Genome Reduction and Evolution in an Obligate Luminous Symbiont.

Abstract

The luminous bacteria symbiotic with anomalopid flashlight fish are unusual compared to other luminous symbionts; they cannot be cultured outside the host and are thought to be obligately dependent on their hosts. The aims of this dissertation are to test if anomalopid symbionts are obligately dependent on hosts for growth and to compare the evolutionary history of anomalopid symbionts to symbionts with varying lifestyles. To do this, I present the sequenced genomes of two species of anomalopid symbionts, which I show to have specific interactions with different host species. I find that anomalopid symbionts are obligately dependent on their hosts and that this interaction has had a large affect on their evolution. While anomalopid symbionts are closely related to facultative luminous symbionts, they have multiple characteristics in common with obligate intracellular symbionts. Anomalopid symbionts have reduced genomes due to gene loss. Gene loss has lead to their inability to synthesize most amino acids and to utilize carbon/energy sources besides glucose. The observation of these metabolic deficiencies supports the obligate dependence of anomalopid symbionts on their hosts. I also find patterns consistent with anomalopid symbionts experiencing high levels of genetic drift. For instance, anomalopid symbionts are evolving at a faster rate than free-living relatives. Additionally, anomalopid symbionts are genetically monomorphic, even across a wide geographic range, and have an excess of rare substitutions. Furthermore, one symbiont species displays a high number of nonsynonymous substitutions. These indications of high genetic drift are consistent with the symbionts undergoing population bottlenecks during transfers between host generations. I also find that the two symbiont species are very similar in gene content but highly divergent at both the nucleotide and amino acid level. This finding is comparable to trends seen in obligate intracellular symbionts. The genomic patterns common to obligate intracellular symbionts are caused by their being intracellular and vertically transmitted, thus it is surprising that the extracellular, environmentally acquired symbionts of flashlight fish would also show so many of these trends. That these commonalities exist between symbionts with different ecologies highlights the importance of host interactions in determining the evolutionary history of symbionts.