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

Abstract

Background Dinoflagellates 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. Results We 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. Conclusion These 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.

Genistein as a regulator of signaling pathways and microRNAs in different types of cancers

“…Genetic mapping and genome wide analysis have enabled researchers to pinpoint different genetic variants of cell signaling cascades. Advancements in functional genomics have laid foundation of a new frontier in molecular oncology and understanding of molecular mechanisms involved in genetic variants [ 1 , 2 ]. Genistein is an isoflavone which could be found in soybean, chickpeas, and another soy-based foodstuff.…”

Is the Dinoflagellate Amoebophrya Really Missing an mtDNA?

“…For each Amoebophrya strain, cox1 sequences from Perkinsus marinus (HQ670240.1) and Perkinsus chesapeaki (HQ670238.1) were used as BLAST queries (v.2.9.0; e value 1e-03) against two libraries: one containing unique DNA-seq reads from Farhat et al. (2021) and another containing meta-transcriptomes assembled for each sampling time using data from Farhat et al.…”

“…But, here again, the authors were unable to identify any regions encoding the highly conserved oxygen-binding domain of COX1, which is all the more intriguing given that Amoebophrya is an aerobic clade ( John et al. 2019 ; Farhat et al. 2021 ).…”

“…More recently, a genome study of two other Amoebophrya strains (A120 and A25) also reported nuclear-encoded cox1 fragments, corresponding to the metal-binding sites located near the C-terminus of the protein and harboring mitochondrial transit peptides ( fig. 1 A ) ( Farhat et al. 2021 ).…”

“…1 B ; supplementary table S1 , Supplementary Material online), all showing expression during at least one life-cycle stage. This has led to doubts about whether Amoebophrya has truly lost its mitochondrial genome ( Farhat et al. 2021 ).…”