold Spring Harb Perspect Biol 5(6):a009050CrossRefGoogle Scholar
  25. Stojanovski D, Koutsopoulos OS, Okamoto K, Ryan MT (2004) Levels of human Fis 1 at the mitochondrial outer membrane regulate mitochondrial morphology. J Cell Sci 117:1201–1210CrossRefGoogle Scholar
  26. Strand MR (2008) The insect cellular immune response. Insect Sci 15:1–14CrossRefGoogle Scholar
  27. Tsakas S, Marmaras VJ (2010) Insect immunity and its signaling: an overview. Invertebr Surviv J 7:228–238Google Scholar
  28. Uchino R, Yu-ki N, Horigome T, Sugiyama S, Furukawa K (2013) Loss of Drosophila A-type lamin C initially causes tendon abnormality including disintegration of cytoskeleton and nuclear lamina in muscular defects. Dev Biol 373:216–227CrossRefGoogle Scholar
  29. Velapatiño B, Zlosnik JE, Hird TJ, Speert DP (2013) Total protein extraction and 2-d gel electrophoresis methods for Burkholderia species. J Vis Exp: JoVE 80:e50730Google Scholar
  30. Wang L, Kounatidis I, Ligoxygakis P (2014) Drosophila as a model to study the role of blood cells in inflammation, innate immunity and cancer. Front Cell Infect Microbiol 3:113CrossRefGoogle Scholar
  31. Weber AL, Khan GF, Magwire MM, Tabor CL, Mackay TF, Anholt RR (2012) Genome-wide association analysis of oxidative stress resistance in Drosophila melanogaster. PLoS One 7(4):e34745CrossRefGoogle Scholar
  32. Wiesner A, Rohloff L-H, Wittwer D, Pohl U, Sambeek VJ, Kurtz J, Gotz P (1998) Phagocytosis by insect hemocytes in vitro. In: Wiesner A, Dunphy GB, Marmaras VJ, Morishima I, Sugumara M, Yamakawa M (eds) Techniques in Insect Immunology. SOS Publications, Fair Haven, New York, pp 11–20Google Scholar
  33. Yakura H (1994) The role of protein tyrosine phosphatases in lymphocyte activation and differentiation. Crit Rev Immunol 14(3-4):311CrossRefGoogle Scholar
  34. Zhao P, Dong Z, Duan J, Wang G, Wang L, Li Y, Xiang Z, Xia Q (2012) Genome-wide identification and immune response analysis of serine protease inhibitor genes in the silkworm, Bombyx mori. PLoS One 7(2):e31168CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Applied Microbiology Laboratory, Centre for Rural Development and TechnologyIndian Institute of Technology DelhiNew DelhiIndia

Personalised recommendations