Symbiodinium Transcriptomes: Genome Insights into the Dinoflagellate Symbionts of Reef-Building Corals

Till Bayer,Manuel Aranda,Michael K Desalvo,Mónica Medina,Shinichi Sunagawa,Erika Lindquist,Mary Alice Coffroth,Christian R Voolstra,Lauren K Yum,Ahmed Moustafa

doi:10.1371/journal.pone.0035269

Abstract

Dinoflagellates are unicellular algae that are ubiquitously abundant in aquatic environments. Species of the genus Symbiodinium form symbiotic relationships with reef-building corals and other marine invertebrates. Despite their ecologic importance, little is known about the genetics of dinoflagellates in general and Symbiodinium in particular. Here, we used 454 sequencing to generate transcriptome data from two Symbiodinium species from different clades (clade A and clade B). With more than 56,000 assembled sequences per species, these data represent the largest transcriptomic resource for dinoflagellates to date. Our results corroborate previous observations that dinoflagellates possess the complete nucleosome machinery. We found a complete set of core histones as well as several H3 variants and H2A.Z in one species. Furthermore, transcriptome analysis points toward a low number of transcription factors in Symbiodinium spp. that also differ in the distribution of DNA-binding domains relative to other eukaryotes. In particular the cold shock domain was predominant among transcription factors. Additionally, we found a high number of antioxidative genes in comparison to non-symbiotic but evolutionary related organisms. These findings might be of relevance in the context of the role that Symbiodinium spp. play as coral symbionts.Our data represent the most comprehensive dinoflagellate EST data set to date. This study provides a comprehensive resource to further analyze the genetic makeup, metabolic capacities, and gene repertoire of Symbiodinium and dinoflagellates. Overall, our findings indicate that Symbiodinium possesses some unique characteristics, in particular the transcriptional regulation in Symbiodinium may differ from the currently known mechanisms of eukaryotic gene regulation.

Highlights

Dinoflagellates are ubiquitous marine and freshwater unicellular eukaryotes
In CassKB8 we identified a total of 106 genes encoding a Trx domain, which is substantially higher than what is found in the plants Arabidopsis thaliana and Physcomitrella patens (79 and 70), while 73 putative Trx genes were identified in Mf1.05b
And completeness The sequence data reported in this study comprises the largest transcriptome of dinoflagellates to date, and surpasses the available number of dinoflagellate sequences currently in public databases

Summary

Introduction

Dinoflagellates are ubiquitous marine and freshwater unicellular eukaryotes. As photosynthetic plankton, they are responsible for much of the primary production of oceans, rivers, and lakes. Dinoflagellates belong to the Alveolata, a large eukaryotic clade that comprises the ciliates, which are free-living, as well as the Apicomplexans, which all have parasitic lifestyles. Dinoflagellate genomic DNA has been shown to occur in a crystal-like state [8], with chromosomes condensed throughout the cell cycle [9]. Some of these observations initially led authors to conclude that dinoflagellates lacked histones [9]. Despite the high gene number, dinoflagellate genomes are assumed to consist mostly of non-coding DNA (98–99.9%) [13] Another unique feature characteristic of the dinoflagellate molecular machinery is the trans-splicing of spliced leader sequences [12,14]. SL transsplicing acts to convert polycistronic mRNAs to monocistronic mRNAs and has been suggested to regulate gene expression [15]

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Conclusion