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      Acidophilic green algal genome provides insights into adaptation to an acidic environment

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          Significance

          Extremely acidic environments are scattered worldwide, and their ecosystems are supported by acidophilic microalgae as primary producers. To understand how acidophilic algae evolved from their respective neutrophilic ancestors, we determined the draft genome sequence of the acidophilic green alga Chlamydomonas eustigma and performed comparative genome analyses between C. eustigma and its neutrophilic relative Chlamydomonas reinhardtii. The results suggest that higher expression of heat-shock proteins and H +-ATPase, loss of some metabolic pathways that acidify cytosol, and acquisition of metal-detoxifying genes by horizontal gene transfer have played important roles in the adaptation to acidic environments. These features are also found in other acidophilic green and red algae, suggesting the existence of common mechanisms in the adaptation to acidic environments.

          Abstract

          Some microalgae are adapted to extremely acidic environments in which toxic metals are present at high levels. However, little is known about how acidophilic algae evolved from their respective neutrophilic ancestors by adapting to particular acidic environments. To gain insights into this issue, we determined the draft genome sequence of the acidophilic green alga Chlamydomonas eustigma and performed comparative genome and transcriptome analyses between C. eustigma and its neutrophilic relative Chlamydomonas reinhardtii. The results revealed the following features in C. eustigma that probably contributed to the adaptation to an acidic environment. Genes encoding heat-shock proteins and plasma membrane H +-ATPase are highly expressed in C. eustigma. This species has also lost fermentation pathways that acidify the cytosol and has acquired an energy shuttle and buffering system and arsenic detoxification genes through horizontal gene transfer. Moreover, the arsenic detoxification genes have been multiplied in the genome. These features have also been found in other acidophilic green and red algae, suggesting the existence of common mechanisms in the adaptation to acidic environments.

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          Most cited references50

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          BLAT---The BLAST-Like Alignment Tool

          W. J. Kent (2002)
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            Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D.

            Small, compact genomes of ultrasmall unicellular algae provide information on the basic and essential genes that support the lives of photosynthetic eukaryotes, including higher plants. Here we report the 16,520,305-base-pair sequence of the 20 chromosomes of the unicellular red alga Cyanidioschyzon merolae 10D as the first complete algal genome. We identified 5,331 genes in total, of which at least 86.3% were expressed. Unique characteristics of this genomic structure include: a lack of introns in all but 26 genes; only three copies of ribosomal DNA units that maintain the nucleolus; and two dynamin genes that are involved only in the division of mitochondria and plastids. The conserved mosaic origin of Calvin cycle enzymes in this red alga and in green plants supports the hypothesis of the existence of single primary plastid endosymbiosis. The lack of a myosin gene, in addition to the unexpressed actin gene, suggests a simpler system of cytokinesis. These results indicate that the C. merolae genome provides a model system with a simple gene composition for studying the origin, evolution and fundamental mechanisms of eukaryotic cells.
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              Arsenic speciation in the environment

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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                26 September 2017
                11 September 2017
                : 114
                : 39
                : E8304-E8313
                Affiliations
                [1] aDepartment of Cell Genetics, National Institute of Genetics , Shizuoka 411-8540, Japan;
                [2] bCore Research for Evolutional Science and Technology, Japan Science and Technology Agency , Saitama 332-0012, Japan;
                [3] cDepartment of Environmental and Life Sciences, Toyohashi University of Technology , Aichi 441-8580, Japan;
                [4] dNODAI Genome Research Center, Tokyo University of Agriculture , Tokyo 156-8502, Japan;
                [5] eResearch Group for Aquatic Plants Restoration in Lake Nojiri, Nojiriko Museum , Nagano 389-1303, Japan;
                [6] fDepartment of Genetics, Graduate University for Advanced Studies , Shizuoka 411-8540, Japan;
                [7] gDepartment of Biological Sciences, Graduate School of Science, University of Tokyo , Tokyo 113-0033, Japan;
                [8] hDepartment of Bioscience, Tokyo University of Agriculture , Tokyo 156-8502, Japan
                Author notes
                1To whom correspondence may be addressed. Email: shirooka@ 123456nig.ac.jp or smiyagis@ 123456nig.ac.jp .

                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)

                Author contributions: S. Hirooka and S.-y.M. designed research; S. Hirooka, Y.H., Y.K., S. Higuchi, T.F., R. Onuma, A.E., and S.-y.M. performed research; R. Ohbayashi, A.U., H.N., and H.Y. contributed new reagents/analytic tools; S. Hirooka, Y.H., Y.K., and S.-y.M. analyzed data; and S. Hirooka and S.-y.M. wrote the paper.

                Article
                PMC5625915 PMC5625915 5625915 201707072
                10.1073/pnas.1707072114
                5625915
                28893987
                d0640cc9-6f67-42e7-be5b-fe2954004e4e
                History
                Page count
                Pages: 10
                Categories
                PNAS Plus
                Biological Sciences
                Plant Biology
                PNAS Plus

                comparative transcriptomics,environmental adaptation,acidic environment,acidophilic alga,comparative genomics

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