Rapid protein evolution, organellar reductions, and invasive intronic elements in the marine aerobic parasite dinoflagellate Amoebophrya spp

Sarah Farhat,Pierre Rouzé,Florian Maumus,Tsinda Rukwavu,Betina M Porcel,Phuong Thi Le ,Jeremy Szymczak,Isabelle Florent,Ehsan Kayal,Matthieu Le Corre ,Corinne Da Silva,Benjamin Istace,Yves Van De Peer,Ruibo Cai,Thierry Tonon,Stéphane Rombauts ,Adriana Alberti,Dominique Marie,Patrick Wincker,Catharina Alves‐De‐Souza ,Tristan Barbeyron,Jean‐Marc Aury ,Jonathan Mercier,Estelle Bigeard,Karine Labadie,Benjamin Noël ,Laure Guillou

doi:10.1186/s12915-020-00927-9

Abstract

BackgroundDinoflagellates are aquatic protists particularly widespread in the oceans worldwide. Some are responsible for toxic blooms while others live in symbiotic relationships, either as mutualistic symbionts in corals or as parasites infecting other protists and animals. Dinoflagellates harbor atypically large genomes (~ 3 to 250 Gb), with gene organization and gene expression patterns very different from closely related apicomplexan parasites. Here we sequenced and analyzed the genomes of two early-diverging and co-occurring parasitic dinoflagellate Amoebophrya strains, to shed light on the emergence of such atypical genomic features, dinoflagellate evolution, and host specialization.ResultsWe sequenced, assembled, and annotated high-quality genomes for two Amoebophrya strains (A25 and A120), using a combination of Illumina paired-end short-read and Oxford Nanopore Technology (ONT) MinION long-read sequencing approaches. We found a small number of transposable elements, along with short introns and intergenic regions, and a limited number of gene families, together contribute to the compactness of the Amoebophrya genomes, a feature potentially linked with parasitism. While the majority of Amoebophrya proteins (63.7% of A25 and 59.3% of A120) had no functional assignment, we found many orthologs shared with Dinophyceae. Our analyses revealed a strong tendency for genes encoded by unidirectional clusters and high levels of synteny conservation between the two genomes despite low interspecific protein sequence similarity, suggesting rapid protein evolution. Most strikingly, we identified a large portion of non-canonical introns, including repeated introns, displaying a broad variability of associated splicing motifs never observed among eukaryotes. Those introner elements appear to have the capacity to spread over their respective genomes in a manner similar to transposable elements. Finally, we confirmed the reduction of organelles observed in Amoebophrya spp., i.e., loss of the plastid, potential loss of a mitochondrial genome and functions.ConclusionThese results expand the range of atypical genome features found in basal dinoflagellates and raise questions regarding speciation and the evolutionary mechanisms at play while parastitism was selected for in this particular unicellular lineage.

Highlights

Dinoflagellates are aquatic protists widespread in the oceans worldwide
Compact genomes among early-diverging dinoflagellates Genome assemblies of the two Amoebophrya sp. strains resulted in cumulative sizes of 116 Mb and 115.5 Mb for A25 and A120, respectively (Table 1, Table S2)
Both strains share many similarities with other dinoflagellates at the genome level: their chromosomes appear to be condensed most of the time and remain attached to the nuclear membrane [16]; they code for dinoflagellate/viral nucleoproteins (DVNPs) [7]; some of their mature transcripts contain a truncated dinoflagellate-specific spliced leader (DinoSL) motif found in other dinoflagellates [12] resulting from trans-splicing of premRNAs; they share more orthologous genes with Dinophyceae than with any other myzozoan

Summary

Introduction

Dinoflagellates are aquatic protists widespread in the oceans worldwide. Dinoflagellates harbor atypically large genomes (~ 3 to 250 Gb), with gene organization and gene expression patterns very different from closely related apicomplexan parasites. Half of known dinoflagellates are photosynthetic species representing important marine primary producers, with some of them responsible for toxic blooms. Permanently packed into condensed liquid-crystalline dinokaryons [5, 6] Their genetic material is associated with dinoflagellate/viral nucleoproteins (DVNPs) that likely originated from phycodnaviruses [7] and histonelike proteins derived from bacterial HU-like proteins [8]. The exploration of early-diverging dinoflagellate lineages such as the Syndiniales ( known as environmental Marine ALVeolates or MALVs [15]) shall shed light on the emergence of such atypical genomic features

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