Dynamic plastid and mitochondrial genomes in Chaetopeltidales (Chlorophyceae) and characterization of a new chlorophyte taxon

Abstract

Premise: Chaetopeltidales is a poorly characterized order in the Chlorophyceae, with only two plastid and no mitochondrial genomes published. Here we describe a new taxon in Chaetopeltidales, Gormaniella terricola gen. et sp. nov. and characterize both of its organellar genomes. Methods: Gormaniella terricola was inadvertently isolated from a surface-sterilized hornwort thallus. Light microscopy was used to characterize its vegetative morphology. Organellar genomes were assembled, annotated, and analyzed using a variety of software packages. Results: The mitochondrial genome (66,927 bp) represents the first complete mitochondrial genome published for Chaetopeltidales. The chloroplast genome, measuring 428,981 bp, is one of the largest plastid genomes published to date and shares this large size and an incredible number of short, dispersed repeats with the other sequenced chloroplast genomes in Chaetopeltidales. Despite these shared features, the chloroplast genomes of Chaetopeltidales appear to be highly rearranged when compared to one another, with numerous inversions, translocations, and duplications, suggesting a particularly dynamic chloroplast genome. Both the chloroplast and mitochondrial genomes of G. terricola contain a number of mobile group I and group II introns, which appear to have invaded separately. Three of the introns within the mitochondrial genome encode homing endonucleases that are phylogenetically nested within those found in fungi, rather than algae, suggesting a possible case of horizontal gene transfer. Conclusions: These results help to shed light on a poorly understood group of algae and their unusual organellar genomes, raising additional questions about the unique patterns of genome evolution within Chaetopeltidales.

Hydrocytium expands the phylogenetic, morphological, and genomic diversity of the poorly known green algal order Chaetopeltidales

“…However, in stationary-phase cultures, the formation of branching Hormotilopsis-like colonies prevails (Groover and Hofstetter, 1969). The accumulation of an extensive laminated extracellular matrix in older cultures of the closely related (if not congeneric) Gormaniella terricola was also observed (Robison et al, 2022). We noticed a similar matrix accumulation for Hydrocytium as well (Figure 1L).…”

“…corresponding to multiple separately transcribed, discontinuous fragments of the rns and of the rnl gene, as was also reported for G. terricola (Robison et al, 2022); note that the identification and annotation of all fragments is challenging without transcriptome data and that our annotation should be considered incomplete in this regard. The mitochondrial genes were not interrupted by introns, contrary to what has been found in Gormaniella (Robison et al, 2022).…”

“…Rather than indicating the mitogenome being multipartite, the separation of the sequence into three scaffolds reflects the presence of complex, difficult-to-resolve sequence repeats. Together, the three scaffolds account for 60,829 bp, which is less than the size of the mitogenome reported from Gormaniella (66,927 bp; Robison et al, 2022). However, combined they contain the same set of standard mitochondrial protein-coding genes found in Gormaniella (Appendix S2, Figure S3), with the exception of cox2a (transferred to the nucleus in SAG 40.91, see below).…”

“…) with 450,749 bp, exceeding the size of the Koshicola and Gormaniella plastomes(Watanabe et al, 2016;Robison …”

“…The discovery of Koshicola suggested that the exploration of the Chaetopeltidales diversity is incomplete, and novel undescribed species are definitely hiding somewhere. Indeed, a new member of the family Chaetopeltidaceae, Gormaniella terricola , has recently been isolated from the thallus of a hornwort and formally described, with the main attention paid to the organellar genomes and their intriguing features (Robison et al, 2022). The discovery of additional chaetopeltidalean algae could be enhanced not only by sampling previously unexplored habitats or paying more attention to the microflora of ordinary freshwater and terrestrial microhabitats (as exemplified by the two noted species), but also by investigating already established strains that either have not been sequenced yet, or have occupied unstable positions in previous phylogenetic analyses.…”