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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. [ABSTRACT FROM AUTHOR]

With growing urbanization and ongoing development activities, the consumption of heavy metals has been increasing globally. Although heavy metals are vital for the survival of living beings, they can become hazardous when they surpass the permissible limit. The effect of heavy metals varies from normal to acute depending on the individual, so it is necessary to treat the heavy metals before releasing them into the environment. Various conventional treatment technologies have been used based on physical, chemical, and biological methods. However, due to technical and economic constraints and poor sustainability towards the environment, the use of these technologies has been limited. Microalgal-based heavy metal removal has been explored for the past few decades and has been seen as an effective, environment-friendly, and inexpensive method compared to conventional treatment technology. Cyanidiales that belong to red algae have the potential for remediation of heavy metals as they can withstand and tolerate extreme stresses of heat, acid salts, and heavy metals. Cyanidiales are the only photosynthetic organisms that can survive and thrive in acidic mine drainage, where heavy metal contamination is often prevalent. This review focuses on the algal species belonging to three genera of Cyanidiales: Cyanidioschyzon, Cyanidium, and Galdieria. Papers published after 2015 were considered in order to examine these species' efficiency in heavy metal removal. The result is summarized as maximum removal efficiency at the optimum experimental conditions and based on the parameters affecting the metal ion removal efficiency. This study finds that pH, initial metal concentration, initial algal biomass concentration, algal strains, and growth temperature are the major parameters that affect the heavy metal removal efficiency of Cyanidiales. [ABSTRACT FROM AUTHOR]

Cyanidioschyzonmerolae is an extremophilic red microalga which grows in low-pH, high-temperature environments. The basis of C. merolae's environmental resilience is not fully characterized, including whether this alga uses a carbon-concentrating mechanism (CCM). To determine if C. merolae uses a CCM, we measured CO2 uptake parameters using an open-path infra-red gas analyzer and compared them to values expected in the absence of a CCM. These measurements and analysis indicated that C. merolae had the gas-exchange characteristics of a CCM-operating organism: low CO2 compensation point, high affinity for external CO2, and minimized rubisco oxygenation. The biomass δ13C of C. merolae was also consistent with a CCM. The apparent presence of a CCM in C. merolae suggests the use of an unusual mechanism for carbon concentration, as C. merolae is thought to lack a pyrenoid and gas-exchange measurements indicated that C. merolae primarily takes up inorganic carbon as carbon dioxide, rather than bicarbonate. We use homology to known CCM components to propose a model of a pH-gradient-based CCM, and we discuss how this CCM can be further investigated. [ABSTRACT FROM AUTHOR]

The Cyanidiales are a group of mostly thermophilic and acidophilic red algae that thrive near volcanic vents. Despite their phylogenetic relationship, the reduced genomes of Cyanidioschyzon merolae and Galdieria sulphuraria are strikingly different with respect to pre‐mRNA splicing, a ubiquitous eukaryotic feature. Introns are rare and spliceosomal machinery is extremely reduced in C. merolae, in contrast to G. sulphuraria. Previous studies also revealed divergent spliceosomes in the mesophilic red alga Porphyridium purpureum and the red algal derived plastid of Guillardia theta (Cryptophyta), along with unusually high levels of unspliced transcripts. To further examine the evolution of splicing in red algae, we compared C. merolae and G. sulphuraria, investigating splicing levels, intron position, intron sequence features, and the composition of the spliceosome. In addition to identifying 11 additional introns in C. merolae, our transcriptomic analysis also revealed typical eukaryotic splicing in G. sulphuraria, whereas most transcripts in C. merolae remain unspliced. The distribution of intron positions within their host genes was examined to provide insight into patterns of intron loss in red algae. We observed increasing variability of 5′ splice sites and branch donor regions with increasing intron richness. We also found these relationships to be connected to reductions in and losses of corresponding parts of the spliceosome. Our findings highlight patterns of intron and spliceosome evolution in related red algae under the pressures of genome reduction. [ABSTRACT FROM AUTHOR]

Cyanidiales were named enigmatic microalgae due to their unique polyextreme properties, considered for a very long time unattainable for eukaryotes. Cyanidiales mainly inhabit hot sulfuric springs with high acidity (pH 0-4), temperatures up to 56°C, and ability to survive in the presence of dissolved heavy metals. Owing to the minimal for eukaryotes genome size, Cyanidiales have become one of the most important research objects in plant cell physiology, biochemistry, molecular biology, phylogenomics, and evolutionary biology. They play an important role in studying many aspects of oxygenic photosynthesis and chloroplasts origin. The ability to survive in stressful habitats and the corresponding metabolic pathways were acquired by Cyanidiales from archaea and bacteria via horizontal gene transfer (HGT). Thus, the possibility of gene transfer from prokaryotes to eukaryotes was discovered, which was a new step in understanding of the origin of eukaryotic cell. [ABSTRACT FROM AUTHOR]

Several eukaryotic cell lineages proliferate by multiple fission cell cycles, during which cells grow to manyfold of their original size, then undergo several rounds of cell division without intervening growth. A previous study on volvocine green algae, including both unicellular and multicellular (colonial) species, showed a correlation between the minimum number of successive cell divisions without intervening cellular growth, and the threshold cell size for commitment to the first round of successive cell divisions: two times the average newly born daughter cell volume for unicellular Chlamydomonas reinhardtii, four times for four-celled Tetrabaena socialis, in which each cell in the colony produces a daughter colony by two successive cell divisions, and eight times for the eight-celled Gonium pectorale, in which each cell produces a daughter colony by three successive cell divisions. To assess whether this phenomenon is also applicable to other lineages, we have characterized cyanidialean red algae, namely, Cyanidioschyzon merolae, which proliferates by binary fission, as well as Cyanidium caldarium and Galdieria sulphuraria, which form up to four and 32 daughter cells (autospores), respectively, in a mother cell before hatching out. The result shows that there is also a correlation between the number of successive cell divisions and the threshold cell size for cell division or the first round of the successive cell divisions. In both C. merolae and C. caldarium, the cell size checkpoint for cell division(s) exists in the G1-phase, as previously shown in volvocine green algae. When C. merolae cells were arrested in the G1-phase and abnormally enlarged by conditional depletion of CDKA, the cells underwent two or more successive cell divisions without intervening cellular growth after recovery of CDKA, similarly to C. caldarium and G. sulphuraria. These results suggest that the threshold size for cell division is a major factor in determining the number of successive cell divisions and that evolutionary changes in the mechanism of cell size monitoring resulted in a variation of multiple fission cell cycle in eukaryotic algae. [ABSTRACT FROM AUTHOR]

Red algae have adapted to extreme environments by acquiring genes from bacteria and archaea.

Rapid fluctuation of environmental conditions can impose severe stress upon living organisms. Surviving such episodes of stress requires a rapid acclimation response, e.g., by transcriptional and post-transcriptional mechanisms. Persistent change of the environmental context, however, requires longer-term adaptation at the genetic level. Fast-growing unicellular aquatic eukaryotes enable analysis of adaptive responses at the genetic level in a laboratory setting. In this study, we applied continuous cold stress (28°C) to the thermoacidophile red alga G. sulphuraria, which is 14°C below its optimal growth temperature of 42°C. Cold stress was applied for more than 100 generations to identify components that are critical for conferring thermal adaptation. After cold exposure for more than 100 generations, the cold-adapted samples grew ∼30% faster than the starting population. Whole-genome sequencing revealed 757 variants located on 429 genes (6.1% of the transcriptome) encoding molecular functions involved in cell cycle regulation, gene regulation, signaling, morphogenesis, microtubule nucleation, and transmembrane transport. CpG islands located in the intergenic region accumulated a significant number of variants, which is likely a sign of epigenetic remodeling. We present 20 candidate genes and three putative cis-regulatory elements with various functions most affected by temperature. Our work shows that natural selection toward temperature tolerance is a complex systems biology problem that involves gradual reprogramming of an intricate gene network and deeply nested regulators.

The role and extent of horizontal gene transfer (HGT) in eukaryotes are hotly disputed topics that impact our understanding of the origin of metabolic processes and the role of organelles in cellular evolution. We addressed this issue by analyzing 10 novel Cyanidiales genomes and determined that 1% of their gene inventory is HGT-derived. Numerous HGT candidates share a close phylogenetic relationship with prokaryotes that live in similar habitats as the Cyanidiales and encode functions related to polyextremophily. HGT candidates differ from native genes in GC-content, number of splice sites, and gene expression. HGT candidates are more prone to loss, which may explain the absence of a eukaryotic pan-genome. Therefore, the lack of a pan-genome and cumulative effects fail to provide substantive arguments against our hypothesis of recurring HGT followed by differential loss in eukaryotes. The maintenance of 1% HGTs, even under selection for genome reduction, underlines the importance of non-endosymbiosis related foreign gene acquisition.

Rapid fluctuation of environmental conditions can impose severe stress upon living organisms. Surviving such episodes of stress requires a rapid acclimation response, e.g., by transcriptional and post-transcriptional mechanisms. Persistent change of the environmental context, however, requires longer-term adaptation at the genetic level. Fast-growing unicellular aquatic eukaryotes enable analysis of adaptive responses at the genetic level in a laboratory setting. In this study, we applied continuous cold stress (28°C) to the thermoacidophile red alga G. sulphuraria , which is 14°C below its optimal growth temperature of 42°C. Cold stress was applied for more than 100 generations to identify components that are critical for conferring thermal adaptation. After cold exposure for more than 100 generations, the cold-adapted samples grew ∼30% faster than the starting population. Whole-genome sequencing revealed 757 variants located on 429 genes (6.1% of the transcriptome) encoding molecular functions involved in cell cycle regulation, gene regulation, signaling, morphogenesis, microtubule nucleation, and transmembrane transport. CpG islands located in the intergenic region accumulated a significant number of variants, which is likely a sign of epigenetic remodeling. We present 20 candidate genes and three putative cis -regulatory elements with various functions most affected by temperature. Our work shows that natural selection toward temperature tolerance is a complex systems biology problem that involves gradual reprogramming of an intricate gene network and deeply nested regulators. [ABSTRACT FROM AUTHOR]

Thermoacidophilic Cyanidiales maintain a competitive edge in inhabiting extreme environments enriched with metals. Here, species of Cyanidioschyzon merolae (Cm), Cyanidium caldarium (Cc), and Galdieria partita (Gp) were exploited to remove hexavalent chromium [Cr(VI)]. Cm and Gp could remove 168.1 and 93.7 mg g−1 of Cr(VI) at pH 2.0 and 7.0, respectively, wherein 89% and 62% of sorbed Cr on Cm and Gp occurred as trivalent chromium [Cr(III)]. Apart from surface-sorbed Cr(VI), the in vitro Cr(III) bound with polysaccharide and in vivo chromium(III) hydroxide [Cr(OH) 3 ] attested to the reduction capability of Cyanidiales. The distribution of Cr species varied as a function of sorbed Cr amount, yet a relatively consistent proportion of Cr(OH) 3 , irrespective of Cr sorption capacity, was found only on Cm and Cc at pH 2.0. In conjunction with TXM (transmission X-ray microscopy) images that showed less impaired cell integrity and possible intracellular Cr distribution on Cm and Cc at pH 2.0, the in vivo Cr(OH) 3 might be the key to promoting the Cr sorption capacity (≥ 152 mg g−1). Cyanidiales are promising candidates for the green and sustainable remediation of Cr(VI) due to their great removal capacity, the spontaneous reduction under oxic conditions, and in vivo accumulation. [Display omitted] • C. merolae removed 168 mg g−1 of Cr(VI) at pH 2.0% and 89% was reduced to Cr(III). • G. partita removed 94 mg g−1 of Cr(VI) at pH 7.0% and 62% was reduced to Cr(III). • Cr retained as surface-sorbed Cr(VI) and in vitro as well as in vivo Cr(III). • Cr(III) species included Cr(III)-polysaccharide complexes and Cr(OH) 3 precipitates. • Cr(OH) 3 promoted Cr sorption capacity of Cyanidiales. [ABSTRACT FROM AUTHOR]

Thermoacidophilic cyanidia (Cyanidiales) are the primary photosynthetic eukaryotes in volcanic areas. These red algae also serve as important model organisms for studying life in extreme habitats. The global biodiversity and community structure of Cyanidiales remain unclear despite previous sampling efforts. Here, we surveyed the Cyanidiales biodiversity in the Tatun Volcano Group ( TVG) area in Taiwan using environmental DNA sequencing. We generated 174 rbcL sequences from eight samples from four regions in the TVG area, and combined them with 239 publicly available rbcL sequences collected worldwide. Species delimita-tion using this large rbcL data set suggested at least 20 Cyanidiales OTUs (operational taxono-mic units) worldwide, almost three times the presently recognized seven species. Results from environmental DNA showed that OTUs in the TVG area were divided into three groups: (i) dominant in hot springs with 92%-99% sequence identity to Galdieria maxima; (ii) largely distributed in drier and more acidic microhabitats with 99% identity to G. partita; and (iii) primarily distributed in cooler microhabitats and lacking identity to known cyanidia species (a novel Cyanidiales lineage). In both global and individual area analyses, we observed greater species diversity in non-aquatic than aquatic habitats. Community structure analysis showed high similarity between the TVG community and West Pacific-Iceland communities, reflecting their geographic proximity to each other. Our study is the first examination of the global species diversity and biogeographic affinity of cyanidia. Additionally, our data illuminate the influence of microhabitat type on Cyanidiales diversity and highlight intriguing questions for future ecological research. [ABSTRACT FROM AUTHOR]

Several species of unicellular eukaryotic algae exhibit relatively simple genomic and cellular architecture. Laboratory cultures of these algae grow faster than plants and often provide homogeneous cellular populations exposed to an almost equal environment. These characteristics are ideal for conducting experiments at the cellular and subcellular levels. Many microalgal lineages have recently become genetically tractable, which have started to evoke new streams of studies. Among such algae, the unicellular red alga Cyanidioschyzon merolae is the simplest organism; it possesses the minimum number of membranous organelles, only 4,775 protein-coding genes in the nucleus, and its cell cycle progression can be highly synchronized with the diel cycle. These properties facilitate diverse omics analyses of cellular proliferation and structural analyses of the intracellular relationship among organelles. C. merolae cells lack a rigid cell wall and are thus relatively easily disrupted, facilitating biochemical analyses. Multiple chromosomal loci can be edited by highly efficient homologous recombination. The procedures for the inducible/repressive expression of a transgene or an endogenous gene in the nucleus and for chloroplast genome modification have also been developed. Here, we summarize the features and experimental techniques of C. merolae and provide examples of studies using this alga. From these studies, it is clear that C. merolae-either alone or in comparative and combinatory studies with other photosynthetic organisms-can provide significant insights into the biology of photosynthetic eukaryotes., (© The Author(s) 2021. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.)

• Cyanidium caldarium (Cc) showed superior sorption capacity (298 mg g−1) for Pb(II). • Modulation of Pb tolerance by Cyanidiales was classified into four mechanisms. • Formation of organic complexes promoted Pb(II) ion sorption capacity of Cyanidiales. • Cyanidiales are innovative green materials for the environmental remediation. Thermoacidophilic Cyanidiales are capable to survive in extreme environments (20–56 °C; pH 0.5–5.0) with concentrated metals, allowing them to serve as promising green materials applied in metal remediation. It is the first attempt to determine the capacity and related mechanisms for Pb(II) ions sorption on three Cyanidiales genera: Galdieria maximum (Gm), Cyanidioschyzon merolae (Cm), and Cyanidium caldarium (Cc) in relation to changes in Pb speciation obtained from Pb L III -edge X-ray absorption, organic functional groups, and protein secondary structures derived from synchrotron-based Fourier-transform infrared spectroscopy. Three-dimensional images of Cyanidiales were collected using Transmission X-ray microscopy. Lead tolerance on Cyanidiales was modulated according to four mechanisms: the defense line provide by polysaccharide, the inorganic Pb-PO 4 precipitation, the organic Pb complexation concomitant with the transport to cell vacuoles, and the specific thiol-Pb chelation involved in disruption of protein secondary structures. Despite Cyanidiales generally performed all mechanisms against Pb toxicity, individual defense responses were highlighted by specific Cyanidiales species. The redistribution of Pb-polysaccharide species and inorganic Pb-PO 4 precipitates toward organic complexation promoted Pb(II) ions sorption capacity of Cyanidiales, accounting for the almost eight-time-greater sorbed Pb (298.4 mg g−1) on Cc in comparison to Gm. The knowledge provided here could improve the application of the Cyanidiales in environmental remediation as an innovative green technology. [ABSTRACT FROM AUTHOR]