Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-10T15:00:02.816Z Has data issue: false hasContentIssue false
  • English
  • Français

Bacterial feeding nematodes ingest haemocytes in the haemocoel of the insect Galleria mellonella

Published online by Cambridge University Press:  18 November 2019

Masaya Ono ,
Yoichi Hayakawa  and
Toyoshi Yoshiga Open the ORCID record for Toyoshi Yoshiga [Opens in a new window]
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
Yoichi Hayakawa
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
Get access Rights & Permissions [Opens in a new window]

Abstract

Insect parasitic nematodes have acquired mechanisms to evade their host immune response for successful parasitism. Despite the importance of understanding of the evolution of evasion mechanisms from host immunity, insect immune response against non-parasitic nematodes has not been well studied. In our previous study, we demonstrated that a non-insect parasitic nematode Caenorhabditis elegans was not encapsulated by haemocytes in the larvae of the greater wax moth Galleria mellonella. To understand how nematodes influence insect haemocytes to escape encapsulation, we examined the effect of C. elegans on haemocytes in the haemocoel of G. mellonella larvae. Injection of nematodes resulted in the decrease of haemocyte density while mortality and spreading ability of haemocytes, the haematopoietic organs were not affected. In vitro co-incubation of haemocytes with nematodes resulted in a decrease of haemocyte density and we observed feeding on haemocytes by nematodes. Injection of C. elegans feeding-delay mutants into insects did not cause the decrease of haemocyte density. The decrease of haemocyte density was due to the nematode's ingestion of haemocytes. Furthermore, an entomopathogenic nematode and other bacterial feeding nematodes also showed similar feeding behaviour. The nematode's ability to feed on haemocytes may have played an important role in the evolution of nematode parasitism in bacterial-feeding nematodes.

Keywords

Caenorhabditis eleganscellularencapsulationGalleria mellonellahaemocyteimmuneinsectnematode
Type
Research Article
Information
Parasitology , Volume 147 , Issue 3 , March 2020 , pp. 279 - 286
Check for updates
Copyright
Copyright © Cambridge University Press 2019

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

Alvandi, J, Karimi, J and Dunphy, GB (2014) Cellular reactions of the white grub larvae, Polyphylla adspersa, against entomopathogenic nematodes. Nematology 16, 1–12.CrossRefGoogle Scholar
Ayaad, TH, Dorrah, MA, Shaurub, SH and Sadawy, HA (2001) Effects of the entomopathogenic nematode, Heterorhabditis bacteriophora HP 88 and azadirachtin on the immune defence response and prophenoloxidase of Parasarcophaga surcoufi larvae (Diptera: Sarcophagidae). Journal of the Egyptian Society of Parasitology 31, 295–325.Google Scholar
Bird, DM, Jones, JT, Opperman, CH, Kikuchi, T and Danchin, EG (2014) Signatures of adaptation to plant parasitism in nematode genomes. Parasitology 142, S71–S84.CrossRefGoogle Scholar
Blaxter, M and Koutsovoulos, G (2014) The evolution of parasitism in Nematoda. Parasitology 142, S26–S39.CrossRefGoogle ScholarPubMed
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, 71–75.CrossRefGoogle ScholarPubMed
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, 149–156.CrossRefGoogle ScholarPubMed
Bulet, P and Stocklin, R (2005) Insect antimicrobial peptides: structures, properties and gene regulation. Protein and Peptide Letters 12, 3–11.CrossRefGoogle ScholarPubMed
Dowds, BCA and Peters, A (2002) Virulence mechanisms. In Gaugler, R (ed.), Entomopathogenic Nematology. New York, USA: CABI, pp. 79–98.CrossRefGoogle Scholar
Eleftherianos, I and Revenis, C (2011) Role and importance of phenoloxidase in insect hemostasis. Journal of Innate Immunity 3, 28–33.CrossRefGoogle ScholarPubMed
Félix, M-A and Braendle, C (2010) The natural history of Caenorhabditis elegans. Current Biology 20, R965–R969.CrossRefGoogle ScholarPubMed
Huang, F, Shi, M, Yang, YY, Li, JY and Chen, XX (2009) Changes in hemocytes of Plutella xylostella after parasitism by Diadegma semiclausum. Archives of Insect Biochemistry and Physiology 70, 177–187.CrossRefGoogle ScholarPubMed
Jiang, H, Vilcinskas, A and Kanost, MR (2010) Immunity in lepidopteran insects. Advances in Experimental Medicine and Biology 708, 181–204.CrossRefGoogle ScholarPubMed
Jiao, Z, Wen, G, Tao, S, Wang, J and Wang, G (2018) Induction of hemocyte apoptosis by Ovomermis sinensis: implications for host immune suppression. Journal of Invertebrate Pathology 159, 41–48.CrossRefGoogle ScholarPubMed
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, 845–851.Google Scholar
Kim, Y, Ji, D, Cho, S and Park, Y (2005) Two groups of entomopathogenic bacteria, Photorhabdus and Xenorhabdus, share an inhibitory action against phospholipase A2 to induce host immunodepression. Journal of Invertebrate Pathology 89, 258–264.CrossRefGoogle ScholarPubMed
Kim, H, Choi, D, Jung, J and Kim, Y (2018) Eicosanoid mediation of immune responses at early bacterial infection stage and its inhibition by Photorhabdus temperata subsp. temperata, an entomopathogenic bacterium. Archives of Insect Biochemistry and Physiology 99, e21502.CrossRefGoogle ScholarPubMed
Kiontke, K, Gavin, NP, Raynes, Y, Roehrig, C, Piano, F and Fitch, DH (2004) Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proceedings of the National Academy of Sciences of the United States of America 101, 9003–9008.CrossRefGoogle ScholarPubMed
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: Official Organ of the Indian Society for Parasitology 42, 204–211.CrossRefGoogle Scholar
Lavine, MD and Strand, MR (2001) Surface characteristics of foreign targets that elicit an encapsulation response by the moth Pseudoplusia includens. Journal of Insect Physiology 47, 965–974.CrossRefGoogle ScholarPubMed
Lavine, MD and Strand, MR (2002) Insect haemocyte and their role in immunity. Insect Biochemistry and Molecular Biology 32, 295–309.CrossRefGoogle Scholar
Li, X, Cowles, EA, Cowles, RS, Gaugler, R and Cox-Foster, DL (2009 a) Characterization of immunosuppressive surface coat proteins from Steinernema glaseri that selectively kill blood cells in susceptible hosts. Molecular and Biochemical Parasitology 165, 162–169.CrossRefGoogle ScholarPubMed
Li, Q, Sun, Y, Wang, G and Liu, X (2009 b) Effects of the mermithid nematode Ovomermis sinensis on the hemocytes of its host Helicoverpa armigera. Journal of Insect Physiology 55, 47–50.CrossRefGoogle ScholarPubMed
Manachini, B, Schillaci, D and Arizza, V (2013) Biological responses of Rhynchophorus ferrugineus (Coleoptera: Curculionidae) to Steinernema carpocapsae (Nematoda: Steinernematidae). Journal of Economic Entomology 106, 1582–1589.CrossRefGoogle Scholar
Ono, M and Yoshiga, T (2018) Cellular immunity in the insect Galleria mellonella against insect non-parasitic nematodes. Parasitology 146, 708–715.CrossRefGoogle Scholar
Pech, LL and Strand, MR (1996) Granular cells are required for encapsulation of foreign targets by insect haemocytes. Journal of Cell Science 109(Pt 8), 2053–2060.Google ScholarPubMed
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, 337–345.CrossRefGoogle Scholar
Sanghvi, GV, Baskaran, P, Röseler, W, Sieriebriennikov, B, Rödelsperger, C and Sommer, RJ (2016) Life history responses and gene expression profiles of the nematode Pristionchus pacificus cultured on Cryptococcus yeasts. PLoS One 11, e0164881. https://doi.org/10.1371/journal.pone.0164881.CrossRefGoogle ScholarPubMed
Shapiro-Ilan, D and Gaugler, R (2002) Production technology for entomopathogenic nematodes and their bacterial symbionts. Journal of Industrial Microbiology & Biotechnology 28, 137–146.CrossRefGoogle ScholarPubMed
Silveira, EB, Ribeiro, BM and Báo, SN (2003) Characterization of larval haemocytes from the velvetbean caterpillar Anticarsia gemmatalis (Hübner) (Lepidoptera: Noctuidae). Journal of Submicroscopic Cytology and Pathology 35, 129–139.Google Scholar
Stiernagle, T (1999) Maintenance of C. elegans. In Hope, I (ed.), C. elegans: A Practical Approach. Oxford, UK: Oxford University Press, pp. 51–67.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. 143–161.Google Scholar
Teramoto, T and Tanaka, T (2004) Mechanism of reduction in the number of the circulating hemocytes in the Pseudaletia separata host parasitized by Cotesia kariyai. Journal of Insect Physiology 50, 1103–1111.CrossRefGoogle ScholarPubMed
Tsuzuki, S, Matsumoto, H, Furihata, S, Ryuda, M, Tanaka, H, Sung, EJ, Bird, GS, Zhou, Y, Shears, SB and Hayakawa, Y (2014) Switching between humoral and cellular immune responses in Drosophila is guided by the cytokine GBP. Nature Communications 5, 4628.CrossRefGoogle ScholarPubMed
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, 161–174.CrossRefGoogle 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, 25–38.CrossRefGoogle 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, 597–608.CrossRefGoogle Scholar
Supplementary material: Image

Ono et al. supplementary material

Ono et al. supplementary material 1

Download Ono et al. supplementary material(Image)
Image 1.6 MB

Ono et al. supplementary material

Ono et al. supplementary material 2

Download Ono et al. supplementary material(Video)
Video 1.6 MB
Supplementary material: Image

Ono et al. supplementary material

Ono et al. supplementary material 3

Download Ono et al. supplementary material(Image)
Image 2.6 MB