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2003 Annual Science Report

Marine Biological Laboratory Reporting  |  JUL 2002 – JUN 2003

Microbial Symbionts: Agents for Reorganizing Genome Architectures.

4 Institutions
3 Teams
0 Publications
0 Field Sites
Field Sites

Project Progress

The evolution of multicellular complexity required close interactions among a myriad of microbial symbionts, ranging from transient associations within populations to genome integration of endosymbionts and organelles. Today, bacterial endosymbionts allow numerous animal, plant, and protist lineages to occupy niches that are otherwise inhospitable. Stable associations between bacteria and insects provide model systems to study host-symbiont coevolution and the specialization of bacterial genomes to long-term intracellular associations. We integrate molecular evolution, population genetics, and comparative genomics to decipher the evolutionary forces operating in three such symbiotic systems: Blochmannia of ants, Wigglesworthia of tsetse flies, and Buchnera of aphids. Our lab also hosts Seth R. Bordenstein, an NAI/NRC Postdoctoral Fellow whose project is described in a separate progress report.

During the reporting period, we made significant progress toward identifying the effects of mutational pressure and genetic drift on protein evolution in obligate endosymbionts. We obtained a broad phylogenetic sample of protein-coding loci from Blochmannia, Buchnera, and their free-living relative E. coli, totaling more than 450 kb across isolates. Our sample of Blochmannia provided the first protein-coding genes of this ant endosymbiont (~7.34 kb for each of 16 taxa associated with diverse Camponotus host species). Using maximum likelihood and Bayesian methods of phylogenetic inference, we demonstrated congruence of host and symbiont phylogenies that indicates strict host-symbiont cospeciation throughout tens of millions of years (Degnan et al. 2003). Similarly, congruence among bacterial loci implies severe constraints on lateral gene transfer in obligate endosymbionts. This genome stasis may limit the evolutionary potential of these intracellular bacteria and accelerate the accumulation of deleterious changes through genetic drift.

Population genetic analyses provided insights into the specific forces that shape deoxyribonucleic acid (DNA) sequence evolution, and further supported effects of mutational pressure and drift. We identified signatures of genetic drift at groEL, a highly expressed chaperonin that is considered critical in the bacterial-aphid symbiosis (Herbeck et al., submitted). Thus, even these functionally important endosymbiont genes are not immune from genome degradation. Our population genetic analysis of synonymous base changes in Buchnera also provided the first robust estimates of their AT mutational bias (Wernegreen and Funk, submitted). We found that a remarkable 90% of the mutational changes within Buchnera species were GC->AT.

Genome analyses included a comparison of gene contents of Buchnera and Wigglesworthia, which we linked to the distinct nutritional physiologies of their insect hosts (Wernegreen 2003). As an expansion of a previous study in Buchnera, we explored codon and amino acid usage in the fully sequenced genome of Wigglesworthia (Herbeck et al., in press). This bacterium has a similar lifestyle as Buchnera, but is phylogenetically distinct and thus provides an independent “natural experiment” to identify forces shaping endosymbiont genome evolution. Our correspondence analysis demonstrated a strong impact of AT mutational bias on amino acid usage across this small (698 kb) genome, yet a reduced impact of AT pressure at high expression genes. This pattern parallels that observed in Buchnera and might provide a computational tool to identify candidate high expression genes in uncultivable bacteria that are difficult to study experimentally.

    Jennifer Wernegreen Jennifer Wernegreen
    Seth Bordenstein

    Joshua Herbeck

    Patrick Degnan
    Research Staff

    Adam Lazarus
    Research Staff

    Objective 4.2
    Foundations of complex life

    Objective 5.1
    Environment-dependent, molecular evolution in microorganisms

    Objective 5.2
    Co-evolution of microbial communities

    Objective 6.2
    Adaptation and evolution of life beyond Earth