Infection by the castrating parasitic nematode Sphaerularia bombi changes gene expression in Bombus terrestris bumblebee queens

• Published in: Insect molecular biology 2020-04, Vol.29 (2), p.170-182
• Main Authors: Colgan, T. J., Carolan, J. C., Sumner, S., Blaxter, M. L., Brown, M. J. F.
• Format: Article
• Language: English
• Subjects: Animals; Bees - genetics; Bees - immunology; Bees - parasitology; Biological activity; Biological effects; Bombus terrestris; Bumblebees; Castration; Circadian rhythms; Diapause; Diapause, Insect; Energy consumption; Energy usage; extended phenotype; Female; Gene expression; Gene Expression Profiling; Gene Expression Regulation - immunology; Gene sequencing; Genes; Genome, Insect - immunology; Genomes; Host-Parasite Interactions; Immune response; Immune system; Infections; insect immunity; Insect Proteins - immunology; molecular parasitism; Molecular structure; Nematodes; Overwintering; Parasites; Parasitism; Phenotypes; pollinator health; Queens; Ribonucleic acid; RNA; RNA-Seq; Seasons; Signal transduction; Sphaerularia; Transcription; Tylenchida - physiology
• ISSN: 0962-1075; 1365-2583
• DOI: 10.1111/imb.12618

Parasitism can result in dramatic changes in host phenotype, which are themselves underpinned by genes and their expression. Understanding how hosts respond at the molecular level to parasites can therefore reveal the molecular architecture of an altered host phenotype. The entomoparasitic nematode Sphaerularia bombi is a parasite of bumblebee (Bombus) hosts where it induces complex behavioural changes and host castration. To examine this interaction at the molecular level, we performed genome‐wide transcriptional profiling using RNA‐Sequencing (RNA‐Seq) of S. bombi‐infected Bombus terrestris queens at two critical time‐points: during and just after overwintering diapause. We found that infection by S. bombi affects the transcription of genes underlying host biological processes associated with energy usage, translation, and circadian rhythm. We also found that the parasite affects the expression of immune genes, including members of the Toll signalling pathway providing evidence for a novel interaction between the parasite and the host immune response. Taken together, our results identify host biological processes and genes affected by an entomoparasitic nematode providing the first steps towards a molecular understanding of this ecologically important host–parasite interaction. Infection by the nematode Sphaerularia bombi alters gene expression in bumblebee Bombus terrestris queens during and just after host diapause. Infection results in differential expression of genes involved in mitochondrial function, translation, and circadian rhythm. Host immune expression was altered postdiapause providing the first evidence of a molecular interaction between the parasite and the host immune system.