Abstract

BackgroundDinoflagellates in the family Symbiodiniaceae are important photosynthetic symbionts in cnidarians (such as corals) and other coral reef organisms. Breakdown of the coral-dinoflagellate symbiosis due to environmental stress (i.e. coral bleaching) can lead to coral death and the potential collapse of reef ecosystems. However, evolution of Symbiodiniaceae genomes, and its implications for the coral, is little understood. Genome sequences of Symbiodiniaceae remain scarce due in part to their large genome sizes (1–5 Gbp) and idiosyncratic genome features.ResultsHere, we present de novo genome assemblies of seven members of the genus Symbiodinium, of which two are free-living, one is an opportunistic symbiont, and the remainder are mutualistic symbionts. Integrating other available data, we compare 15 dinoflagellate genomes revealing high sequence and structural divergence. Divergence among some Symbiodinium isolates is comparable to that among distinct genera of Symbiodiniaceae. We also recovered hundreds of gene families specific to each lineage, many of which encode unknown functions. An in-depth comparison between the genomes of the symbiotic Symbiodinium tridacnidorum (isolated from a coral) and the free-living Symbiodinium natans reveals a greater prevalence of transposable elements, genetic duplication, structural rearrangements, and pseudogenisation in the symbiotic species.ConclusionsOur results underscore the potential impact of lifestyle on lineage-specific gene-function innovation, genome divergence, and the diversification of Symbiodinium and Symbiodiniaceae. The divergent features we report, and their putative causes, may also apply to other microbial eukaryotes that have undergone symbiotic phases in their evolutionary history.

Highlights

  • Dinoflagellates in the family Symbiodiniaceae are important photosynthetic symbionts in cnidarians and other coral reef organisms

  • We included in our analysis available genome assemblies from six other Symbiodiniaceae and two hybrid assemblies from the outgroup species Polarella glacialis, totalling 15 dinoflagellate genomes

  • Gene functions related to symbiosis and stress response are less abundant in symbiotic Symbiodiniaceae We examined the functions annotated for the predicted genes from all 15 Suessiales genomes based on the annotated Gene Ontology (GO) terms and protein domains

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Summary

Introduction

Dinoflagellates in the family Symbiodiniaceae are important photosynthetic symbionts in cnidarians (such as corals) and other coral reef organisms. Dinoflagellates of the family Symbiodiniaceae are the predominant photosynthetic symbionts of cnidarians (e.g. corals, sea anemones and jellyfish), giant clams, sponges and other microorganisms including foraminiferans and ciliates [1]. A modest episodic increase in ocean surface temperature in this environment can result in oxidative damage and the decoupling of carbon flow between the symbiont and the host. Conservation strategies are urgently needed to maintain and restore existing coral reefs. The design of such interventions requires a multi-pronged approach to understand the role of each biotic component to sustain a healthy, resilient symbiosis [9,10,11]. The dearth of genome data from Symbiodiniaceae is explained by the relatively large sizes (1–5 Gbp) [13, 14], and complex, atypical structure of dinoflagellate genomes and chromosomes [15, 16]

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