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Chromosome-Scale Genomes, Resolving the Sister Phylum to Other Animals, and Novel Bioluminescent Systems.

Creative Commons 'BY-NC' version 4.0 license

Understanding how animals evolved from unicellular life requires comprehensive analyses that sample all animal phyla. However, some major outstanding questions in evolutionary biology, such as the evolutionary provenance of neurons, developmental pathways, and animal-specific genes, remain unanswered for one reason: it is unclear whether sponges (phylum Porifera) or ctenophores (phylum Ctenophora) as the sister phylum to all other animals. Here, we resolved this question using a chromosome-scale, whole-genome comparative approach. First, we generated chromosome-scale genomes of ctenophore species, and of three species that are unicellular, and outgroups to the Metazoa. By comparing these genomes to other chromosome-scale animal genomes, we identified groupings of genes that have persisted together on the same chromosomes since the common ancestor of the Filozoa, more than one billion years ago. We track the fate of these linked genes in the genomes of extant species, and find irreversible chromosomal fusions-with-mixing that preclude sponges from being the sister phylum to other animals. Thus, ctenophores must be the sister phylum to other animals.

As a parallel effort, we sought to use transcriptomics and genomics to study a trait that is common to many of the marine species that we studied above: bioluminescence. Light-emitting luciferase proteins are a useful tool for visualizing sub-cellular processes in microscopy, and are an interesting case of convergent evolution in over fifty clades. We used transcriptomics, full-length cDNA sequencing, and protein purification techniques to identify a novel luciferase in the polychaete worm Odontosylllis undecimdonta. This luciferase appears to be specific to the genus Odontosyllis, and there is no evidence for homologs in the transcriptomes of other polychaetes. In addition to the polychate luminescence, we also identified luminescence in a species of deep-sea sponge. This finding is significant, as reports of sponge luminescence in the past have been dubious. We used a biochemical approach to identify the luminous small molecule, coelenterazine, that is used in the bioluminescence reaction. A metagenomics sequencing approach revealed that the sponge sample contained little to no bacteria, and therefore the luminescence produced by the sponge was likely endogenous. Future efforts will focus on genome sequencing, and identifying the luciferase, to determine if the luciferase is truly encoded in the sponge genome.

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