Molecular phylogenetics supports a clade of red algal parasites retaining native plastids: taxonomy and terminology revised

Abstract

Parasitism is a life strategy that has repeatedly evolved within the Florideophyceae. Historically, the terms adelphoparasite and alloparasite have been used to distinguish parasites based on the relative phylogenetic relationship of host and parasite. However, analyses using molecular phylogenetics indicate that nearly all red algal parasites infect within their taxonomic family, and a range of relationships exist between host and parasite. To date, all investigated adelphoparasites have lost their plastid, and instead, incorporate a host‐derived plastid when packaging spores. In contrast, a highly reduced plastid lacking photosynthesis genes was sequenced from the alloparasite Choreocolax polysiphoniae. Here we present the complete Harveyella mirabilis plastid genome, which has also lost genes involved in photosynthesis, and a partial plastid genome from Leachiella pacifica. The H. mirabilis plastid shares more synteny with free‐living red algal plastids than that of C. polysiphoniae. Phylogenetic analysis demonstrates that C. polysiphoniae, H. mirabilis, and L. pacifica form a robustly supported clade of parasites, which retain their own plastid genomes, within the Rhodomelaceae. We therefore transfer all three genera from the exclusively parasitic family, Choreocolacaceae, to the Rhodomelaceae. Additionally, we recommend applying the terms archaeplastic parasites (formerly alloparasites), and neoplastic parasites (formerly adelphoparasites) to distinguish red algal parasites using a biological framework rather than taxonomic affiliation with their hosts.

Response to Preuss and Zuccarello (2020): biological definitions that can be unambiguously applied for red algal parasites

“…, Kurihara et al. , Salomaki and Lane ). With well over 100 independent evolutionary events giving rise to red algal parasites, and most descriptions based on morphology alone, using an inferred evolutionary relationship between host and parasite is inherently problematic.…”

“…However, they mischaracterize our conclusions and infer statements from our paper that confuse the issue at hand. This is a result, in part, due to an over specification in table 2 of our manuscript that relies, perhaps too heavily, on traits from the few well‐studied red algal parasites (Salomaki and Lane ). Here we clarify these issues.…”

“…Recently, we proposed to update the terminology for discussing different types of red algal parasites, based on biological differences, rather than evolutionary relationships to their hosts (Salomaki and Lane ). Preuss and Zuccarello () have written a commentary in which they point out some important issues that should be addressed, and also suggest that it is premature to update terminology.…”

A Comment on Salomaki and Lane 2019 “Molecular Phylogenetics Supports a Clade of Red Algal Parasites Retaining Native Plastids: Taxonomy and Terminology Revised”1

“…The new terminology introduced by Salomaki and Lane () of “archaeplastic” parasites was proposed to contain all parasites with their own reduced native plastid (i.e., lacking all, or most, photosynthesis related genes) based on data from Choreocolax polysiphoniae and Harveyella mirabilis . The authors proposed that this grouping should apply to all parasites distantly related to their host (formerly “alloparasites”).…”

“…While groupings based on common origins, common developmental patterns or common genomic changes could be useful in understanding their evolution, even the preliminary data to date indicate that these groupings of parasites proposed by Salomaki and Lane () is premature and probably too simplistic. There are over 120 described red algal parasites, and only a very small subset has been studied in any depth (Preuss et al.…”