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Acidophilic Green Algal Genome Provides Insights Into Adaptation To Acidophilic green algal genome provides insights into PNAS PLUS adaptation to an acidic environment Shunsuke Hirookaa,b,1, Yuu Hirosec, Yu Kanesakib,d, Sumio Higuchie, Takayuki Fujiwaraa,b,f, Ryo Onumaa, Atsuko Eraa,b, Ryudo Ohbayashia, Akihiro Uzukaa,f, Hisayoshi Nozakig, Hirofumi Yoshikawab,h, and Shin-ya Miyagishimaa,b,f,1 aDepartment of Cell Genetics, National Institute of Genetics, Shizuoka 411-8540, Japan; bCore Research for Evolutional Science and Technology, Japan Science and Technology Agency, Saitama 332-0012, Japan; cDepartment of Environmental and Life Sciences, Toyohashi University of Technology, Aichi 441-8580, Japan; dNODAI Genome Research Center, Tokyo University of Agriculture, Tokyo 156-8502, Japan; eResearch Group for Aquatic Plants Restoration in Lake Nojiri, Nojiriko Museum, Nagano 389-1303, Japan; fDepartment of Genetics, Graduate University for Advanced Studies, Shizuoka 411-8540, Japan; gDepartment of Biological Sciences, Graduate School of Science, University of Tokyo, Tokyo 113-0033, Japan; and hDepartment of Bioscience, Tokyo University of Agriculture, Tokyo 156-8502, Japan Edited by Krishna K. Niyogi, Howard Hughes Medical Institute, University of California, Berkeley, CA, and approved August 16, 2017 (received for review April 28, 2017) Some microalgae are adapted to extremely acidic environments in pumps that biotransform arsenic and archaeal ATPases, which which toxic metals are present at high levels. However, little is known probably contribute to the algal heat tolerance (8). In addition, the about how acidophilic algae evolved from their respective neutrophilic reduction in the number of genes encoding voltage-gated ion ancestors by adapting to particular acidic environments. To gain channels and the expansion of chloride channel and chloride car- insights into this issue, we determined the draft genome sequence rier/channel families in the genome has probably contributed to the of the acidophilic green alga Chlamydomonas eustigma and per- algal acid tolerance (8). Likewise, a study in the acidophilic green formed comparative genome and transcriptome analyses between alga Chlamydomonas acidophila showed that phytochelatin syn- C. eustigma and its neutrophilic relative Chlamydomonas reinhardtii. thase genes of bacterial HGT origin played an important role in The results revealed the following features in C. eustigma that prob- the tolerance to cadmium (10). ably contributed to the adaptation to an acidic environment. Genes + However, the genomes of acidophilic algae other than cyani- encoding heat-shock proteins and plasma membrane H -ATPase are dialean red algae have not been sequenced. The green and red highly expressed in C. eustigma. This species has also lost fermentation algae diverged relatively soon after the emergence of primitive PLANT BIOLOGY pathways that acidify the cytosol and has acquired an energy shuttle eukaryotic algae (11). In addition, comparisons with neutrophilic and buffering system and arsenic detoxification genes through hori- relatives are feasible in the case of acidophilic green algae but are zontal gene transfer. Moreover, the arsenic detoxification genes have difficult in the case of cyanidialean red algae because their last been multiplied in the genome. These features have also been found common acidophilic ancestor diverged from other neutrophilic red in other acidophilic green and red algae, suggesting the existence of algae 1.2–1.3 billion y ago (12). Thus, whole-genome comparisons common mechanisms in the adaptation to acidic environments. between evolutionarily related neutrophilic and acidophilic green algae will give insights into how acidophiles evolved from their environmental adaptation | acidic environment | acidophilic alga | neutrophilic ancestors. comparative genomics | comparative transcriptomics Significance everal eukaryotic microalgae have been identified in acidic environments (pH <4.0) such as acid mine drainage (AMD) S Extremely acidic environments are scattered worldwide, and and geothermal hot springs (1). In this pH range, cyanobacteria their ecosystems are supported by acidophilic microalgae as are not present, and only acidophilic eukaryotic phototrophs are primary producers. To understand how acidophilic algae capable of photosynthesis (Fig. 1) (2, 3). The extremely low pH evolved from their respective neutrophilic ancestors, we de- of these waters is due to the dissolution and oxidation of sulfur termined the draft genome sequence of the acidophilic green that is exposed to water and oxygen and produces sulfuric acid alga Chlamydomonas eustigma and performed comparative (4). The low pH facilitates metal solubility in water; therefore, genome analyses between C. eustigma and its neutrophilic acidic waters tend to have high concentrations of metals (5). relative Chlamydomonas reinhardtii. The results suggest that Thus, acidophilic eukaryotic algae usually possess the ability to + higher expression of heat-shock proteins and H -ATPase, loss cope with toxic heavy metals in addition to low pH, both of which of some metabolic pathways that acidify cytosol, and acquisi- are lethal to most eukaryotes (2). Acidophilic algae are distrib- tion of metal-detoxifying genes by horizontal gene transfer uted throughout different branches of the eukaryotes, such as in have played important roles in the adaptation to acidic envi- red and green algae, stramenopiles, and euglenids. In most cases, ronments. These features are also found in other acidophilic neutrophilic relatives have been identified, suggesting that aci- green and red algae, suggesting the existence of common dophilic algae evolved from their respective neutrophilic ances- mechanisms in the adaptation to acidic environments. tors multiple times independently (6). However, it is largely unknown how several lineages of algae have successfully adapted Author contributions: S. Hirooka and S.-y.M. designed research; S. Hirooka, Y.H., Y.K., to their acidic environments. S. Higuchi, T.F., R. Onuma, A.E., and S.-y.M. performed research; R. Ohbayashi, A.U., Thus, far, the genomes of three related thermo-acidophilic red H.N., and H.Y. contributed new reagents/analytic tools; S. Hirooka, Y.H., Y.K., and S.-y.M. algae, Cyanidioschyzon merolae (7), Galdieria sulphuraria (8), and analyzed data; and S. Hirooka and S.-y.M. wrote the paper. Galdieria phlegrea (9), have been sequenced (all belong to the The authors declare no conflict of interest. cyanidialean red algae, which inhabit sulfuric hot springs worldwide This article is a PNAS Direct Submission. and grow optimally at 40–45 °C and pH 2–3). Genomic analyses Data deposition: The sequences reported in this paper have been deposited in DNA Data showed that horizontal gene transfer (HGT) from environmental Bank of Japan/European Molecular Biology Laboratory-European Bioinformatics Institute/ GenBank under the accession codes PRJDB5468, PRJDB6154, and PRJDB6155. prokaryotes, the expansion of gene families, and the loss of genes 1To whom correspondence may be addressed. Email: [email protected] or smiyagis@nig. have probably played important roles in the adaptation of Cyani- ac.jp. diales to acidic and high-temperature environments (8). Through This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. HGT, cyanidialean red algae acquired arsenical-resistance efflux 1073/pnas.1707072114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1707072114 PNAS Early Edition | 1of10 Downloaded by guest on September 28, 2021 A Acid mine drainage protonema of moss stramenopile green algae acidophilic moss euglenid bacteria amoeba 1 cm B concentrations (mg/L) pH Fe2+ Fe3+ Al3+ Mn2+ Cu2+ Zn2+ Na+ K+ 2.13 59.4 143.5 35.1 0.5 0.3 0.1 8.3 4.4 2+ 2+ 2- - + - 3- Fig. 1. Habitat, taxonomic position, and physiological temp. (°C) Mg Ca SO4 Cl NH4 NO3 PO4 H2SiO3 14.5 9.3 31.9 1155 3.4 0.4 0.08 1.6 90.6 features of the acidophilic green alga C. eustigma. (A) The algae inhabiting AMD in Yokote, Nagano Pre- CDML/BI fecture, Japan, and confirmation of the existence of C. eustigma C. reinhardtii 0.2 100/1.00 Volvox carteri C. eustigma. Algae were found predominantly in as- substitutions/site μ 100/1.00 Chlamydomonas reinhardtii sociation with acidophilic mosses. (Scale bars: 10 m.) 99/1.00 Chlamydomonas eustigma (B) pH, temperature, and concentrations of some ions in the AMD. (C)CellsofC. eustigma NIES-2499 (Left) 59/0.95 Stigeoclonium helveticum Chlorophyceae and C. reinhardtii 137c mt+ (Right). (Scale bar: 10 μm.) Pseudendoclonium akinetum 75/1.00 (D) A phylogenetic tree of green and red algae based Oltmannsiellopsis viridis -/0.95 on the concatenated datasets (21 taxa, 11,367 sites) of Chlorella valiaviris E -/- Ulvophyceae five chloroplast protein-coding genes (atpB, psaA, psaB, 1 2 3 4 5 6 7 8 (pH) Chlorella vulgaris psbC,andrbcL) and chloroplast ribosomal DNA se- C. eustigma 100/1.00 Chlorophyta quence (16S and 23S). The maximum likelihood (ML) 100/1.00 Coccomyxa subellipsoidea 99/1.00 Paradoxia multiseta (RaxML 8.0.0) and Bayesian (MrBayes 3.2.6) analyses C. reinhardtii 63/1.00 were calculated under separate model conditions. Nephroselmis olivacea Trebouxiophyceae Bootstrap values (BP) >50% obtained by ML and Nephroselmis astigmatica Bayesian posterior probabilities (BI) >0.95 obtained by F 100/1.00 73/1.00 Micromonas commoda 1.6 Bayesian analysis (MrBayes 3.2.6) are shown above the C. eustigma 100/1.00 Ostreococcus tauri ) 1.4 branches. The branch lengths reflect the evolutionary -1 C. reinhardtii 99/1.00 Prasinophyceae 1.2 Arabidopsis thaliana distances indicated by the scale bar. Filled red circles on 1.0 Klebsormidium flaccidum the right indicate organisms for which genomes have 0.8 Mesostigma viride been sequenced thus far. (E) C. eustigma and C. rein- 83/1.00 0.6 Streptophyta hardtii were cultured for 1 d in the same photoauto- 67/1.00 Cyanidium caldarium 0.4 Cyanidioschyzon merolae trophic medium at a series of pH. (F) Growth rates of Growth rate μ (d 100/1.00 C. eustigma and C. reinhardtii basedontheincreasein 0.2 Galdieria sulphuraria 0 Rhodophyta the cell number at the indicated pH. The error bars Cyanophora paradoxa 1 2 3 4 5 6 7 8 (pH) Glaucophyta represent the SD of three biological replicates.
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