Investigation of host-symbiont-parasite interactions using the African cotton stainer insect (Dysdercus fasciatus)
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Abstract
Symbiotic associations are ubiquitous in nature and can extend along a dynamic continuum from mutualism to parasitism. In mutualism, the interacting organisms benefit from each other while in parasitism, one partner benefits and the other is harmed. Here, I studied mutualism and parasitism in the African cotton stainer insect (Dysdercus fasciatus) mid-gut using a combination of molecular, microbiological, and microscopic techniques as well as experimental manipulation. For millions of years, this insect has maintained a mutualistic relationship with its gut bacterial community that is dominated by Coriobacterium glomerans and Gordonibacter sp. (Actinobacteria), Hungatella sp. and Lactococcus lactis (Firmicutes), and Klebsiella sp. (Proteobacteria) bacterial symbionts that supplement the insect’s cotton seed diet with limiting B-vitamins. Additionally, their guts are often infested with Leptomonas pyrrhocoris, a generalized monoxenous trypanosomatid parasite, that co-localizes with the bacterial symbionts within the mid-gut. Because of their importance, the bacterial symbionts are transmitted to the offspring vertically (via egg surface smearing and probing) and horizontally (via coprophagic behavior). In this thesis, I investigated the risk associated with bacterial symbiont transmission, the role of gut bacterial symbionts in protecting the host against L. pyrrhocoris infections, and molecular interactions between the bacterial symbionts and the insect’s immunity. I revealed that transmission of the bacterial symbionts entails a significant risk of co-transmitting L. pyrrhocoris parasite that hitch-hikes on the symbiont transmission routes. Further, I showed that successful transmission of L. pyrrhocoris with the bacterial symbionts results in low parasite titre infections characterized by prolonged nymphal developmental times and a slight alteration of the gut microbiota composition. However, in the absence of the bacterial symbionts, the infections are characterized by significantly higher titers of this parasite which can invade the hemolymph resulting in an uncontrolled replication and ultimately the death of the host. Colonization of the insect’s peritrophic matrix along the gut wall by symbiotic bacteria likely acts as a barrier blocking parasite attachment, multiplication and entry into the peritrophic matrix and hemolymph. Importantly, I showed that the gut bacterial symbionts remain insensitive to the cotton stainer antimicrobial immune effectors once established in the mid-guts of second and third instar nymphs. This suggests that close associations of beneficial bacterial symbionts with their hosts can result in the evolution of mechanisms ensuring that symbionts remain resistant to host immunological responses, which may be important for the evolutionary stability of beneficial animal-microbe symbiotic associations.