Spliceosome loss in the red tide ciliate Mesodinium rubrum presents a symbiotic cul-de-sac

Abstract

Mesodinium rubrum, a marine microbial eukaryote associated with some of the largest red tides on Earth, has the remarkable ability to commandeer the plastids, mitochondria and nuclei from the alga Teleaulax amphioxeia for photosynthesis. Here we report analyses of assemblies of M. rubrums two nuclear genomes. Unexpectedly, M. rubrum appears to have completely lost its spliceosomal introns, most spliceosomal molecules, and the key genes for an intron splicing-associated process, Nonsense-mediated mRNA Decay (NMD). In contrast, non-spliceosomal tRNA introns have been retained, as have thousands of intron analogs spliced out of DNA during ciliate somatic genome development (internal eliminated sequences - IESs). Intron-containing genes, especially from intron-rich species like T. amphioxeia, would likely be defunct if horizontally transferred to a host without a spliceosome like M. rubrum, and thus we propose that introns can be a roadblock to progressive endosymbiotic genomic integration.