Environmental Science and Pollution Research

, Volume 22, Issue 19, pp 15171–15178 | Cite as

The effect of Beauveria bassiana infection on cell mediated and humoral immune response in house fly, Musca domestica L.

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


Entomopathogenic fungi that manifest infections by overcoming insect’s immune response could be a successful control agent for the house fly, Musca domestica L. which is a major domestic, medical, and veterinary pest. In this study, the immune response of house fly to Beauveria bassiana infection was investigated to reveal fundamental aspects of house fly hemocyte biology, such as hemocyte numbers and size, which is poorly understood. The total hemocyte counts (THCs) in B. bassiana-infected house fly showed an initial increase (from 6 to 9 h), followed by subsequent decrease (9 to 12 h) with increase in time of infection. The THCs was slightly greater in infected flies than the non-infected ones. Insight into relative hemocyte counts depicted a significant increase in prohemocyte (PR) and decrease in granulocyte (GR) in infected house flies compared to non-infected ones. The relative cell area of hemocyte cells showed a noticeable increase in PR and intermediate cells (ICs), while a considerable reduction was observed for plasmatocyte (PL) and GR. The considerable variation in relative cell number and cell area in the B. bassiana-infected house flies indicated stress development during infection. The present study highlights changes occurring during B. bassiana invasion to house fly leading to establishment of infection along with facilitation in understanding of basic hemocyte biology. The results of the study is expected to help in better understanding of house fly immune response during fungal infection, so as to assist production of more efficient mycoinsecticides for house fly control using B. bassiana.


Musca domestica Beauveria bassiana Cell-mediated immune response Hemocyte Pathogenesis 



This work was supported by Indian Council of Medical Research (IRIS_ID No. 201007860), India. CSIR fellowship to one of the authors (SM) is gratefully acknowledged. The authors also acknowledge Mr. Satendar Singh (IIT Delhi, India) for his help in experimental work.


  1. Abozenadah NYA (2010) Physiological studies on the house fly Musca domestica Vicina Muscidae, Diptera. JKAU: Sci 22(2):27-38. doi: 10.4197 / Sci. 22-2.3Google Scholar
  2. Baton LA, Robertson A, Warr E, Strand MR, Dimopoulos G (2009) Genome-wide transcriptomic profiling of Anopheles gambiae hemocytes reveals pathogen-specific signatures upon bacterial challenge and Plasmodium berghei infection. BMC Genomics 10(1):257. doi: 10.1186/1471-2164-10-257 CrossRefGoogle Scholar
  3. Bhikshapati E, Nagrajarao P, Rao KR, Shagalolu VV, Mushan LC (2012) Haemolytic activity of housefly larval extract in various seasons. Trends Life Sci 1(4):5–7, ISSN: 2319–4731Google Scholar
  4. Borowska J (2006) Effects of heavy metal on an organism—studies on cellular, individual and population levels in Musca domestica L. Doctoral Thesis. Jagiellonian University, KrakówGoogle Scholar
  5. Borowska J, Pyza E (2011) Effects of heavy metals on insects immunocompetent cells. J Insect Physiol 57(6):760–770. doi: 10.1016/j.jinsphys.2011.02.012 CrossRefGoogle Scholar
  6. Borowska J, Sulima B, Niklińska M, Pyza E (2004) Heavy metal accumulation and its effects on development, survival and immuno-competent cells of the house flyMusca domestica from closed laboratory populations as model organism. Fresenius Environ Bull 13(12):1402–1409, Google Scholar
  7. Bryant WB, Michel K (2014) Blood feeding induces hemocyte proliferation and activation in the African malaria mosquito, Anopheles gambiae Giles. J Exp Biol 217:1238–1245. doi: 10.1242/jeb.094573 CrossRefGoogle Scholar
  8. Casteels-Josson K, Zhang W, Capaci T, Casteels P, Tempst P (1994) Acute transcriptional response of the honeybee peptide-antibiotics gene repertoire and required post-translational conversion of the precursor structures. J Biol Chem 269(46):28569–28575, Google Scholar
  9. Castillo J, Brown MR, Strand MR (2011) Blood feeding and insulin-like peptide 3 stimulate proliferation of hemocytes in the mosquito Aedes aegypti. PLoS Pathog 7:e1002274. doi: 10.1371/journal.ppat.1002274 CrossRefGoogle Scholar
  10. Chifanzwa R (2011) House fly (Musca domestica L.) temporal and spatial immune response to Streptococcus pyogenes and Salmonella typhimurium: role of pathogen density in bacterial fate, persistence and transmission. Electronic Theses & Dissertations, Jack N. Averitt College of Graduate Studies (COGS) at Digital Commons@Georgia Southern. Paper 749 Scholar
  11. Choe KM, Werner T, Stoven S, Hultmark D, Anderson KV (2002) Requirement for a peptidoglycan recognition protein (PGRP) in Relish activation and antibacterial immune responses in Drosophila. Science 296:359–362. doi: 10.1126/science.1070216 CrossRefGoogle Scholar
  12. Christensen BM, Huff BM, Miranpuri GS, Harris KL, Christensen LA (1989) Hemocyte population changes during the immune response of Aedes aegypti to inoculated microfilariae of Dirofilaria immitis. J Parasitol 75:119–123, CrossRefGoogle Scholar
  13. Coggins SA, Estevez-Lao TY, Hillyer JF (2012) Increased survivorship following bacterial infection by the mosquito Aedes aegypti as compared to Anopheles gambiae correlates with increased transcriptional induction of antimicrobial peptides. Dev Comp Immunol 37:390–401. doi: 10.1016/j.dci.2012.01.005 CrossRefGoogle Scholar
  14. Da Silva JP, Alviano DS, Alviano CS, De Souza W, Travassos LR, Diniz JA, Rozental S (2002) Comparison of Fonsecaea pedrosoi sclerotic cells obtained in vivo and in vitro: ultrastructure and antigenicity. FEMS Immunol Med Microbiol 33(1):63–99. doi: 10.1111/j.1574-695X.2002.tb00574.x CrossRefGoogle Scholar
  15. Filipiak M, Bilska E, Tylko G, Pyza E (2010) Effects of zinc on programmed cell death of Musca domestica and Drosophila melanogaster blood cells. J Insect Physiol 56(4):383–390. doi: 10.1016/j.jinsphys.2009.11.010 CrossRefGoogle Scholar
  16. González-Chávez SA, Arévalo-Gallegos S, Rascón-Cruz Q (2009) Lactoferrin: structure, function and applications. Int J Antimicrob Agents 33(4):301.e1–301.e8. doi: 10.1016/j.ijantimicag.2008.07.020 CrossRefGoogle Scholar
  17. Hillyer JF, Schmidt SL, Christensen BM (2003) Hemocyte-mediated phagocytosis and melanization in the mosquito Armigeres subalbatus following immune challenge by bacteria. Cell Tissue Res 313:117–127. doi: 10.1007/s00441-003-0744-y CrossRefGoogle Scholar
  18. King JG, Hillyer JF (2013) Spatial and temporal in vivo analysis of circulating and sessile immune cells in mosquitoes: hemocyte mitosis following infection. BMC Biol 11:55. doi: 10.1186/1741-7007-11-55 CrossRefGoogle Scholar
  19. Kraaijeveld AR, Limentani EC, Godfray HC (2001) Basis of the trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Proc Biol Sci 268:259–261. doi: 10.1098/rspb.2000.1354 CrossRefGoogle Scholar
  20. Liang Y, Wang JX, Zhao XF, Du XJ, Xue JF (2006) Molecular cloning and characterization of cecropin from the housefly (Musca domestica), and its expression in Escherichia coli. Dev Comp Immunol 30(3):249–257. doi: 10.1016/j.dci.2005.04.005 CrossRefGoogle Scholar
  21. Malik A, Singh N, Satya S (2007) House fly (Musca domestica): a review of control strategies for a challenging pest. J Environ Sci Health B 42(4):453–469. doi: 10.1080/10934520601187658 CrossRefGoogle Scholar
  22. 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 34:43–49. doi: 10.1016/j.ibmb.2003.09.001 CrossRefGoogle Scholar
  23. Mishra S (2013) Development of fungal formulations for house fly control. Indian Institute of Technology, Delhi, Google Scholar
  24. Mishra S, Kumar P, Malik A, Satya S (2011) Comparative efficacy of Beauveria bassiana and Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) for the control of adult house fly, Musca domestica (Diptera: Muscidae). Parasitol Res 108(6):1483–1492. doi: 10.1007/s00436-010-2203-5 CrossRefGoogle Scholar
  25. Mishra S, Malik A (2013) Nutritional optimization of a native Beauveria bassiana isolate (HQ917687) pathogenic to house fly, Musca domestica L. J Parasit Dis 37(2):199–207. doi: 10.1007/s12639-012-0165-5 CrossRefGoogle Scholar
  26. Moret Y, Schmid-Hempel P (2000) Survival for immunity: the price of immune system activation for bumble-bee workers. Science 290(5494):1166–1168. doi: 10.1126/science.290.5494.1166 CrossRefGoogle Scholar
  27. Ren Q, Zhao XF, Wang JX (2009) Molecular characterization and expression analysis of a chicken-type lysozyme gene from housefly (Musca domestica). J Genet Genomics 36(1):7–16. doi: 10.1016/S1673-8527(09)60002-3 CrossRefGoogle Scholar
  28. Ribeiro SA, D’Ambrosio MV, Vale RD (2014) Induction of focal adhesions and motility in Drosophila S2 cells. Mol Biol Cell 25:3861–3869. doi: 10.1091/mbc.E14-04-0863 CrossRefGoogle Scholar
  29. Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C (2010) Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 329:1353–1355. doi: 10.1126/science.1190689 CrossRefGoogle Scholar
  30. Russo J, Brehelin M, Carton Y (2001) Haemocyte changes in resistant and susceptible strains of D. melanogaster caused by virulent and avirulent strains of the parasitic wasp Leptopilina boulardi. J Insect Physiol 47:167–172, PII: S0022-1910(00)00102-5 CrossRefGoogle Scholar
  31. Sims D, Duchek P, Baum B (2009) PDGF/VEGF signaling controls cell size in Drosophila. Genome Biol 10:R20. doi: 10.1186/gb-2009-10-2-r20 CrossRefGoogle Scholar
  32. Strand MR (2008) The insect cellular immune response. Insect Sci 15:1–14. doi: 10.1111/j.1744-7917.2008.00183.x CrossRefGoogle Scholar
  33. Sundaravadivelan C, Padmanabhan MN (2014) Effect of mycosynthesized silver nanoparticles from filtrate of Trichoderma harzianum against larvae and pupa of dengue vector Aedes aegypti L. Environ Sci Pollut Res 21(6):4624–4633. doi: 10.1007/s11356-013-2358-6 CrossRefGoogle Scholar
  34. Teramoto T, Tanaka T (2004) Mechanism of reduction in the number of the circulating hemocytes in the Pseudaletia separata host parasitized by Cotesia kariyai. J Insect Physiol 50:1103–1111. doi: 10.1016/j.jinsphys.2004.08.005 CrossRefGoogle Scholar
  35. Tsakas S, Marmaras VJ (2010) Insect Immunity and its signaling: an overview. Invertebr Surviv J 7:228–238, ISSN 1824-307XGoogle Scholar
  36. Turnbull MW, Martin SB, Webb BA (2004) Quantitative analysis of hemocyte morphological abnormalities associated with Campoletis sonorensis parasitization. J Insect Sci 4(1):11,
  37. Wang JX, Zhao XF, Liang YL, Li L, Zhang W, Ren Q, Wang LC, Wang LY (2006) Molecular characterization and expression of the antimicrobial peptide defensin from the housefly (Musca domestica). Cell Mol Life Sci 63:3072–3082. doi: 10.1007/s00018-006-6284-3 CrossRefGoogle Scholar
  38. Wiesner A, Rohloff L-H, Wittwer D, Pohl U, Van Sambeek J, 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, pp 11–20Google Scholar
  39. Yan R, Wan QH, Liu H, Liu L, Zhang X (2007) The morphological character of hemocytes in the Musca domestica larva of the 3th instar. Acta Academiae Medicinae Zunyi 01Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Applied Microbiology Lab, Centre for Rural Development and TechnologyIndian Institute of TechnologyNew DelhiIndia

Personalised recommendations