Effect of host defenses on symbiont adaptations and genome erosion in a protective mutualism
Microbial Ecology and Applied Microbiology
Final Report Abstract
Many vertically transmitted insect symbionts experience degenerative genome evolution due to the repeated bottlenecks during transmission and the relaxed selective pressure on expendable genes in the stable host environment. While the outcome of this process is well-documented, the early stages and the factors triggering the process remain poorly understood. In this project, we studied the defensive symbiosis between solitary beewolf wasps and antibiotic-producing Streptomyces bacteria. Sequencing the genomes of 25 symbionts from different host species and comparing them to freeliving relatives revealed differential genome reduction and pseudogene accumulation across symbiont strains, with at least two independent origins of genome erosion. While most frameshift mutations occurred in accessory genes, some affected primary metabolic pathways, leading to vitamin and amino acid auxotrophies that were confirmed by in vitro bioassays in the P. triangulum symbiont. In contrast to the strong A+T bias observed in most other insect symbionts, we found a significant G+C enrichment in regions likely experiencing relaxed selection, demonstrating that the erosion of the large, linear, and G+C-rich Streptomyces genome follows a different trajectory than that of Gram-negative endosymbionts. During transmission of the symbionts from mother to offspring, they are exposed to a burst of nitric oxide (NO) produced by the developing beewolf egg. Using in vitro bioassays and RNAseq experiments, we demonstrate that the symbionts strongly upregulate protective enzymes upon NO exposure, but that they are nevertheless unable to survive NO concentrations that mimic those experienced under natural conditions, indicating that other protective mechanisms must exist. Interestingly, in vivo bioassays revealed that the beewolf’s antennal gland secretion (AGS) surrounding the bacterial symbionts in the brood cell effectively protects them from NO exposure, and follow-up experiments implicated the secretion’s long-chain hydrocarbons in NO protection. These experiments reveal a novel mechanism of how an insect protects its mutualistic symbionts from its own external immune defenses. Collectively, our findings illuminate novel host and symbiont adaptations for survival and successful vertical transmission, and they yield insights into the evolutionary history and the dynamics of genome erosion in antibiotic-producing Streptomyces symbionts.
Publications
- (2018) Convergent evolution in intracellular elements: plasmids as model endosymbionts. Trends in Microbiology 26 (9): 755-768
Dietel, A.-K., Kaltenpoth, M. & Kost C.
(See online at https://doi.org/10.1016/j.tim.2018.03.004) - (2018) Influence of microbial symbionts on insect pheromones. Natural Product Reports 35: 386-397
Engl, T. & Kaltenpoth, M.
(See online at https://doi.org/10.1039/c7np00068e) - (2018) Transmission of mutualistic bacteria in social and gregarious insects. Current Opinion in Insect Science 28: 50-58
Onchuru, T. O., Martinez, A.J., Ingham, C. S. & Kaltenpoth, M.
(See online at https://doi.org/10.1016/j.cois.2018.05.002) - (2019) Selective advantages favour high genomic AT-contents in intracellular elements. PLoS Genetics 15 (4): e1007778
Dietel, A.-K., Merker, H., Kaltenpoth, M. & Kost C.
(See online at https://doi.org/10.1371/journal.pgen.1007778) - (2020) Versatile and dynamic symbioses between insects and Burkholderia bacteria. Annual Review of Entomology 65: 145-170
Kaltenpoth, M. & Flórez, L.V.
(See online at https://doi.org/10.1146/annurev-ento-011019-025025) - (2021) Incipient genome erosion and metabolic streamlining for antibiotic production in a defensive symbiont. Proceedings of the National Academy of Sciences of the USA 118 (17): e2023047118
Nechitaylo, T.Y., Sandoval-Calderón, M., Engl, T., Wielsch, N., Dunn, D.M., Goesmann, A., Strohm, E., Svatoš, A., Dale, C., Weiss, R.B., Kaltenpoth, M.
(See online at https://doi.org/10.1073/pnas.2023047118)
