DNA Damage Response Pathways in Dinoflagellates

Abstract

Dinoflagellates are a general group of phytoplankton, ubiquitous in aquatic environments. Most dinoflagellates are non-obligate autotrophs, subjected to potential physical and chemical DNA-damaging agents, including UV irradiation, in the euphotic zone. Delay of cell cycles by irradiation, as part of DNA damage responses (DDRs), could potentially lead to growth inhibition, contributing to major errors in the estimation of primary productivity and interpretations of photo-inhibition. Their liquid crystalline chromosomes (LCCs) have large amount of abnormal bases, restricted placement of coding sequences at the chromosomes periphery, and tandem repeat-encoded genes. These chromosome characteristics, their large genome sizes, as well as the lack of architectural nucleosomes, likely contribute to possible differential responses to DNA damage agents. In this study, we sought potential dinoflagellate orthologues of eukaryotic DNA damage repair pathways, and the linking pathway with cell-cycle control in three dinoflagellate species. It appeared that major orthologues in photoreactivation, base excision repair, nucleotide excision repair, mismatch repair, double-strand break repair and homologous recombination repair are well represented in dinoflagellate genomes. Future studies should address possible differential DNA damage responses of dinoflagellates over other planktonic groups, especially in relation to possible shift of life-cycle transitions in responses to UV irradiation. This may have a potential role in the persistence of dinoflagellate red tides with the advent of climatic change.

Comparison of 15 dinoflagellate genomes reveals extensive sequence and structural divergence in family Symbiodiniaceae and genus Symbiodinium

“…Compared to the symbiotic Breviolum and Cladocopium lineages, we observed a higher relative abundance of gene functions related to DNA damage repair and cell division in genomes of Symbiodinium , Fugacium and Polarella (Additional File 2 : Supplementary Figure 9). This is consistent with results from earlier studies [ 36 , 43 ], lending support for sexual reproduction [ 35 , 44 , 45 ] and recombination as a contributing factor to the genetic diversity of Symbiodiniaceae [ 46 – 50 ]. Sexual reproduction has been described in other dinoflagellates [ 51 ].…”

Genomes of Symbiodiniaceae reveal extensive sequence divergence but conserved functions at family and genus levels

“…6). The abundance of genes annotated with DNA repair functions is consistent with the previously reported overrepresentation of these functions in genomes and transcriptomes of Suessiales 7 and the presence of gene orthologs involved in a wide range of DNA damage responses in dinoflagellates 25 . Likewise, the relatively high abundance of functions related to DNA recombination may represent further support for the potential of sexual reproduction in these dinoflagellates 11,26 , and for the contribution of sexual recombination to genetic diversity of Symbiodiniaceae 27–31 .…”

Putative Meiotic Toolkit in the Dinoflagellate Prorocentrum cordatum: Additional Evidence for Sexual Process from Transcriptome

“…MND1 alone has also been found in L. polyedra, and HOP2-MND1 entirely has not been identified in A. carterae (Morse 2019). The data on these proteins vary in Symbiodiniaceae (Chi et al 2014;Li and Wong 2019;Liu et al 2018;Morse 2019), although Shah et al (2020) included HOP2-MND1 heterodimer in the proposed model of sexual stages of the life cycle in this group. We identified homologs of MLH1 endonuclease, SGS1 helicase, and EXO1 exonuclease, which participate in crossover pathway I, and MUS81 endonuclease of crossover pathway II in P. cordatum transcriptome data.…”

“…MLH1, in turn, is also a part of the DNA mismatch repair complex (Kunkel and Erie 2005). Nevertheless, the possibility of pathway I in dinoflagellates merits investigation since homologs of its key elements-MSH4-MSH5 heterodimer and MLH3 interacting with MLH1-have been found in L. polyedra and some Symbiodiniaceae species (Chi et al 2014;Li and Wong 2019;Liu et al 2018;Morse 2019;Shah et al 2020). The studied dinoflagellates have no homologs of MUS81-associated proteins (yeast MMS4 or plant EME1A-EME1B).…”