Hostname: page-component-5c6d5d7d68-ckgrl Total loading time: 0 Render date: 2024-08-24T14:48:14.008Z Has data issue: false hasContentIssue false

Cellular immunity in the insect Galleria mellonella against insect non-parasitic nematodes

Published online by Cambridge University Press:  20 December 2018

Masaya Ono
Affiliation:
Department of Applied Biological Sciences, Faculty of Agriculture, Saga University, Saga, Japan The United Graduate School of Agricultural Sciences, Kagoshima University, Kagoshima, Japan
Toyoshi Yoshiga*
Affiliation:
Department of Applied Biological Sciences, Faculty of Agriculture, Saga University, Saga, Japan The United Graduate School of Agricultural Sciences, Kagoshima University, Kagoshima, Japan
*
Author for correspondence: Toyoshi Yoshiga, E-mail: tyoshiga@cc.saga-u.ac.jp

Abstract

Immunity to microbial infections is well understood; however, information regarding the immunity to parasitic multicellular organisms remains lacking. To understand innate host cellular immunity to nematodes, we compared the cellular response of the greater wax moth (Galleria mellonella) larvae against the non-parasitic, bacterial-feeding nematode Caenorhabditis elegans and pathogenic nematode Heterorhabditis bacteriophora. When intact first-instar or dauer larvae of C. elegans were injected into a G. mellonella larva, most of the nematodes were alive and not confined by the surrounding reaction by insect haemocytes (encapsulation), similarly as the pathogenic nematode, whereas most of the heat-killed nematodes of both species were severely encapsulated by 24 h after inoculation. Other non-parasitic nematodes were also not encapsulated. Surprisingly, C. elegans injected into the insect haemocoel grew and propagated in the live insect, resulting in death of the host insect. Our results suggest that C. elegans has some basic mechanisms to evade immunity of G. mellonenlla and grow in the haemocoel.

Type
Research Article
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

Aliota, MT, Fuchs, JF, Mayhew, GF, Chen, CC and Christensen, BM (2007) Mosquito transcriptome changes and filarial worm resistance in Armigeres subalbatus. BMC Genomics 8, 463.Google Scholar
Aliota, MT, Fuchs, JF, Rocheleau, TA, Clark, AK, Hillyer, JF, Chen, CC and Christensen, BM (2010) Mosquito transcriptome profiles and filarial susceptibility in Armigeres subalbatus. PLoS Neglected Tropical Diseases 4, e666.Google Scholar
Balasubramanian, N, Hao, YJ, Toubarro, D, Nascimento, G and Simões, N (2009) Purification, biochemical and molecular analysis of a chymotrypsin protease with prophenoloxidase suppression activity from the entomopathogenic nematode Steinernema carpocapsae. International Journal for Parasitology 39, 975984.Google Scholar
Balasubramanian, N, Toubarro, D and Simões, N (2010) Biochemical study and in vitro insect immune suppression by a trypsin-like secreted protease from the nematode Steinernema carpocapsae. Parasite Immunology 32, 165175.Google Scholar
Bier, E and Guichard, A (2012) Deconstructing host-pathogen interactions in Drosophila. Disease Models & Mechanisms 5, 4861.Google Scholar
Bird, DM, Jones, JT, Opperman, CH, Kikuchi, T and Danchin, EGJ (2014) Signatures of adaptation to plant parasitism in nematode genomes. Parasitology 142(suppl), S71S84.Google Scholar
Blaxter, M and Koutsovoulos, G (2014) The evolution of parasitism in Nematoda. Parasitology 142(suppl), S26S39.Google Scholar
Blaxter, ML, De Ley, P, Garey, JR, Liu, LX, Scheldeman, P, Vierstraete, A, Vanfleteren, JR, Mackey, LY, Dorris, M, Frisse, LM, Vida, JT and Thomas, WK (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392, 7175.Google Scholar
Boemare, N (2002) Biology, taxonomy and systematics of Photorhabdus and Xenorhabdus. In Gaugler, R (ed.) Entomopathogenic Nematology. New York, USA: CABI, pp. 3556.Google Scholar
Bovien, P (1937) Some types of association between nematodes and insects. Videnskabelige Meddelelser fra Dansk Naturhistorik Forening 101, 1114.Google Scholar
Brivio, MF, Pagani, M and Restelli, S (2002) Immune suppression of Galleria mellonella (Insecta, Lepidoptera) humoral defenses induced by Steinernema feltiae (Nematoda, Rhabditida): involvement of the parasite cuticle. Experimental Parasitology 101, 149156.Google Scholar
Brivio, MF, Mastore, M and Moro, M (2004) Role of Steinernema feltiae body-surface lipids in host–parasite immunological interactions. Molecular and Biochemical Parasitology 135, 111121.Google Scholar
Brivio, MF, Toscano, A, De Pasquale, SM, De Lerma Barbaro, A, Giovannardi, S, Finzi, G and Mastore, M (2018) Surface protein components from entomopathogenic nematodes and their symbiotic bacteria: effects on immune responses of the greater wax moth, Galleria mellonella (Lepidoptera: Pyralidae). Pest Management Science 74, 20892099.Google Scholar
Bulet, P and Stocklin, R (2005) Insect antimicrobial peptides: structures, properties and gene regulation. Protein and Peptide Letters 12, 311.Google Scholar
Burman, M (1982) Neoaplectana carpocapsae: toxin production by axenic insect parasitic nematodes. Nematologica 28, 6270.Google Scholar
Castillo, JC, Reynolds, SE and Eleftherianos, I (2011) Insect immune responses to nematode parasites. Trends in Parasitology 27, 537547.Google Scholar
Castillo, JC, Creasy, T, Kumari, P, Shetty, A, Shokal, U, Tallon, LJ and Eleftherianos, I (2015) Drosophila anti-nematode and antibacterial immune regulators revealed by RNA-Seq. BMC Genomics 16, 519.Google Scholar
Cooper, D and Eleftherianos, I (2016) Parasitic nematode immunomodulatory strategies: recent advances and perspectives. Pathogens (Basel, Switzerland) 5, 58.Google Scholar
Dionne, M and Schneider, D (2008) Models of infectious diseases in the fruit fly Drosophila melanogaster. Disease Models & Mechanisms 1, 4349.Google Scholar
Dowds, BCA and Peters, A (2002) Virulence mechanisms. In Gaugler, R (ed.) Entomopathogenic Nematology. New York, USA: CABI, pp. 7998.Google Scholar
Ehlers, RU, Wulff, A and Peters, A (1997) Pathogenicity of axenic Steinernema feltiae, Xenorhabdus bovienii, and the bacto–helminthic complex to larvae of Tipula oleracea (Diptera) and Galleria mellonella (Lepidoptera). Journal of Invertebrate Pathology 69, 212217.Google Scholar
Eleftherianos, I and Revenis, C (2011) Role and importance of phenoloxidase in insect hemostasis. Journal of Innate Immunity 3, 2833.Google Scholar
Eleftherianos, I, Joyce, S, ffrench-Constant, RH, Clarke, DJ and Reynolds, SE (2010) Probing the tri-trophic interaction between insects, nematodes and Photorhabdus. Parasitology 137, 16951706.Google Scholar
Erickson, SM, Xi, Z, Mayhew, GF, Ramirez, JL, Aliota, MT, Christensen, BM and Dimopoulos, G (2009) Mosquito infection responses to developing filarial worms. PLoS Neglected Tropical Diseases 3, e529.Google Scholar
Forst, S and Clarke, D (2002) Bacteria-nematode symbiosis. In Gaugler, R (ed.) Entomopathogenic Nematology. New York, USA: CABI, pp. 5778.Google Scholar
Fuchi, M, Ono, M, Kondo, E and Yoshiga, T (2016) Pathogenicity of the axenic entomopathogenic nematode Steinernema carpocapsae against Galleria mellonella and Spodoptera litura larvae. Nematological Research 46, 3944.Google Scholar
Hallem, EA, Michelle, R, Todd, AC and Paul, WS (2007) Nematodes, bacteria, and flies: a tripartite model for nematode parasitism. Current Biology 17, 898904.Google Scholar
Han, R and Ehlers, RU (2000) Pathogenicity, development, and reproduction of Heterorhabditis bacteriophora and Steinernema carpocapsae under axenic in vivo conditions. Journal of Invertebrate Pathology 75, 5558.Google Scholar
Kariuki, MM, Hearne, LB and Beerntsen, BT (2010) Differential transcript expression between the microfilariae of the filarial nematodes, Brugia malayi and B. pahangi. BMC Genomics 11, 225.Google Scholar
Kikuta, S, Kiuchi, T, Aoki, F and Nagata, M (2008) Development of an entomopathogenic nematode, Steinernema carpocapsae, in cultured insect cells under axenic conditions. Nematology 10, 845851.Google Scholar
Kiontke, KC, Félix, MA, Ailion, M, Rockman, MV, Braendle, C, Pénigault, JB and Fitch, DH (2011) A phylogeny and molecular barcodes for Caenorhabditis, with numerous new species from rotting fruits. BMC Evolutionary Biology 11, 339.Google Scholar
Lalitha, K, Karthi, S, Vengateswari, G, Karthikraja, R, Perumal, P and Shivakumar, MS (2018) Effect of entomopathogenic nematode of Heterorhabditis indica infection on immune and antioxidant system in lepidopteran pest Spodoptera litura (Lepidoptera: Noctuidae). Journal of Parasitic Diseases 42, 204211.Google Scholar
Lavine, MD and Strand, MR (2002) Insect haemocyte and their role in immunity. Insect Biochemistry and Molecular Biology 32, 295309.Google Scholar
Lee, DL and Atkinson, HJ (1977) Physiology of Nematodes, 2nd Edn. New York, USA: Columbia University Press.Google Scholar
Li, XY, Cowles, RS, Cowles, EA, Gaugler, R and Cox-Foster, DL (2007) Relationship between the successful infection by entomopathogenic nematodes and the host immune response. International Journal for Parasitology 37, 365374.Google Scholar
Li, Q, Sun, Y, Wang, G and Liu, X (2009 a) Effects of the mermithid nematode Ovomermis sinensis on the hemocytes of its host Helicoverpa armigera. Journal of Insect Physiology 55, 4750.Google Scholar
Li, X, Cowles, EA, Cowles, RS, Gauglerd, R and Cox-Foster, DL (2009 b) Characterization of immunosuppressive surface coat proteins from Steinernema glaseri that selectively kill blood cells in susceptible hosts. Molecular and Biochemical Parasitology 165, 162169.Google Scholar
Lu, D, Macchietto, M, Chang, D, Barros, MM, Baldwin, J, Mortazavi, A and Dillman, AR (2017) Activated entomopathogenic nematode infective juveniles release lethal venom proteins. PLoS Pathogens 13, e1006302.Google Scholar
Mastore, M and Brivio, MF (2008) Cuticular surface lipids are responsible for disguise properties of an entomoparasite against host cellular responses. Developmental & Comparative Immunology 32, 10501062.Google Scholar
Mayhew, GF, Bartholomay, LC, Kou, HY, Rocheleau, TA, Fuchs, JF, Aliota, MT, Tsao, IY, Huang, CY, Liu, TT, Hsiao, KJ, Tsai, SF, Yang, UC, Perna, NT, Cho, WL, Christensen, BM and Chen, CC (2007) Construction and characterization of an expressed sequenced tag library for the mosquito vector Armigeres subalbatus. BMC Genomics 8, 462.Google Scholar
Nation, JL (2008) Insect Physiology and Biochemistry, 2nd Edn. Florida, USA: CRC Press.Google Scholar
Petersen, C, Hermann, RJ, Barg, MC, Schalkowski, R, Dirksen, P, Barbosa, C and Schulenburg, H (2015) Travelling at a slug's pace: possible invertebrate vectors Caenorhabditis nematodes. BMC Ecology 15, 19.Google Scholar
Poinar, GO (1979) Nematodes for Biological Control of Insects. Florida, USA: CRC Press.Google Scholar
Ramarao, N, Nielsen-Leroux, C and Lereclus, D (2012) The insect Galleria mellonella as a powerful infection model to investigate bacterial pathogenesis. Journal of Visualized Experiments 11, e4392.Google Scholar
Rämet, M (2012) The fruit fly Drosophila melanogaster unfolds the secrets of innate immunity. Acta Paediatrica 101, 900905.Google Scholar
Sanda, NB, Muhammad, A, Ali, H and Hou, Y (2018) Entomopathogenic nematode Steinernema carpocapsae surpasses the cellular immune responses of the hispid beetle, Octodonta nipae (Coleoptera: Chrysomelidae). Microbial Pathogenesis 124, 337345.Google Scholar
Shamseldean, MM, Platzer, EG and Gaugler, R (2007) Role of the surface coat of Romanomermis culicivorax in immune evasion. Nematology 9, 1724.Google Scholar
Stiernagle, T (1999) Maintenance of C. elegans. In Hope, I (ed.) C. elegans: A Practical Approach. Oxford, UK: Oxford University Press, pp. 5167.Google Scholar
Sudhaus, W (2008) Evolution of insect parasitism in rhabditid and diplogastrid nematodes. In Makarov, SE and Dimitrijevic, RN (eds), Advances in Arachnology and Developmental Biology. Belgrade, Serbia: Institute of Zoology, pp. 143161.Google Scholar
Sudhaus, W (2010) Preadaptive plateau in Rhabditida (Nematoda) allowed the repeated evolution of zooparasites, with an outlook on evolution of life cycles within Spiroascarida. Palaeodiversity 3(suppl), S117S130.Google Scholar
Tanada, Y and Kaya, HK (1993) Insect Pathology. California, USA: Academic Press.Google Scholar
Toubarro, D, Avila, MM, Montiel, R and Simoes, N (2013) A pathogenic nematode targets recognition proteins to avoid insect defenses. PLoS ONE 8, e75691.Google Scholar
Walter, TM, Dunphy, GB and Mandato, CA (2008) Steinernema carpocapsae DD136: Metabolites limit the non-self adhesion responses of haemocytes of two lepidopteran larvae, Galleria mellonella (Pyralidae) and Malacosoma disstria (Lasiocampidae). Experimental Parasitology 120, 161174.Google Scholar
Wang, P, Zhuo, XR, Tang, L, Liu, XS, Wang, YF, Wang, GX, Yu, XQ and Wang, JL (2017) C-type lectin interacting with β-integrin enhances hemocytic encapsulation in the cotton bollworm, Helicoverpa armigera. Insect Biochemistry and Molecular Biology 86, 2940.Google Scholar
Whitehead, AG and Hemming, JR (1965) A comparison of some quantitative methods of extracting small vermiform nematodes from soil. Annals of Applied Biology 55, 2538.Google Scholar
Yadav, S, Daugherty, S, Shetty, AC and Eleftherianos, I (2017) RNAseq analysis of the Drosophila response to the Entomopathogenic Nematode Steinernema. G3 7, 19551967.Google Scholar
Yi, YH, Wu, GQ, Lv, JL and Li, M (2016) Eicosanoids mediate Galleria mellonella immune response to hemocoel injection of entomopathogenic nematode cuticles. Parasitology Research 11, 597608.Google Scholar
Yoshiga, T and Umezaki, U (2016) A simple and small-scale hydroponic culture system to prepare second-stage juveniles of the root-knot nematode. Applied Entomology and Zoology 51, 151154.Google Scholar
Yu, XQ and Kanost, MR (2004) Immulectin-2, a pattern recognition receptor that stimulates hemocyte encapsulation and melanization in the tobacco hornworm, Manduca sexta. Developmental & Comparative Immunology 28, 891900.Google Scholar