Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle

Abstract

Despite half a century of research, the biology of dinoflagellates remains enigmatic: they defy many functional and genetic traits attributed to typical eukaryotic cells. Genomic approaches to study dinoflagellates are often stymied due to their large, multi-gigabase genomes. Members of the genus Symbiodinium are photosynthetic endosymbionts of stony corals that provide the foundation of coral reef ecosystems. Their smaller genome sizes provide an opportunity to interrogate evolution and functionality of dinoflagellate genomes and endosymbiosis. We sequenced the genome of the ancestral Symbiodinium microadriaticum and compared it to the genomes of the more derived Symbiodinium minutum and Symbiodinium kawagutii and eukaryote model systems as well as transcriptomes from other dinoflagellates. Comparative analyses of genome and transcriptome protein sets show that all dinoflagellates, not only Symbiodinium, possess significantly more transmembrane transporters involved in the exchange of amino acids, lipids, and glycerol than other eukaryotes. Importantly, we find that only Symbiodinium harbor an extensive transporter repertoire associated with the provisioning of carbon and nitrogen. Analyses of these transporters show species-specific expansions, which provides a genomic basis to explain differential compatibilities to an array of hosts and environments, and highlights the putative importance of gene duplications as an evolutionary mechanism in dinoflagellates and Symbiodinium.

Marine Invertebrate Larvae Associated with Symbiodinium: A Mutualism from the Start?

“…Hence, the symbiosis between animal hosts and Symbiodinium likely formed independently on multiple occasions. The ability of Symbiodinium as well as other dinoflagellates to establish symbioses with such a diversity of hosts may derive from their evolutionary background as recently suggested by Aranda et al (2016). Parasitism is common in many extant dinoflagellates (Kuperman and Matey, 1999) as well as their closest relatives, the apicomplexans (Shoguchi et al, 2013;Lin et al, 2015).…”

“…The genomes for types within clades A, B, and F (Shoguchi et al, 2013;Lin et al, 2015;Aranda et al, 2016), transcriptomes for types within clades A-D (Bayer et al, 2012;Ladner et al, 2012;Parkinson et al, 2016) and the plastid genome for type B1 (Mungpakdee et al, 2014) and type C3 have been sequenced in recent years, but further information, especially on metabolic pathways, is still missing. However, a few experiments investigated differential gene expression in coral larvae with and without symbionts, all of which reported the absence of or rather small gene expression differences in the transcriptomes of symbiotic hosts when compared to the aposymbiotic state (deBoer et al, 2007;Voolstra et al, 2009b;Schnitzler and Weis, 2010).…”

Current Knowledge and Recent Advances in Marine Dinoflagellate Transcriptomic Research

“…Annotation of non-model organisms like dinoflagellates based on the annotations from their closest model relatives and several limitations have been identified in this approach [125,126]. Dinoflagellates from genus Symbiodinium might be suitable candidates for dinoflagellate models as they have the smallest genome size and are the only dinoflagellates with an available draft genome [14][15][16]. Furthermore, the biological processes of this genus are widely studied both at the cellular and molecular level [127,128].…”

“…To date, only three dinoflagellates draft genomes have been sequenced from the genus Symbiodinium. A complete genome sequence is not yet available for most dinoflagellates; therefore, attempts to study dinoflagellates at the genomic level are difficult [13][14][15][16]. Studies of the transcriptome can be a practical alternative in such cases [17], commonly being used in large-scale studies of gene expression using either microarrays or next-generation sequencing (NGS) RNA-seq [18].…”

Using Seawater to Document Coral-Zoothanthella Diversity: A New Approach to Coral Reef Monitoring Using Environmental DNA

“…Due to the symbiont natural rates of increase, corals steadily release Symbiodinium cells into the surrounding environment (Yamashita et al, 2011), suggesting that close to reefs, seawater should contain detectable quantities of DNA from both corals and Symbiodinium. Recently, whole genome sequences of an Acropora coral (Shinzato et al, 2011) and Symbiodinium (Shoguchi et al, 2013;Lin et al, 2015;Aranda et al, 2016) have been published, and nextgeneration sequencing (NGS) technologies have been used to investigate coral reef biodiversity (Shinzato et al, 2014b(Shinzato et al, , 2015Combosch and Vollmer, 2015;Bongaerts et al, 2017). In the genus Symbiodinium, each clade contains multiple genetic types, and identification has been performed using ribosomal, mitochondrial, plastid, and nuclear DNA markers (Rowan and Powers, 1991;Wilcox, 1998;Lajeunesse, 2001;Santos et al, 2002;Takabayashi et al, 2004).…”