2004 Annual Science Report
Marine Biological Laboratory Reporting | JUL 2003 – JUN 2004
Microbial Symbionts: Agents for Reorganizing Genome Architectures.
Bacterial endosymbionts, intracellular microbes that replicate within the domain of the host cell, have catalyzed the origin of the eukaryotic cell, the evolution of multicellular complexity, and diversification of numerous eukaryotic lineages. Mitochondria and chloroplasts, for example, result from endosymbiotic events of lasting significance that fundamentally changed cellular structure, species diversity, and the range of acceptable habitats of Life. Today, endosymbionts include several important human pathogens as well as diverse mutualistic lineages that are critical to the reproduction and success of their eukaryotic hosts. This project targets associations between bacteria and insects as model systems to study the drivers and consequences of genome remodeling.
During the reporting period, we made significant progress toward understanding the impact of long-term, stable genome interactions on molecular evolution and genome architecture. Our extensive molecular evolutionary analysis of Blochmannia and its ant hosts demonstrated strict host-symbiont cospeciation, and revealed extremely rapid evolutionary rates indicating unprecedented mutation rates in this ant mutualist (Degnan et al. 2004). As an extension of this work, we have also completed a phylogenetic analysis of endosymbiotic and free-living bacteria that explicitly accounts for their wide variation in GC content and shows independent origins of primary endosymbionts (Herbeck et al., submitted). We have published two population genetic studies showing exceptionally strong effects of mutational pressure and genetic drift in endosymbionts (Herbeck et al. 2003a; Wernegreen and Funk, in press). In addition, we published a genome-wide analysis of codon and amino acid usage in Wigglesworthia, the long-term obligate bacterial endosymbiont of the tsetse fly (Herbeck et al. 2003b). We used multivariate statistical analyses to test the hypothesis that mutational bias and genetic drift shape synonymous codon usage and amino acid usage in this severely reduced, 697-kb genome. Our results showed that codon and amino acid usage in Wigglesworthia reflect a strong AT mutational bias and elevated levels of genetic drift, consistent with expected effects of an endosymbiotic lifestyle and repeated population bottlenecks. However, these impacts of mutation and drift are apparently attenuated by selection on amino acid composition at functionally conserved, high-expression genes.
Our research on Wolbachia , a reproductive parasite, explores the evolution of a dynamic genome-genome interaction. We demonstrated significant genome size variability among parasitic Wolbachia strains (Bordenstein and Wernegreen, in prep). This result sets the stage for comparative genomic analyses to identify changes in gene content that trigger new host associations and symbiont phenotypes. We also documented recombination of an active bacteriophage in Wolbachia strains, and developed a novel hypothesis on the exchange of genetic information between intracellular microbial communities (Bordenstein and Wernegreen, in press). This research is part of the NAI/NRC Fellowship of Dr. Seth Bordenstein, and is described in more detail in his separate report.
PROJECT INVESTIGATORS:Jennifer Wernegreen
PROJECT MEMBERS:Seth Bordenstein
RELATED OBJECTIVES:Objective 4.2
Foundations of complex life
Environment-dependent, molecular evolution in microorganisms
Co-evolution of microbial communities
Adaptation and evolution of life beyond Earth