Revised classification of the Cyanidiophyceae based on plastid genome data with descriptions of the Cavernulicolales ord. nov. and Galdieriales ord. nov. (Rhodophyta)

Abstract

The Cyanidiophyceae, an extremophilic red algal class, is distributed worldwide in extreme environments. Species grow either in acidic hot environments or in dim light conditions (e.g., “cave Cyanidium”). The taxonomy and classification systems are currently based on morphological, eco‐physiological, and molecular phylogenetic characters; however, previous phylogenetic results showed hidden diversity of the Cyanidiophyceae and suggested a revision of the classification system. To clarify phylogenetic relationships within this red algal class, we employ a phylogenomic approach based on 15 plastomes (10 new) and 15 mitogenomes (seven new). Our phylogenies show consistent relationships among four lineages (Galdieria, “cave Cyanidium”, Cyanidium, and Cyanidioschyzon lineages). Each lineage is distinguished by organellar genome characteristics. The “cave Cyanidium” lineage is a distinct clade that diverged after the Galdieria clade but within a larger monophyletic clade that included the Cyanidium and Cyanidioschyzon lineages. Because the “cave Cyanidium” lineage is a mesophilic lineage that differs substantially from the other three thermoacidophilic lineages, we describe it as a new order (Cavernulicolales). Based on this evidence, we reclassified the Cyanidiophyceae into four orders: Cyanidiales, Cyanidioschyzonales, Cavernulicolales ord. nov., and Galdieriales ord. nov. The genetic distance among these four orders is comparable to, or greater than, the distances found between other red algal orders and subclasses. Three new genera (Cavernulicola, Gronococcus, Sciadococcus), five new species (Galdieria javensis, Galdieria phlegrea, Galdieria yellowstonensis, Gronococcus sybilensis, Sciadococcus taiwanensis), and a new nomenclatural combination (Cavernulicola chilensis) are proposed.

Extremophilic red algae reordered

“…In some cases, the re‐definition of a taxon may simply be enough (Barcytė et al, 2022), while in others, novel higher‐rank taxa emerge and deserve formal recognition (Barcytė et al, 2021; Li et al, 2020; Muñoz‐Gómez et al, 2017). This latter scenario is what applies to the the enigmatic red algal class Cyanidiophyceae revised recently by Park et al (2023) and highlighted here.…”

“…The known diversity of Cyanidiophyceae is relatively small. Prior to work of Park et al (2023), only nine species (though some of them had not been validly described) placed in four genera — Cyanidium , Cyanidioschyzon , Cyanidiococcus , and Galdieria — were mentioned in the literature. They differ in cell morphology, cell biology, and ecology.…”

“…Unsurprisingly, plastid phylogenomics and plastid evolution were the main foci in the study of Park et al (2023), helping to chart the new order‐level classification scheme of the Cyanidiophyceae microalgae, dividing the class into a total of four orders, with two of them newly established. Owing to the conducted phylogenomic analyses, the evolutionary branching order of Cyanidiophyceae was also firmly established: the first to diverge was Galdieriales ordo nov. (with three additional Galdieria species described by the respective authors), followed by Cavernulicolales ordo nov. (including the mesophilic or “cave Cyanidium ,” placed now in three novel genera Cavernulicola , Gronococcus , and Sciadococcus , and two new species to science), leaving Cyanidiales (with its representative genus Cyanidium ) and Cyanidioschyzonales (including the monotypic Cyanidioschyzon and Cyanidiococcus ) to branch off most recently (Figure 1).…”

“…The most intriguing features of the Cyanidiophyceae plastid genomes described and discussed by Park et al (2023) include, for example, Cyanidioschyzonales having the smallest genome size yet the highest coding‐region density in comparison with the other three orders. The authors suggested this to be the consequence of the adaptation to the higher temperature tolerance exhibited by the Cyanidioschyzonales members.…”

“…Overall, the comprehensive classification system proposed by Park et al (2023) with crucial insights into plastid genome evolution provides the solid base for future studies of the Cyanidiophyceae algae. Apart from additional cryptic lower‐order taxa awaiting formal descriptions, new lineages of the class are expected to be discovered hidden in little explored or unsampled sites.…”