Genome-wide signatures of adaptation to extreme environments in red algae

Abstract

The high temperature, acidity, and heavy metal-rich environments associated with hot springs have a major impact on biological processes in resident cells. One group of photosynthetic eukaryotes, the Cyanidiophyceae (Rhodophyta), has successfully thrived in hot springs and associated sites worldwide for more than 1 billion years. Here, we analyze chromosome-level assemblies from three representative Cyanidiophyceae species to study environmental adaptation at the genomic level. We find that subtelomeric gene duplication of functional genes and loss of canonical eukaryotic traits played a major role in environmental adaptation, in addition to horizontal gene transfer events. Shared responses to environmental stress exist in Cyanidiales and Galdieriales, however, most of the adaptive genes (e.g., for arsenic detoxification) evolved independently in these lineages. Our results underline the power of local selection to shape eukaryotic genomes that may face vastly different stresses in adjacent, extreme microhabitats.

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

“…The Cyanidiales is characterized by high optimal growth temperatures (50–65°C) and low pH values (0–4). The nuclear genome of C. caldarium consists of 20 chromosomes (Cho et al, 2023). They are obligate photoautotrophs.…”

“…That is, the Cyanidioschyzonales have reduced and condensed plastid genomes compared to the Cyanidiales (Tables S3 and S4), which are caused by extremely shortened intergenic regions, shortened CDS, and overlapped CDS sequences (Figure 5). Also, intron‐poor nuclear genomes are found only with Cyanidioschyzon merolae and Cyanidiococcus yangmingshanensis (Cho et al, 2023; Liu et al, 2020; Matsuzaki et al, 2004).…”

“…The Galderiales plastid genome has specific gene losses, but it also has a relatively increased proportion of repetitive sequences (Figures S4 and S5; Table S4). The nuclear genome is composed of 50–60 or more chromosomes (Cho et al, 2023; Moreira et al, 1994). The nuclear genome has a 37%–40% GC content and is intron‐rich (Cho et al, 2023; Liu et al, 2020; Matsuzaki et al, 2004; Rossoni et al, 2019; Schönknecht et al, 2013).…”

“…The nuclear genome is composed of 50–60 or more chromosomes (Cho et al, 2023; Moreira et al, 1994). The nuclear genome has a 37%–40% GC content and is intron‐rich (Cho et al, 2023; Liu et al, 2020; Matsuzaki et al, 2004; Rossoni et al, 2019; Schönknecht et al, 2013).…”

Extremophilic red algae reordered

“…Increased attention has been paid to the genetic basis of these intriguing microalgae, helping to explain the molecular mechanisms that help them cope with environmental stressors and contribute to habitat specialization. For example, in comparison to other free‐living eukaryotes and their mesophilic red algal sisters, Cyanidiophyte nuclear and mitochondrial genomes are notably reduced (Cho et al, 2020, 2023). Moreover, many nuclear genes were observed to have been acquired by horizontal gene transfer (HGT) from their prokaryotic counterparts (Cho et al, 2023; Jain et al, 2014; Matsuzaki et al, 2004; Qiu et al, 2013; Rossoni et al, 2019; Schönknecht et al, 2013).…”