Characterisation of Deladenus siricidicola genes potentially involved in parasitism and host immunomodulation

Abstract

Nematodes often associate with insects. Usually, it is the nematode that benefits from this interaction as the insect serves either as vector – for many plant- and vertebrate-parasitic nematodes (VPN) – or as the target host in the case of insect-parasitic or entomopathogenic nematodes (EPN). Parasitic nematodes are frequently responsible for chronic, debilitating diseases in millions of people, as well as crop losses, damage to plantations, and loss of livestock. By contrast, EPN used in the biological control of insect pests provide beneficial alternatives to costly and potentially hazardous chemical pesticides. The Steinernematidae and Heterorhabditidae coevolved with symbiotic bacteria and are the EPN families most widely used and well-studied as biocontrol agents of a variety of insect pests. These nematodes have evolved different strategies with which to overcome the robust immune response of the host. Although not as well studied, the nematode Deladenus siricidicola is of particular interest to pine growers, especially in the Southern Hemisphere, where it is the main biocontrol agent of the invasive woodwasp Sirex noctilio. In this study, I apply the available knowledge of immunomodulation in Steinernema spp. and Heterorhabditis spp. to better understand the interaction between D. siricidicola and the immune response of S. noctilio.

Chapter 1 reviews the current knowledge on the immune interactions between parasitic nematodes and their insect hosts. The review provides an overview of the insect immune response, especially in response to nematode invasion. Nematode biology related to host infection and the strategies aimed at overcoming the host immune response is discussed with reference to two well-known nematode-insect interactions. The first interaction is that of the biocontrol EPN of the genera Steinernema and Heterorhabditis, followed by the plant-parasitic pinewood nematode (PWN) Bursaphelenchus xylophilus and its beetle vector Monochamus alternatus. The relevance of and possible approaches for dissecting this interaction between the pine woodwasp, S. noctilio, and its biocontrol nematode, D. siricidicola, is proposed.

In Chapter 2, I identify and characterise genes and gene families in the genome of D. siricidicola which are potentially involved in parasitism and immunomodulation during the infection of S. noctilio. Sequence similarity searches with known virulence genes in Steinernema and other nematodes are performed against the genome of D. siricidicola using local BLAST, protein clustering, and hidden Markov model (HMM) searches. The identified genes are characterised functionally by comparison with functional databases. The expression of the genes are analysed with transcriptome data from both free-living nematodes and an early infection of S. noctilio larvae by D. siricidicola.

The third chapter of this dissertation considers the relevance of studying the interactions between nematodes and insects for human disease. Research on parasitic nematodes and their vertebrate hosts is challenging and costly. However, simpler organisms can be used as models to study complex biological and pathological processes. Although insects lack the sophisticated adaptive immune responses of mammals and rely only on an innate immune system, I argue that the similarities between the interactions of nematodes, insects, and bacteria in EPN and VPN systems, provide opportunities to explore additional and alternative treatment options for challenging human conditions. This chapter is structured as published in the journal Pathogens and Global Health in November 2021.