Gene Responses to Oxygen Availability in Kluyveromyces lactis: an Insight on the Evolution of the Oxygen-Responding System in Yeast
The whole-genome duplication (WGD) may provide a basis for the emergence of the very characteristic life style of Saccharomyces cerevisiae—its fermentation-oriented physiology and its capacity of growing in anaerobiosis. Indeed, we found an over-representation of oxygen-responding genes in the ohnol...
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| creator | Fang, Zi-An Wang, Guang-Hui Chen, Ai-Lian Li, You-Fang Liu, Jian-Ping Li, Yu-Yang Bolotin-Fukuhara, Monique Bao, Wei-Guo |
| description | The whole-genome duplication (WGD) may provide a basis for the emergence of the very characteristic life style of Saccharomyces cerevisiae—its fermentation-oriented physiology and its capacity of growing in anaerobiosis. Indeed, we found an over-representation of oxygen-responding genes in the ohnologs of S. cerevisiae. Many of these duplicated genes are present as aerobic/hypoxic(anaerobic) pairs and form a specialized system responding to changing oxygen availability. HYP2/ANB1 and COX5A/COX5B are such gene pairs, and their unique orthologs in the ‘non-WGD’ Kluyveromyces lactis genome behaved like the aerobic versions of S. cerevisiae. ROX1 encodes a major oxygen-responding regulator in S. cerevisiae. The synteny, structural features and molecular function of putative KlROX1 were shown to be different from that of ROX1. The transition from the K. lactis-type ROX1 to the S. cerevisiae-type ROX1 could link up with the development of anaerobes in the yeast evolution. Bioinformatics and stochastic analyses of the Rox1p-binding site (YYYATTGTTCTC) in the upstream sequences of the S. cerevisiae Rox1p-mediated genes and of the K. lactis orthologs also indicated that K. lactis lacks the specific gene system responding to oxygen limiting environment, which is present in the ‘post-WGD’ genome of S. cerevisiae. These data suggested that the oxygen-responding system was born for the specialized physiology of S. cerevisiae. |
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Indeed, we found an over-representation of oxygen-responding genes in the ohnologs of S. cerevisiae. Many of these duplicated genes are present as aerobic/hypoxic(anaerobic) pairs and form a specialized system responding to changing oxygen availability. HYP2/ANB1 and COX5A/COX5B are such gene pairs, and their unique orthologs in the ‘non-WGD’ Kluyveromyces lactis genome behaved like the aerobic versions of S. cerevisiae. ROX1 encodes a major oxygen-responding regulator in S. cerevisiae. The synteny, structural features and molecular function of putative KlROX1 were shown to be different from that of ROX1. The transition from the K. lactis-type ROX1 to the S. cerevisiae-type ROX1 could link up with the development of anaerobes in the yeast evolution. Bioinformatics and stochastic analyses of the Rox1p-binding site (YYYATTGTTCTC) in the upstream sequences of the S. cerevisiae Rox1p-mediated genes and of the K. lactis orthologs also indicated that K. lactis lacks the specific gene system responding to oxygen limiting environment, which is present in the ‘post-WGD’ genome of S. cerevisiae. These data suggested that the oxygen-responding system was born for the specialized physiology of S. cerevisiae.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0007561</identifier><identifier>PMID: 19855843</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>aerobic conditions ; Amino Acid Sequence ; Anaerobes ; Anaerobiosis ; Analysis ; Baking yeast ; Base Sequence ; Binding sites ; Biochemistry, Molecular Biology ; Bioinformatics ; Biosynthesis ; Cloning ; Cloning, Molecular ; Computational Biology ; Computational Biology - methods ; dissolved oxygen ; Evolution ; Fermentation ; Gene duplication ; Gene expression ; gene expression regulation ; Gene Expression Regulation, Fungal ; Gene sequencing ; Genes ; Genetic engineering ; Genetics and Genomics ; Genome, Fungal ; Genomes ; Genomics ; Hypoxia ; KlROX1 gene ; Kluyveromyces ; Kluyveromyces - genetics ; Kluyveromyces - metabolism ; Kluyveromyces lactis ; Kluyveromyces marxianus var. lactis ; Laboratories ; Life Sciences ; Metabolism ; microbial genetics ; Microbiology and Parasitology ; Microbiology/Microbial Evolution and Genomics ; Microbiology/Microbial Physiology and Metabolism ; Models, Biological ; Molecular Sequence Data ; Oxygen ; Oxygen - chemistry ; Oxygen - metabolism ; Physiological aspects ; Physiology ; Reproduction (copying) ; ROX1 gene ; Saccharomyces ; Saccharomyces cerevisiae ; Saccharomyces cerevisiae - genetics ; Saccharomyces cerevisiae - metabolism ; Sequence Homology, Amino Acid ; species differences ; Stochastic Processes ; Stochasticity ; Synteny ; Yeast ; Yeasts</subject><ispartof>PloS one, 2009-10, Vol.4 (10), p.e7561-e7561</ispartof><rights>COPYRIGHT 2009 Public Library of Science</rights><rights>2009 Fang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>Fang et al. 2009</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c783t-e54afe6434004f7871080970787412b2aefc2e8e96070e19faaaa3cd2e6489e83</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2763219/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2763219/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2095,2914,23846,27903,27904,53770,53772,79347,79348</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19855843$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-00529207$$DView record in HAL$$Hfree_for_read</backlink></links><search><contributor>Davis, Dana</contributor><creatorcontrib>Fang, Zi-An</creatorcontrib><creatorcontrib>Wang, Guang-Hui</creatorcontrib><creatorcontrib>Chen, Ai-Lian</creatorcontrib><creatorcontrib>Li, You-Fang</creatorcontrib><creatorcontrib>Liu, Jian-Ping</creatorcontrib><creatorcontrib>Li, Yu-Yang</creatorcontrib><creatorcontrib>Bolotin-Fukuhara, Monique</creatorcontrib><creatorcontrib>Bao, Wei-Guo</creatorcontrib><title>Gene Responses to Oxygen Availability in Kluyveromyces lactis: an Insight on the Evolution of the Oxygen-Responding System in Yeast</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The whole-genome duplication (WGD) may provide a basis for the emergence of the very characteristic life style of Saccharomyces cerevisiae—its fermentation-oriented physiology and its capacity of growing in anaerobiosis. Indeed, we found an over-representation of oxygen-responding genes in the ohnologs of S. cerevisiae. Many of these duplicated genes are present as aerobic/hypoxic(anaerobic) pairs and form a specialized system responding to changing oxygen availability. HYP2/ANB1 and COX5A/COX5B are such gene pairs, and their unique orthologs in the ‘non-WGD’ Kluyveromyces lactis genome behaved like the aerobic versions of S. cerevisiae. ROX1 encodes a major oxygen-responding regulator in S. cerevisiae. The synteny, structural features and molecular function of putative KlROX1 were shown to be different from that of ROX1. The transition from the K. lactis-type ROX1 to the S. cerevisiae-type ROX1 could link up with the development of anaerobes in the yeast evolution. Bioinformatics and stochastic analyses of the Rox1p-binding site (YYYATTGTTCTC) in the upstream sequences of the S. cerevisiae Rox1p-mediated genes and of the K. lactis orthologs also indicated that K. lactis lacks the specific gene system responding to oxygen limiting environment, which is present in the ‘post-WGD’ genome of S. cerevisiae. These data suggested that the oxygen-responding system was born for the specialized physiology of S. cerevisiae.</description><subject>aerobic conditions</subject><subject>Amino Acid Sequence</subject><subject>Anaerobes</subject><subject>Anaerobiosis</subject><subject>Analysis</subject><subject>Baking yeast</subject><subject>Base Sequence</subject><subject>Binding sites</subject><subject>Biochemistry, Molecular Biology</subject><subject>Bioinformatics</subject><subject>Biosynthesis</subject><subject>Cloning</subject><subject>Cloning, Molecular</subject><subject>Computational Biology</subject><subject>Computational Biology - methods</subject><subject>dissolved oxygen</subject><subject>Evolution</subject><subject>Fermentation</subject><subject>Gene duplication</subject><subject>Gene expression</subject><subject>gene expression regulation</subject><subject>Gene Expression Regulation, Fungal</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Genetic engineering</subject><subject>Genetics and Genomics</subject><subject>Genome, Fungal</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Hypoxia</subject><subject>KlROX1 gene</subject><subject>Kluyveromyces</subject><subject>Kluyveromyces - genetics</subject><subject>Kluyveromyces - metabolism</subject><subject>Kluyveromyces lactis</subject><subject>Kluyveromyces marxianus var. lactis</subject><subject>Laboratories</subject><subject>Life Sciences</subject><subject>Metabolism</subject><subject>microbial genetics</subject><subject>Microbiology and Parasitology</subject><subject>Microbiology/Microbial Evolution and Genomics</subject><subject>Microbiology/Microbial Physiology and Metabolism</subject><subject>Models, Biological</subject><subject>Molecular Sequence Data</subject><subject>Oxygen</subject><subject>Oxygen - chemistry</subject><subject>Oxygen - metabolism</subject><subject>Physiological aspects</subject><subject>Physiology</subject><subject>Reproduction (copying)</subject><subject>ROX1 gene</subject><subject>Saccharomyces</subject><subject>Saccharomyces cerevisiae</subject><subject>Saccharomyces cerevisiae - genetics</subject><subject>Saccharomyces cerevisiae - metabolism</subject><subject>Sequence Homology, Amino Acid</subject><subject>species differences</subject><subject>Stochastic 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Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fang, Zi-An</au><au>Wang, Guang-Hui</au><au>Chen, Ai-Lian</au><au>Li, You-Fang</au><au>Liu, Jian-Ping</au><au>Li, Yu-Yang</au><au>Bolotin-Fukuhara, Monique</au><au>Bao, Wei-Guo</au><au>Davis, Dana</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Gene Responses to Oxygen Availability in Kluyveromyces lactis: an Insight on the Evolution of the Oxygen-Responding System in Yeast</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2009-10-26</date><risdate>2009</risdate><volume>4</volume><issue>10</issue><spage>e7561</spage><epage>e7561</epage><pages>e7561-e7561</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The whole-genome duplication (WGD) may provide a basis for the emergence of the very characteristic life style of Saccharomyces cerevisiae—its fermentation-oriented physiology and its capacity of growing in anaerobiosis. Indeed, we found an over-representation of oxygen-responding genes in the ohnologs of S. cerevisiae. Many of these duplicated genes are present as aerobic/hypoxic(anaerobic) pairs and form a specialized system responding to changing oxygen availability. HYP2/ANB1 and COX5A/COX5B are such gene pairs, and their unique orthologs in the ‘non-WGD’ Kluyveromyces lactis genome behaved like the aerobic versions of S. cerevisiae. ROX1 encodes a major oxygen-responding regulator in S. cerevisiae. The synteny, structural features and molecular function of putative KlROX1 were shown to be different from that of ROX1. The transition from the K. lactis-type ROX1 to the S. cerevisiae-type ROX1 could link up with the development of anaerobes in the yeast evolution. Bioinformatics and stochastic analyses of the Rox1p-binding site (YYYATTGTTCTC) in the upstream sequences of the S. cerevisiae Rox1p-mediated genes and of the K. lactis orthologs also indicated that K. lactis lacks the specific gene system responding to oxygen limiting environment, which is present in the ‘post-WGD’ genome of S. cerevisiae. These data suggested that the oxygen-responding system was born for the specialized physiology of S. cerevisiae.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>19855843</pmid><doi>10.1371/journal.pone.0007561</doi><tpages>e7561</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2009-10, Vol.4 (10), p.e7561-e7561 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1292131978 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS); EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | aerobic conditions Amino Acid Sequence Anaerobes Anaerobiosis Analysis Baking yeast Base Sequence Binding sites Biochemistry, Molecular Biology Bioinformatics Biosynthesis Cloning Cloning, Molecular Computational Biology Computational Biology - methods dissolved oxygen Evolution Fermentation Gene duplication Gene expression gene expression regulation Gene Expression Regulation, Fungal Gene sequencing Genes Genetic engineering Genetics and Genomics Genome, Fungal Genomes Genomics Hypoxia KlROX1 gene Kluyveromyces Kluyveromyces - genetics Kluyveromyces - metabolism Kluyveromyces lactis Kluyveromyces marxianus var. lactis Laboratories Life Sciences Metabolism microbial genetics Microbiology and Parasitology Microbiology/Microbial Evolution and Genomics Microbiology/Microbial Physiology and Metabolism Models, Biological Molecular Sequence Data Oxygen Oxygen - chemistry Oxygen - metabolism Physiological aspects Physiology Reproduction (copying) ROX1 gene Saccharomyces Saccharomyces cerevisiae Saccharomyces cerevisiae - genetics Saccharomyces cerevisiae - metabolism Sequence Homology, Amino Acid species differences Stochastic Processes Stochasticity Synteny Yeast Yeasts |
| title | Gene Responses to Oxygen Availability in Kluyveromyces lactis: an Insight on the Evolution of the Oxygen-Responding System in Yeast |
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