Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-22T18:54:54.542Z Has data issue: false hasContentIssue false
  • English
  • Français

Alteration of the phagocytosis and antimicrobial defense of Octodonta nipae (Coleoptera: Chrysomelidae) pupae to Escherichia coli following parasitism by Tetrastichus brontispae (Hymenoptera: Eulophidae)

Published online by Cambridge University Press:  05 December 2018

E. Meng ,
J. Li ,
B. Tang ,
Y. Hu ,
T. Qiao ,
Y. Hou ,
Y. Lin ,
J. Li  and
Z. Chen
E. Meng
Affiliation:
State Key Laboratory of Ecological Pest Control of Fujian-Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, China Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China
J. Li
Affiliation:
State Key Laboratory of Ecological Pest Control of Fujian-Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, China Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China
B. Tang
Affiliation:
State Key Laboratory of Ecological Pest Control of Fujian-Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, China Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China
Y. Hu
Affiliation:
State Key Laboratory of Ecological Pest Control of Fujian-Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, China Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China
T. Qiao
Affiliation:
State Key Laboratory of Ecological Pest Control of Fujian-Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, China Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China
Y. Hou*
Affiliation:
State Key Laboratory of Ecological Pest Control of Fujian-Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, China Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China
Y. Lin
Affiliation:
State Key Laboratory of Ecological Pest Control of Fujian-Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, China Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China
J. Li
Affiliation:
State Key Laboratory of Ecological Pest Control of Fujian-Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, China Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China
Z. Chen
Affiliation:
Fuzhou Entry-Exit Inspection & Quarantine Bureau of P.R.C, Fuzhou 350002, China
*
*Author for correspondence Phone: 86 591 8376 8654 Fax: 86 591 8378 9365 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Although parasites and microbial pathogens are both detrimental to insects, little information is currently available on the mechanism involved in how parasitized hosts balance their immune responses to defend against microbial infections. We addressed this in the present study by comparing the immune response between unparasitized and parasitized pupae of the chrysomelid beetle, Octodonta nipae (Maulik), to Escherichia coli invasion. In an in vivo survival assay, a markedly reduced number of E. coli colony-forming units per microliter was detected in parasitized pupae at 12 and 24 h post-parasitism, together with decreased phagocytosis and enhanced bactericidal activity at 12 h post-parasitism. The effects that parasitism had on the mRNA expression level of selected antimicrobial peptides (AMPs) of O. nipae pupae showed that nearly all transcripts of AMPs examined were highly upregulated during the early and late parasitism stages except defensin 2B, whose mRNA expression level was downregulated at 24 h post-parasitism. Further elucidation on the main maternal fluids responsible for alteration of the primary immune response against E. coli showed that ovarian fluid increased phagocytosis at 48 h post-injection. These results indicated that the enhanced degradation of E. coli in parasitized pupae resulted mainly from the elevated bactericidal activity without observing the increased transcripts of target AMPs. This study contributes to a better understanding of the mechanisms involved in the immune responses of a parasitized host to bacterial infections.

Keywords

bactericidaldegradationendoparasitoidmaternal fluidsmicrobial infection
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 109 , Issue 2 , April 2019 , pp. 248 - 256
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akira, S. (2009) Innate immunity to pathogens diversity in receptors for microbial recognition. Immunological Reviews 227, 5–8.Google Scholar
Aung, K.M., Boldbaatar, D., Umemiya-Shirafuji, R., Liao, M., Tsuji, N., Xuenan, X., Suzuki, H., Kume, A., Galay, R.L., Tanaka, T. & Fujisaki, K. (2012) HlSRB, a class B scavenger receptor, is key to the granulocyte-mediated microbial phagocytosis in ticks. PLoS ONE 7, e33504.Google Scholar
Bang, K., Park, S., Yoo, J.Y. & Cho, S. (2012) Characterization and expression of attacin, an antibacterial protein-encoding gene, from the beet armyworm, Spodoptera exigua, (Hübner) (insecta: lepidoptera: noctuidae). Molecular Biology Reports 39, 5151–5159.Google Scholar
Bell, A. (2011) Antimalarial peptides-the long and the short of it. Current Pharmaceutical Design 17, 2719–2731.Google Scholar
Bicker, H., Höflich, C., Vogt, K.W., Volk, H.-D. & Katrin, R.S. (2008) A simple assay to measure phagocytosis of live bacteria. Clinical Chemistry 54, 911–915.Google Scholar
Chernysh, S., Gordya, N. & Suborova, T. (2015) Insect antimicrobial peptide complexes prevent resistance development in bacteria. PLoS ONE 10, e0130788.Google Scholar
Cotter, S.C., Kruuk, L.E.B. & Wilson, K. (2004) Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. Journal of Evolutionary Biology 17, 421–429.Google Scholar
Dani, M.P., Richards, E.H., Isaac, R.E. & Edwards, J.P. (2003) Antibacterial and proteolytic activity in venom from the endoparasitic wasp Pimpla hypochondriaca (Hymenoptera: Ichneumonidae). Journal of Insect Physiology 49, 945–954.Google Scholar
Dubovskiy, I.M., Krukova, N.A. & Glupov, V.V. (2008) Phagocytic activity and encapsulation rate of Galleria mellonella larval haemocytes during bacterial infection by Bacillus thuringiensis. Journal of Invertebrate Pathology 98, 360–362.Google Scholar
Er, A., Uçkan, F., Rivers, D.B. & Sak, O. (2011) Cytotoxic effects of parasitism and application of venom from the endoparasitoid Pimpla turionellae on hemocytes of the host Galleria mellonella. Journal of Applied Entomology 135, 225–236.Google Scholar
Fang, Q., Wang, F., Gatehouse, J.A., Gatehouse, A.M.R., Chen, X.-X., Hu, C. & Ye, G.-Y. (2011 a) Venom of parasitoid, Pteromalus puparum, suppresses host, Pieris rapae, immune promotion by decreasing host C-type lectin gene expression. PLoS ONE 6, e26888.Google Scholar
Fang, Q., Wang, L., Zhu, Y., Stanley, D.W., Chen, X., Hu, C. & Ye, G. (2011 b) Pteromalus puparum venom impairs host cellular immune responses by decreasing expression of its scavenger receptor gene. Insect Biochemistry and Molecular Biology 41, 852–862.Google Scholar
Fieck, A., Hurwitz, I., Kang, A. & Durvasula, R. (2010) Trypanosoma cruzi: synergistic cytotoxicity of multiple amphipathic anti-microbial peptides to T. cruzi and potential bacterial hosts. Experimental Parasitology 125, 342–347.Google Scholar
Giglio, A., Battistella, S., Talarico, F.F., Brandmayr, T.Z. & Giulianini, P.G. (2008) Circulating hemocytes from larvae and adults of Carabus (chaetocarabus) lefebvrei dejean 1826 (Coleoptera, Carabidae): cell types and their role in phagocytosis after in vivo artificial non-self-challenge. Micron 39, 552–558.Google Scholar
Gillespie, J.P. & Kanost, M.R. (1997) Biological mediators of insect immunity. Annual Review of Entomology 42, 611–643.Google Scholar
Giulianini, P.G., Bertolo, F., Battistella, S. & Amirante, G.A. (2003) Ultrastructure of the hemocytes of Cetonischema aeruginosa larvae (Coleoptera, Scarabaeidae): involvement of both granulocytes and oenocytoids in in vivo phagocytosis. Tissue and Cell 35, 243–251.Google Scholar
Glupov, V.V. & Kryukova, N.A. (2016) Physiological and biochemical aspects of interactions between insect parasitoids and their hosts. Entomological Review 96, 513–524.Google Scholar
Han, L.-B., Huang, L.-Q. & WANG, C.-Z. (2013) Host preference and suitability in the endoparasitoid Campoletis chlorideae is associated with its ability to suppress host immune responses. Ecological Entomology 38, 173–182.Google Scholar
Haine, E.R., Moret, Y., Siva-Jothy, M.T. & Rolff, J. (2008 a) Antimicrobial defense and persistent infection in insects. Science 322, 1257–1259.Google Scholar
Haine, E.R., Pollitt, L.C., Moret, Y., Siva-Jothy, M.T. & Rolff, J. (2008 b) Temporal patterns in immune responses to a range of microbial insults (Tenebrio molitor). Journal of Insect Physiology 54, 1090–1097.Google Scholar
Hou, Y.M. & Weng, Z.Q. (2010) Temperature-dependent development and life table parameters of Octodonta nipae (Coleoptera: Chrysomelidae). Environmental Entomology 39, 1676–1684.Google Scholar
Hou, Y.M., Wu, Z.J. & Wang, C.F. (2011) The status and harm of invasive insects in Fujian, China. pp. 111–114 in Xie, L.H., You, M.S. & Hou, Y.M. (Eds) Biological Invasions: Problems and Countermeasures. Beijing, Science Press.Google Scholar
Hou, Y.M., Miao, Y.X. & Zhang, Z.Y. (2014 a) Leaf consumption capacity and damage projection of Octodonta nipae (Coleoptera: Chrysomelidae) on three palm species. Annals of the Entomological Society of America 107, 1010–1017.Google Scholar
Hou, Y.M., Miao, Y.X. & Zhang, Z.Y. (2014 b) Study on life parameters of the invasive species Octodonta nipae (Coleoptera: Chrysomelidae) on different palm species, under laboratory conditions. Journal of Economic Entomology 107, 1486–1495.Google Scholar
Huang, F., Yang, Y.Y., Shi, M., Li, J.Y., Chen, Z.Q., Chen, F.S. & Chen, X.X. (2010) Ultrastructural and functional characterization of circulating hemocytes from Plutella xylostella larva: cell types and their role in phagocytosis. Tissue and Cell 42, 360–364.Google Scholar
Huang, F., Shi, M., Chen, X. & Zhang, J. (2011) Effect of parasitism by Diadegma semiclausum (Hymenoptera: Ichneumonidae) and its venom on the phagocytic ability of hemocytes from Plutella xylostella (Lepidoptera: Plutellidae) larvae. Acta Entomologica Sinica 54, 989–996.Google Scholar
Hultmark, D., Engström, A., Andersson, K., Steiner, H., Bennich, H. & Boman, H.G. (1983) Insect immunity. Attacins, a family of antibacterial proteins from Hyalophora cecropia. EMBO Journal 2, 571–576.Google Scholar
Ishihara, T., Maruyama, Y. & Furukawa, S. (2017) Gene expression and molecular characterization of a novel C-type lectin, encapsulation promoting lectin (EPL), in the rice armyworm, Mythimna separata. Insect Biochemistry and Molecular Biology 89, 51–57.Google Scholar
Jan, S.L. & Shieh, G. (2013) Sample size determinations for Welch's test in one-way heteroscedastic ANOVA. British Journal of Mathematical and Statistical Psychology 67, 72–93.Google Scholar
Kacsoh, B.Z. & Schlenke, T.A. (2012) High hemocyte load is associated with increased resistance against parasitoids in Drosophila suzukii, a relative of D. melanogaster. PLoS ONE 7, e34721.Google Scholar
Laughton, A.M., Garcia, J.R., Altincicek, B., Strand, M.R. & Gerardo, N.M. (2011) Characterisation of immune responses in the pea aphid, Acyrthosiphon pisum. Journal of Insect Physiology 57, 830–839.Google Scholar
Lavine, M.D., Chen, G. & Strand, M.R. (2005) Immune challenge differentially affects transcript abundance of three antimicrobial peptides in hemocytes from the moth Pseudoplusia includens. Insect Biochemistry and Molecular Biology 35, 1335–1346.Google Scholar
Lesser, K.J., Paiusi, I.C. & Leips, J. (2006) Naturally occurring genetic variation in the age-specific immune response of Drosophila melanogaster. Aging Cell 5, 293–295.Google Scholar
Li, L.F., Xu, Z.W., Liu, N.Y., Wu, G.X., Ren, X.M. & Zhu, J.Y. (2018) Parasitism and venom of ectoparasitoid Scleroderma guani impairs host cellular immunity. Archives of Insect Biochemistry and Physiology 98, e21451.Google Scholar
Ling, E.J. & Yu, X.Q. (2006) Hemocytes from the tobacco hornworm Manduca sexta have distinct functions in phagocytosis of foreign particles and self dead cells. Developmental and Comparative Immunology 30, 301–309.Google Scholar
Mabiala-Moundoungou, A.D.N., Doury, G., Eslin, P., Cherqui, A. & Prévost, G. (2010) Deadly venom of Asobara japonica parasitoid needs ovarian antidote to regulate host physiology. Journal of Insect Physiology 56, 35–41.Google Scholar
Madanagopal, N. & Kim, Y. (2006) Parasitism by Cotesia glomerata induces immunosuppression of Pieris rapae: effects of ovarian protein and polydnavirus. Journal of Asia-Pacific Entomology 9, 339–346.Google Scholar
Mahmoud, A.M.A., De Luna-Santillana, E.J. & Rodríguez-Perez, M.A. (2012) Parasitism by the endoparasitoid wasp Cotesia flavipes induces cellular immunosuppression and enhances the susceptibility. Journal of Insect Science 11, 19.Google Scholar
Makarova, O., Rodriguez-Rojas, A., Eravci, M., Weise, C., Dobson, A., Johnston, P. & Rolff, J. (2016) Antimicrobial defence and persistent infection in insects revisited. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 371, 1257–1259.Google Scholar
McGwire, B., Olson, C., Tack, B. & Engman, D. (2003) Killing of African trypanosomes by antimicrobial peptides. Journal of Infectious Disease 188, 146–152.Google Scholar
Meng, E., Tang, B., Hou, Y., Chen, X., Chen, J. & Yu, X. (2016) Altered immune function of Octodonta nipae (Maulik) to its pupal endoparasitoid, Tetrastichus brontispae Ferrière. Comparative Biochemistry and Physiology, Part B Biochemistry and Molecular Biology 198, 100–109.Google Scholar
Moreau, S.J.M. (2013) ‘It stings a bit but it cleans well’: venoms of Hymenoptera and their antimicrobial potential. Journal of Insect Physiology 59, 186–204.Google Scholar
Moret, Y. & Schmid-Hempel, P. (2001) Immune defence in bumble-bee offspring. Nature 414, 506.Google Scholar
Nalini, M., Ibrahim, A.M.A., Hwang, I. & Kim, Y. (2009) Altered actin polymerization of Plutella xylostella (L.) in response to ovarian calyx components of an endoparasitoid Cotesia plutellae (Kurdjumov). Physiological Entomology 34, 110–118.Google Scholar
Namba, O., Nakamatsu, Y., Miura, K. & Tanaka, T. (2008) Autographa nigrisigna looper (Lepidoptera: Noctuidae) excludes parasitoid egg using cuticular encystment induced by parasitoid ovarian fluid. Applied Entomology and Zoology 43, 359–367.Google Scholar
Nazario-Toole, A. & Wu, L. (2017) Phagocytosis in insect immunity. Advances in Insect Physiology 52, 35–82.Google Scholar
Perron, G.G., Zasloff, M. & Bell, G. (2006) Experimental evolution of resistance to an antimicrobial peptide. Proceedings Biological Sciences 273, 251–256.Google Scholar
Pfaffl, W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45.Google Scholar
Richards, E.H. & Parkinson, N.M. (2000) Venom from the endoparasitic wasp Pimpla hypochondriaca adversely affects the morphology, viability, and immune function of hemocytes from larvae of the tomato moth, Lacanobia oleracea. Journal of Invertebrate Pathology 76, 33–42.Google Scholar
Rohloff, L., Wiesner, A. & Götz, P. (1994) A fluorescence assay demonstrating stimulation of phagocytosis by haemolymph molecules of Gallerta mellonella. Journal of Insect Physiology 40, 1045–1049.Google Scholar
Rosales, C. (2017). Cellular and molecular mechanisms of insect immunity. pp. 179–212 in Vonnie, S. (Ed.) Insect Physiology and Ecology. London, InTech.Google Scholar
Seufi, A.M., Hafez, E.E. & Galal, F.H. (2011) Identification, phylogenetic analysis and expression profile of an anionic insect defensin gene, with antibacterial activity, from bacterial-challenged cotton leafworm, Spodoptera littoralis. BMC Molecular Biology 12, 47.Google Scholar
Shen, X., Ye, G., Cheng, X., Yu, C., Yao, H. & Hu, C. (2010) Novel antimicrobial peptides identified from an endoparasitic wasp cDNA library. Journal of Peptide Science 16, 58–64.Google Scholar
Shi, Z.H. & Sun, J.H. (2010) Immunocompetence of the red turpentine beetle, Dendroctonus valens LeConte (Coleoptera: Curculionidae, Scolytinae): variation between developmental stages and sexes in populations in China. Journal of Insect Physiology 56, 1696–1701.Google Scholar
Shiratsuchi, A., Nitta, M., Kuroda, A., Komiyama, C., Gawasawa, M., Shimamoto, N., Tuan, T.Q., Morita, T., Aiba, H. & Nakanishi, Y. (2016) Inhibition of phagocytic killing of Escherichia coli in Drosophila hemocytes by RNA Chaperone Hfq. Journal of Immunology 197, 1298–1307.Google Scholar
Smilanich, A.M., Dyer, L.A. & Gentry, G.L. (2009) The insect immune response and other putative defenses as effective predictors of parasitism. Ecology 90, 1434–1440.Google Scholar
Stoehr, A.M. (2007) Inter- and intra-sexual variation in immune defence in the cabbage white butterfly, Pieris rapae L. (Lepidoptera: Pieridae). Ecological Entomology 32, 188–193.Google Scholar
Strand, M.R. (2008) The insect cellular immune response. Insect Science 15, 1–14.Google Scholar
Strand, M.R. & Pech, L.L. (1995) Immunological basis for compatibility in parasitoid-host relationships. Annual Review of Entomology 40, 31–56.Google Scholar
Strand, M.R., Beck, M.H., Lavine, M.D. & Clark, K.D. (2006) Microplitis demolitor bracovirus inhibits phagocytosis by hemocytes from Pseudoplusia includens. Archives of Insect Biochemistry and Physiology 61, 134–145.Google Scholar
Tang, B.Z. & Hou, Y.M. (2017) Nipa palm hispid beetle Octodonta nipae (Maulik). pp. 257–266 in Wan, F.H., Jiang, M.X. & Zhan, A.B. (Eds) Biological Invasions and Its Management in China, Volume 11 of the Series Invading Nature – Springer Series in Invasion Ecology. The Netherlands, Springer.Google Scholar
Tang, B.Z., Xu, L. & Hou, Y.M. (2014 a) Effects of rearing conditions on the parasitism of Tetrastichus brontispae on its pupal host Octodonta nipae. Biocontrol 59, 647–657.Google Scholar
Tang, B.Z., Chen, J., Hou, Y.M. & Meng, E. (2014 b) Transcriptome immune analysis of the invasive beetle Octodonta nipae (Maulik) (Coleoptera: Chrysomelidae) parasitized by Tetrastichus brontispae Ferrière (Hymenoptera: Eulophidae). PLoS ONE 9, 1–12.Google Scholar
Teng, Z., Xu, G., Gan, S., Chen, X., Fang, Q. & Ye, G.Y. (2016) Effects of the endoparasitoid Cotesia chilonis (Hymenoptera: Braconidae) parasitism, venom, and calyx fluid on cellular and humoral immunity of its host Chilo suppressalis (Lepidoptera: Crambidae) larvae. Journal of Insect Physiology 85, 46–56.Google Scholar
Tsuzuki, S., Matsumoto, H., Furihata, S., Ryuda, M., Tanaka, H., Sung, E.J., Bird, G.S., Zhou, Y., Shears, S.B. & Hayakawa, Y. (2014) Switching between humoral and cellular and humoral responses in Drosophila is guided by the cytokine CBP. Nature Communications 5, 1–11.Google Scholar
Vogelweith, F., Korner, M., Foitzik, S. & Meunier, J. (2017) Age, pathogen exposure, but not maternal care shape offspring immunity in an insect with facultative family life. BMC Evolutionary Biology 17, 69.Google Scholar
Wan, F.H., Hou, Y.M. & Jiang, M.X. (2015) Invasion Biology. Beijing, China, Science Press, pp. 240–244.Google Scholar
Xi, B., Zhang, Z.Y., Hou, Y.M. & Shi, Z.H. (2013) Effects of host plants on the developmental duration, feeding and reproduction of the nipa palm hispid, Octodonta nipae (Coleoptera: Chrysomelidae). Acta Entomologica Sinica 56, 799–806.Google Scholar
Xu, L., Lan, J.L., Hou, Y.M., Chen, Y.S., Chen, Z.X. & Weng, Z.Q. (2011) Molecular identification and pathogenicity assay on Metarhizium against Octodonta nipae (Coleoptera: Chrysomelidae). Chinese Journal of Applied Entomology 48, 922–927.Google Scholar
Ye, J., Zhao, H., Wang, H., Bian, J. & Zheng, R. (2010) A defensin antimicrobial peptide from the venoms of Nasonia vitripennis. Toxicon 56, 101–106.Google Scholar
Yi, H., Chowdhury, M., Huang, Y. & Yu, X. (2014) Insect antimicrobial peptides and their applications. Applied Microbiology Biotechnology 98, 5807–5822.Google Scholar
Zhang, Q., Huang, J., Zhu, J. & Ye, G. (2012) Parasitism of Pieris rapae (Lepidoptera: Pieridae) by the endoparasitic wasp Pteromalus puparum (Hymenoptera: Pteromalidae): effects of parasitism on differential hemocyte counts, micro- and ultra-structures of host hemocytes. Insect Science 19, 485–497.Google Scholar
Zhong, K., Liu, Z., Wang, J. & Liu, X. (2017) The entomopathogenic fungus Nomuraea rileyi impairs cellular immunity of its host Helicoverpa armigera. Archives of Insect Biochemistry and Physiology 96, e21402.Google Scholar
Supplementary material: File

Meng et al. supplementary material

Meng et al. supplementary material 1

Download Meng et al. supplementary material(File)
File 51.5 KB