Effect of host defenses on symbiont adaptations and genome erosion in a protective mutualism

• Applicant: Professor Dr. Martin Kaltenpoth
• Subject Area: Evolution, Anthropology ; Microbial Ecology and Applied Microbiology
• Term: from 2012 to 2021
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 225865913

During the evolution of mutualistic associations, the symbiotic partners often evolve increasingly intimate interdependence, resulting in relaxed selective pressures on dispensable genes under the stable conditions associated with the symbiotic lifestyle. Together with strong genetic drift due to population bottlenecks during transmission, this commonly results in the loss of genetic material and an increase in AT content, a process called genome erosion. While the results of this process are well-documented in insect symbionts, the early stages of genome erosion and the mechanistic factors accelerating it are still poorly understood. In the proposed project, we aim to reconstruct genome erosion in the defensive beewolf-Streptomyces mutualism in order to understand the causes and consequences of genomic decay in symbiotic microorganisms. Our key hypothesis is that exposure to host-produced nitric oxide (NO) inflicts a high mutational pressure on the symbiont genome and - particularly upon damage of the DNA repair machinery - plays a key role in genome erosion. In order to test this hypothesis and recapitulate genome erosion in the beewolf-Streptomyces symbiosis, we will (i) sequence and compare the genomes of 15 closely related symbiont strains in different stages of genomic decay to reconstruct the sequence of pseudogenization events and assess signatures of selection, (ii) investigate in vitro and in vivo the genomic and/or gene regulatory adaptations that allow the beewolf symbionts to cope with the extreme nitrosative stress, and (iii) use in vitro experiments and experimental evolution to test whether NO exposure and malfunctions of the DNA repair machinery play key roles in triggering or accelerating degenerative genome evolution. As nitric oxide is a widely occurring signaling and defense molecule in antagonistic and mutualistic associations, the results of the proposed project will not only shed light on the factors accelerating genome erosion, but will also enhance our general understanding of molecular host-microbe interactions governing symbiosis specificity and maintenance.

• DFG Programme: Research Grants