Adaptation of the glycerol-3-phosphate dehydrogenase Gpd1 to high salinities in the extremely halotolerant Hortaea werneckii and halophilic Wallemia ichthyophaga

Fungal Biology - Tập 115 - Trang 959-970 - 2011
Metka Lenassi1,2, Janja Zajc3, Cene Gostinčar2, Alenka Gorjan1, Nina Gunde-Cimerman3,2, Ana Plemenitaš1
1Institute of Biochemistry, Faculty of Medicine, University of Ljubljana, Vrazov trg 2, SI-1000, Ljubljana, Slovenia
2Centre of Excellence for Integrated Approaches in Chemistry and Biology of Proteins (CIPKeBiP), Jamova 39, SI-1000 Ljubljana, Slovenia
3Department of Biology, Biotechnical Faculty, University of Ljubljana, Večna pot 111, SI-1000 Ljubljana, Slovenia

Tài liệu tham khảo

Albertyn, 1994, GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway, Molecular and Cellular Biology, 14, 4135, 10.1128/MCB.14.6.4135 Altschul, 1997, Gapped BLAST and PSI-BLAST: a new generation of protein database search programs, Nucleic Acids Research, 25, 3389, 10.1093/nar/25.17.3389 Andre, 1991, Osmoregulation in Saccharomyces cerevisiae. Studies on the osmotic induction of glycerol production and glycerol-3-phosphate dehydrogenase (NAD+), FEBS Letters, 286, 13, 10.1016/0014-5793(91)80930-2 Anisimova, 2006, Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative, Systematic Biology, 55, 539, 10.1080/10635150600755453 Ansell, 1997, The two isoenzymes for yeast NAD+-dependent glycerol 3-phosphate dehydrogenase encoded by GPD1 and GPD2 have distinct roles in osmoadaptation and redox regulation, EMBO Journal, 16, 2179, 10.1093/emboj/16.9.2179 Anton, 2000, Extremely halophilic bacteria in crystallizer ponds from solar salterns, Applied and Environmental Microbiology, 66, 3052, 10.1128/AEM.66.7.3052-3057.2000 Berrada, 2002, Purification and characterization of cytosolic glycerol-3-phosphate dehydrogenase from skeletal muscle of jerboa (Jaculus orientalis), Molecular and Cellular Biochemistry, 231, 117, 10.1023/A:1014464831573 Blomberg, 1989, Roles of glycerol and glycerol-3-phosphate dehydrogenase (NAD+) in acquired osmotolerance of Saccharomyces cerevisiae, Journal of Bacteriology, 171, 1087, 10.1128/jb.171.2.1087-1092.1989 Chen, 2008, Cloning and characterization of a NAD+-dependent glycerol-3-phosphate dehydrogenase gene from Candida glycerinogenes, an industrial glycerol producer, FEMS Yeast Research, 8, 725, 10.1111/j.1567-1364.2008.00382.x Chenna, 2003, Multiple sequence alignment with the Clustal series of programs, Nucleic Acids Research, 31, 3497, 10.1093/nar/gkg500 Daum, 1998, Biochemistry, cell biology and molecular biology of lipids of Saccharomyces cerevisiae, Yeast, 14, 1471, 10.1002/(SICI)1097-0061(199812)14:16<1471::AID-YEA353>3.0.CO;2-Y DeLuna, 2010, Need-based up-regulation of protein levels in response to deletion of their duplicate genes, PLoS Biology, 8, e1000347, 10.1371/journal.pbio.1000347 Eriksson, 1995, Cloning and characterization of GPD2, a second gene encoding sn-glycerol 3-phosphate dehydrogenase (NAD+) in Saccharomyces cerevisiae, and its comparison with GPD1, Molecular Microbiology, 17, 95, 10.1111/j.1365-2958.1995.mmi_17010095.x Fillinger, 2001, Molecular and physiological characterization of the NAD-dependent glycerol 3-phosphate dehydrogenase in the filamentous fungus Aspergillus nidulans, Molecular Microbiology, 39, 145, 10.1046/j.1365-2958.2001.02223.x Furukawa, 2007, Novel reporter gene expression systems for monitoring activation of the Aspergillus nidulans HOG pathway, Bioscience, Biotechnology, and Biochemistry, 71, 1724, 10.1271/bbb.70131 Gorjan, 2006, Identification and characterization of ENA ATPases HwENA1 and HwENA2 from the halophilic black yeast Hortaea werneckii, FEMS Microbiology Letters, 265, 41, 10.1111/j.1574-6968.2006.00473.x Gostinčar, 2009, The expressions of Delta 9-, Delta 12-desaturases and an elongase by the extremely halotolerant black yeast Hortaea werneckii are salt dependent, FEMS Yeast Research, 9, 247, 10.1111/j.1567-1364.2009.00481.x Guindon, 2003, A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood, Systematic Biology, 52, 696, 10.1080/10635150390235520 Gunde-Cimerman, 2006, Ecology and molecular adaptations of the halophilic black yeast Hortaea werneckii, Reviews in Environmental Science and Biotechnology, 5, 323, 10.1007/s11157-006-9105-0 Gunde-Cimerman, 2000, Hypersaline waters in salterns – natural ecological niches for halophilic black yeasts, FEMS Microbiology Ecology, 32, 235 Hohmann, 2002, Osmotic stress signaling and osmoadaptation in yeasts, Microbiology and Molecular Biology Reviews, 66, 300, 10.1128/MMBR.66.2.300-372.2002 Huelsenbeck, 2001, MrBayes: Bayesian inference of phylogenetic trees, Bioinformatics, 17, 754, 10.1093/bioinformatics/17.8.754 Jung, 2010, Dynamic changes in the subcellular distribution of Gpd1p in response to cell stress, Journal of Biological Chemistry, 285, 6739, 10.1074/jbc.M109.058552 Katoh, 2005, MAFFT version 5: improvement in accuracy of multiple sequence alignment, Nucleic Acids Research, 33, 511, 10.1093/nar/gki198 Katoh, 2008, Recent developments in the MAFFT multiple sequence alignment program, Briefings in Bioinformatics, 9, 286, 10.1093/bib/bbn013 Kogej, 2007, Osmotic adaptation of the halophilic fungus Hortaea werneckii: role of osmolytes and melanization, Microbiology, 153, 4261, 10.1099/mic.0.2007/010751-0 Kondrashov, 2002, Selection in the evolution of gene duplications, Genome Biology, 3, 10.1186/gb-2002-3-2-research0008 Kralj Kunčič, 2010, Morphological response of the halophilic fungal genus Wallemia to high salinity, Applied and Environmental Microbiology, 76, 329, 10.1128/AEM.02318-09 Lanišnik Rižner, 1999, A novel 17beta-hydroxysteroid dehydrogenase in the fungus Cochliobolus lunatus: new insights into the evolution of steroid-hormone signalling, Biochemical Journal, 337, 425, 10.1042/0264-6021:3370425 Larsson, 1990, Osmoregulation of the salt-tolerant yeast Debaryomyces hansenii grown in a chemostat at different salinities, Journal of Bacteriology, 172, 1769, 10.1128/jb.172.4.1769-1774.1990 Lee, 2008, Cloning and characterization of CmGPD1, the Candida magnoliae homologue of glycerol-3-phosphate dehydrogenase, FEMS Yeast Research, 8, 1324, 10.1111/j.1567-1364.2008.00446.x Lenassi, 2007, Novel group VII histidine kinase HwHhk7B from the halophilic fungi Hortaea werneckii has a putative role in osmosensing, Current Genetics, 51, 393, 10.1007/s00294-007-0131-4 Lenassi, 2007, The MAP kinase HwHog1 from the halophilic black yeast Hortaea werneckii: coping with stresses in solar salterns, Saline Systems, 3, 3, 10.1186/1746-1448-3-3 Nevoigt, 1996, Reduced pyruvate decarboxylase and increased glycerol-3-phosphate dehydrogenase [NAD+] levels enhance glycerol production in Saccharomyces cerevisiae, Yeast, 12, 1331, 10.1002/(SICI)1097-0061(199610)12:13<1331::AID-YEA28>3.0.CO;2-0 Nevoigt, 1997, Osmoregulation and glycerol metabolism in the yeast Saccharomyces cerevisiae, FEMS Microbiology Reviews, 21, 231, 10.1111/j.1574-6976.1997.tb00352.x Norbeck, 1997, Metabolic and regulatory changes associated with growth of Saccharomyces cerevisiae in 1.4M NaCl. Evidence for osmotic induction of glycerol dissimilation via the dihydroxyacetone pathway, Journal of Biological Chemistry, 272, 5544, 10.1074/jbc.272.9.5544 Norbeck, 1996, Journal of Biological Chemistry, 271, 13875, 10.1074/jbc.271.23.13875 Ou, 2006, Crystal structures of human glycerol 3-phosphate dehydrogenase 1 (GPD1), Journal of Molecular Biology, 357, 858, 10.1016/j.jmb.2005.12.074 Peng, 2010, Cloning and characterization of a glycerol-3-phosphate dehydrogenase (NAD+) gene from the halotolerant yeast Pichia farinosa, Yeast, 27, 115 Petrovič, 2002, Cellular responses to environmental salinity in the halophilic black yeast Hortaea werneckii, Molecular Microbiology, 45, 665, 10.1046/j.1365-2958.2002.03021.x Rambaut A, Drummond A, 2007. Tracer v1.4, http://beast.bio.ed.ac.uk/. Remize, 1999, Glycerol overproduction by engineered Saccharomyces cerevisiae wine yeast strains leads to substantial changes in by-product formation and to a stimulation of fermentation rate in stationary phase, Applied and Environmental Microbiology, 65, 143, 10.1128/AEM.65.1.143-149.1999 Rep, 1999, Different signalling pathways contribute to the control of GPD1 gene expression by osmotic stress in Saccharomyces cerevisiae, Microbiology, 145, 715, 10.1099/13500872-145-3-715 Ronquist, 2003, MrBayes 3: Bayesian phylogenetic inference under mixed models, Bioinformatics, 19, 1572, 10.1093/bioinformatics/btg180 Rozman, 1994, Isolation of genomic DNA from filamentous fungi with high glucan level, Biotechniques, 16, 382 Thome, 2004, Isolation of a GPD gene from Debaryomyces hansenii encoding a glycerol 3-phosphate dehydrogenase (NAD+), Yeast, 21, 119, 10.1002/yea.1070 Turk, 2002, The HOG pathway in the halophilic black yeast Hortaea werneckii: isolation of the HOG1 homolog gene and activation of HwHog1p, FEMS Microbiology Letters, 216, 193, 10.1111/j.1574-6968.2002.tb11435.x Valadi, 2004, Distinct intracellular localization of Gpd1p and Gpd2p, the two yeast isoforms of NAD+-dependent glycerol-3-phosphate dehydrogenase, explains their different contributions to redox-driven glycerol production, Journal of Biological Chemistry, 279, 39677, 10.1074/jbc.M403310200 Vaupotič, 2007, Novel 3′-phosphoadenosine-5′-phosphatases from extremely halotolerant Hortaea werneckii reveal insight into molecular determinants of salt tolerance of black yeasts, Fungal Genetics and Biology, 44, 1109, 10.1016/j.fgb.2007.02.005 Vaupotič, 2007, Differential gene expression and Hog1 interaction with osmoresponsive genes in the extremely halotolerant black yeast Hortaea werneckii, BMC Genomics, 8, 280, 10.1186/1471-2164-8-280 Watanabe, 2008, Expression of glycerol 3-phosphate dehydrogenase gene (CvGPD1) in salt-tolerant yeast Candida versatilis is stimulated by high concentrations of NaCl, Yeast, 25, 107, 10.1002/yea.1550 Whelan, 2001, A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach, Molecular Biology and Evolution, 18, 691, 10.1093/oxfordjournals.molbev.a003851 Yale, 2001, Transcript expression in Saccharomyces cerevisiae at high salinity, Journal of Biological Chemistry, 276, 15996, 10.1074/jbc.M008209200 Yan, 2008, Glycerol accumulation in the dimorphic yeast Saccharomycopsis fibuligera: cloning of two glycerol 3-phosphate dehydrogenase genes, one of which is markedly induced by osmotic stress, Yeast, 25, 609, 10.1002/yea.1606 Zalar, 2005, Taxonomy and phylogeny of the xerophilic genus Wallemia (Wallemiomycetes and Wallemiales, cl. et ord. nov.), Antonie Van Leeuwenhoek, 87, 311, 10.1007/s10482-004-6783-x Zdobnov, 2001, InterProScan – an integration platform for the signature-recognition methods in InterPro, Bioinformatics, 17, 847, 10.1093/bioinformatics/17.9.847