The bacterial symbionts of mealybugs (Pseudococcidae)

Symbioses between insects and bacteria are widespread in nature. Bacterial symbionts may provide nutrition for their insect hosts and thereby help to occupy specialized niches. They may also provide defence against parasites, or manipulate host reproduction regulating population size and composition. Bacterial symbionts of insects are thus considered an important driving force in the evolution of their hosts. In this project, we will investigate the bacterial symbionts of mealybugs (Pseudococcidae). This group of insects has only been poorly studied with respect to their symbionts - despite a unique feature which makes this symbiosis different from all other known symbioses: The two phylogenetically different bacterial symbionts of mealybugs are not located in the same or neighbouring bacteriocytes, but one symbiont (`Candidatus Tremblaya princeps`) contains the other symbiont, which lives directly within its cytoplasm - the only reported case of endobacterial symbiosis so far. By genome sequencing, comparative genomics, and transcriptomics using next generation sequencing technology we will investigate the roles of both symbionts for their insect host and for each other. We will predict metabolic interdependencies between each symbiosis partner and establish interaction model. By comparing different mealybug species and their symbionts, we will be able to elucidate the evolutionary history of this unique symbiotic association. The proposed project will lead to a better understanding of the biology and ecology of a group of mealybugs which occurs as a major pest all over the world. It also addresses several fundamental questions such as the establishment and evolution of endobacterial symbiosis, which has implications for our understanding of early evolutionary processes leading to the first eukaryotic cell.

Symbiosis between insects and bacteria is widespread in nature. Bacterial symbionts provide nutrition for their insect hosts and thereby help to occupy specialized niches. They may also provide defense against parasites, or manipulate host reproduction affecting population size and composition. Bacterial symbionts of insects are thus considered an important driving force in the evolution of their hosts. In this project, we have investigated two groups of plant sap sucking insects, which include major pests but have been poorly studied with respect to their symbionts so far. Mealybugs (Pseudococcidae) are unique among insect hosts as many of them contain two different bacterial symbionts, where one symbiont resides within the cells of the other. In our study we could show that all three members of this symbiotic association act together to produce essential nutrients (amino acids) lacking in the hosts diet. Biosynthesis of these compounds requires the action of enzymes from the insect host as well as from both nested bacterial symbionts. Remarkably, this tightly connected metabolic network has developed multiple times independently among the mealybugs with partly unrelated bacterial partners. Other insects such as aphids contain only a single well conserved bacterial symbiont, which has been associated with this insect groups for more than 250 Million years and co-diversified with its host. We investigated the closest relatives of aphids and were able to show that the evolutionary history of the association of adelgids (Adelgidae) with bacterial symbionts is fundamentally different. Adelgids contain a number of different bacterial symbionts, where always two symbionts co-reside in a single species of this insect group. Phylogenetic analysis demonstrated that the evolution of this symbiosis originated from multiple symbiont acquisition and replacement events. Our first detailed analysis of a representative adelgid species showed that evolutionarily relatively young symbionts occur in extant adelgids. They both serve in nutrition of their insect host, show shared metabolic pathways with some redundancy, and both seem to be obligate for their host. Together, this project contributed to a better understanding of the intricate association between plant sap feeding insects and their bacterial symbionts. Our work addresses fundamental questions in microbiology and evolutionary biology but also has implications for pest management.