High-throughput sequencing of the kelp Alaria (Phaeophyceae) reveals epi-endobiotic associations, including a likely phaeophycean parasite

ABSTRACT Whole genome sequencing datasets present the opportunity to not only study evolution in the target organism, but also the associated holobiont. The capacity to study epi-endobiotic kelp associations is improving substantially with the increased availability of high-throughput sequencing datasets. The goal of this study was to determine if shotgun sequencing libraries could be used to document epi- and endophyte/faunal species colonizing Alaria kelp sporophytes from Kamchatka (Russia), the Bay of Fundy (Atlantic Canada) and Nuuk (Greenland). Mitochondrial coxI and plastid rbcL reads were extracted and assembled from six Alaria whole genome sequencing datasets. In total, contigs representing 11 epi-endobiotic species were assembled, of which Chordariacean diversity dominated. Given the presence of a newly discovered phaeophycean coxI sequence lacking an rbcL counterpart, we secondarily tested our hypothesis that the coxI sequence belonged to a phaeophycean parasite. The entire read dataset was assembled for the Alaria specimen hosting the putative parasite, the mitochondrial genome was retrieved, and plastid scaffolds were annotated and screened for phylogenetic placement matching the coxI sequence. The mitochondrial genome of the candidate parasite displayed numerous atypical features, including duplicated genes and rearrangements, and clear signs of relaxed selection, in line with the notion this organism may have a deviant lifestyle. The plastid genome was recovered as several fragments and lacked genes for photosystem and cytochrome complexes and chlorophyll biosynthesis, confirming our hypothesis that the unknown phaeophycean represented a parasitic species. Furthermore, classification to order remained unclear for the phaeophycean parasite, suggesting this species could represent a newly discovered higher-level lineage. Our study showcases the utility of whole-genome sequencing datasets in revealing surprising aspects of the eukaryotic diversity inhabiting kelp holobionts.