Plasmid‐Associated Organelle Genome Evolution In Red Algae

Mitochondria and plastids are derived through endosymbiosis events from a-proteobacteria and cyanobacteria, respectively. In the case of plastids, a heterotrophic eukaryote engulfed the prokaryotic symbiont, followed by the many complex processes associated with organellogenesis (Brodie et al. 2017). In general, eukaryotic organelles are maternally inherited and lack genetic recombination (Bhattacharya et al. 2004, Timmis et al. 2004), thereby providing powerful phylogenetic markers (e.g., Yang et al. 2015, Costa et al. 2016, Lee et al. 2016a, D ıaz-Tapia et al. 2017). Since the rise of high-throughput sequencing (HTS) technologies, massive organelle genome databases have become available to better understand the evolutionary history of eukaryotes. For example, based on HTS data, it was suggested that the primary plastid-containing Archaeplastida (i.e., Rhodophyta, Glaucophyta, and Viridiplantae) underwent differential gene gains and losses in their organelle genomes after the endosymbiosis event. As a consequence, Rhodophyta (red algae) contains the largest number of plastid genes but the smallest mitochondrial gene inventory is found among Archaeplastida (Lee et al. 2016a, Qiu et al. 2017). Exceptions to genome size conservation are provided by the plastid of the green alga Haematococcus lacustris (~1.3 million base pairs [Mbp]; Bauman et al. 2018) and red algal Rhodellophyceae species (~0.5-1.1 Mbp; Mu~ nozG omez et al. 2017), which however, contain conserved gene inventories. Additional organellar genome data will undoubtedly bring new insights into evolutionary trends as well as further resolve algal and other eukaryotic phylogenetic relationships. In red algae, there have been several interesting studies in recent decades about plasmid-associated organelle genome evolution (Hagopian et al. 2004, Janou skovec et al. 2013, Campbell et al. 2014, Lee et al. 2015, 2016a,b, Du et al. 2016, Ng et al. 2017). Plasmid-derived sequences (PDS) were frequently reported in red algal organellar genomes that were likely derived from viruses, bacterial plasmids, as well as nuclear and mitochondrial genomes of diverse eukaryotic lineages (i.e., land plants, stramenopiles, Rhizaria). For instance, plasmid-derived horizontal gene transfers (HGTs) of cyanobacterial hypothetical proteins containing the novel DNA polymerase type-B family catalytic domain superfamily was found in red algal organellar genomes, analogous to the proteobacterial-derived leucine biosynthesis operon (leuC/D genes; Janou skovec et al. 2013, Lee et al. 2016b). Interestingly, the PDS regions are present in all reported organellar genomes in the Gracilariaceae. Iha et al. (2018) summarized these organellar PDS in the Gracilariaceae with the addition of nine plastid and 10 mitochondrial genomes from 10 species (Gracilaria caudata, G. ferox, G. gracilis, G. rangiferina, G. tenuistipitata, G. vermiculophylla, Gracilariopsis longissima, Gp. mclachlanii, Gp. tenuifrons, and Melanthalia intermedia) as well as three new plasmid sequences from two species (G. ferox [Gfe3115], and G. vermiculophylla [Gve4548 and Gve7464]). This study found the leucine biosynthesis genes (leuC/D) not only in plastid genomes but also in plasmids of the Gracilariaceae (i.e., the leuC/D homologous proteins in G. vermiculophylla plasmids) and suggested plasmid-mediated HGTs to the plastid genome. These three novel plasmids in the Gracilariaceae could provide the opportunity to study the intertwined evolutionary history of red algal organelles and plasmids within a species. Because abundant plasmid gene pools and their PDS regions are available, this study suggested that the family Gracilariaceae is a useful taxonomic group to study the impacts of PDS in genome evolution. However, to trace the evolutionary trajectory of PDSs, it is essential to study nuclear genomes. There are currently two available nuclear genomes from Gracilariaceae species (Gp. chorda [92 Mbp, N50 = 220 Kbp, 1,211 contigs; Lee et al. 2018], and Gp. lemaneiformis [88 Mbp, N50 = 30 Kbp, 13,825 contigs; Sun et al. 2018]); therefore, further study should focus on how genes are transferred among different genetic compartments of plasmid, organellar, and nuclear genomes. Such data might prove useful in testing hypotheses about plasmid-associated genome evolution. What is the role of PDS insertions? The possible role of plasmids as mediators of HGTs is intriguing J. Phycol. 54, 772–774 (2019) © 2019 Phycological Society of America DOI: 10.1111/jpy.12797