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

Sarah Farhat 1, 2 Phuong Le 3 Ehsan Kayal 4 Benjamin Noel 1 Estelle Bigeard 5 Erwan Corre 4 Florian Maumus 6 Isabelle Florent 7 Adriana Alberti 1 Jean-Marc Aury 1 Tristan Barbeyron 8 Ruibo Cai 5 Corinne da Silva 1 Benjamin Istace 1 Karine Labadie 1 Dominique Marie 5 Jonathan Mercier 1 Tsinda Rukwavu 1 Jeremy Szymczak 4, 5 Thierry Tonon 9 Catharina Alves-De-Souza 10 Pierre Rouzé 3 Yves van de Peer 3, 11 Patrick Wincker 1 Stephane Rombauts 3 Betina Porcel 1, * Laure Guillou 5, *
* Corresponding author
1 UMR 8030 - Génomique métabolique
2 SoMAS - School of Marine and Atmospheric Sciences [Stony Brook]
3 PSB Center - Center for Plant Systems Biology
4 FR2424 - ABiMS - Informatique et bioinformatique = Analysis and Bioinformatics for Marine Science
5 ECOMAP - ECOlogy of MArine Plankton
AD2M - Adaptation et diversité en milieu marin
6 URGI - Unité de Recherche Génomique Info
7 MCAM - Molécules de Communication et Adaptation des Micro-organismes
8 LBI2M - Laboratoire de Biologie Intégrative des Modèles Marins
9 University of York [York, UK]
10 UNC - University of North Carolina [Wilmington]
11 Department of Biochemistry, Genetics and Microbiology [Pretoria]
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.
Keywords : Non-canonical introns Introner elements Genome Parasite Dinoflagellate
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Submitted on : Monday, October 18, 2021 - 3:48:18 PM
Last modification on : Monday, April 11, 2022 - 10:39:24 AM

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INRAE | UNIV-PARIS-SACLAY | CEA | JACOB | CEA-DRF | UNIV-EVRY | MNHN | FR2424 | GENOSCOPE | SU-SCIENCES | LBI2M | CEA-UPSAY | GS-BIOSPHERA | GS-LIFE-SCIENCES-HEALTH | CNRS | ADMM | ANR | SORBONNE-UNIVERSITE | SU-TI

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Sarah Farhat, Phuong Le, Ehsan Kayal, Benjamin Noel, Estelle Bigeard, et al.. Rapid protein evolution, organellar reductions, and invasive intronic elements in the marine aerobic parasite dinoflagellate Amoebophrya spp. BMC Biology, BioMed Central, 2021, 19 (1), ⟨10.1186/s12915-020-00927-9⟩. ⟨hal-03114990⟩

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