Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote

The ciliate Tetrahymena thermophila is a model organism for molecular and cellular biology. Like other ciliates, this species has separate germline and soma functions that are embodied by distinct nuclei within a single cell. The germline-like micronucleus (MIC) has its genome held in reserve for se...

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Published in:PLoS biology 2006-09, Vol.4 (9), p.e286-e286
Main Authors: Eisen, Jonathan A, Coyne, Robert S, Wu, Martin, Wu, Dongying, Thiagarajan, Mathangi, Wortman, Jennifer R, Badger, Jonathan H, Ren, Qinghu, Amedeo, Paolo, Jones, Kristie M, Tallon, Luke J, Delcher, Arthur L, Salzberg, Steven L, Silva, Joana C, Haas, Brian J, Majoros, William H, Farzad, Maryam, Carlton, Jane M, Smith, Jr, Roger K, Garg, Jyoti, Pearlman, Ronald E, Karrer, Kathleen M, Sun, Lei, Manning, Gerard, Elde, Nels C, Turkewitz, Aaron P, Asai, David J, Wilkes, David E, Wang, Yufeng, Cai, Hong, Collins, Kathleen, Stewart, B Andrew, Lee, Suzanne R, Wilamowska, Katarzyna, Weinberg, Zasha, Ruzzo, Walter L, Wloga, Dorota, Gaertig, Jacek, Frankel, Joseph, Tsao, Che-Chia, Gorovsky, Martin A, Keeling, Patrick J, Waller, Ross F, Patron, Nicola J, Cherry, J Michael, Stover, Nicholas A, Krieger, Cynthia J, del Toro, Christina, Ryder, Hilary F, Williamson, Sondra C, Barbeau, Rebecca A, Hamilton, Eileen P, Orias, Eduardo
Format: Article
Language:English
Subjects:
Alveolates
Animals
Cells, Cultured
Chromosome Mapping - methods
Chromosomes
Databases, Genetic
Deoxyribonucleic acid
DNA
Eukaryotic Cells - physiology
Evolution, Molecular
Genetics
Genetics/Genomics/Gene Therapy
Genome, Protozoan
Genomes
Genomics
Macronucleus - genetics
Micronucleus, Germline - genetics
Microorganisms
Models, Animal
Models, Biological
Phylogenetics
Phylogeny
Signal Transduction
Tetrahymena thermophila
Tetrahymena thermophila - genetics
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cited_by cdi_FETCH-LOGICAL-c625t-445568fb8ee5696fc06c558b23c528a6c019bfe95e8c3ec226b3a46985fcdfc53
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container_end_page e286
container_issue 9
container_start_page e286
container_title PLoS biology
container_volume 4
creator Eisen, Jonathan A
Coyne, Robert S
Wu, Martin
Wu, Dongying
Thiagarajan, Mathangi
Wortman, Jennifer R
Badger, Jonathan H
Ren, Qinghu
Amedeo, Paolo
Jones, Kristie M
Tallon, Luke J
Delcher, Arthur L
Salzberg, Steven L
Silva, Joana C
Haas, Brian J
Majoros, William H
Farzad, Maryam
Carlton, Jane M
Smith, Jr, Roger K
Garg, Jyoti
Pearlman, Ronald E
Karrer, Kathleen M
Sun, Lei
Manning, Gerard
Elde, Nels C
Turkewitz, Aaron P
Asai, David J
Wilkes, David E
Wang, Yufeng
Cai, Hong
Collins, Kathleen
Stewart, B Andrew
Lee, Suzanne R
Wilamowska, Katarzyna
Weinberg, Zasha
Ruzzo, Walter L
Wloga, Dorota
Gaertig, Jacek
Frankel, Joseph
Tsao, Che-Chia
Gorovsky, Martin A
Keeling, Patrick J
Waller, Ross F
Patron, Nicola J
Cherry, J Michael
Stover, Nicholas A
Krieger, Cynthia J
del Toro, Christina
Ryder, Hilary F
Williamson, Sondra C
Barbeau, Rebecca A
Hamilton, Eileen P
Orias, Eduardo
description The ciliate Tetrahymena thermophila is a model organism for molecular and cellular biology. Like other ciliates, this species has separate germline and soma functions that are embodied by distinct nuclei within a single cell. The germline-like micronucleus (MIC) has its genome held in reserve for sexual reproduction. The soma-like macronucleus (MAC), which possesses a genome processed from that of the MIC, is the center of gene expression and does not directly contribute DNA to sexual progeny. We report here the shotgun sequencing, assembly, and analysis of the MAC genome of T. thermophila, which is approximately 104 Mb in length and composed of approximately 225 chromosomes. Overall, the gene set is robust, with more than 27,000 predicted protein-coding genes, 15,000 of which have strong matches to genes in other organisms. The functional diversity encoded by these genes is substantial and reflects the complexity of processes required for a free-living, predatory, single-celled organism. This is highlighted by the abundance of lineage-specific duplications of genes with predicted roles in sensing and responding to environmental conditions (e.g., kinases), using diverse resources (e.g., proteases and transporters), and generating structural complexity (e.g., kinesins and dyneins). In contrast to the other lineages of alveolates (apicomplexans and dinoflagellates), no compelling evidence could be found for plastid-derived genes in the genome. UGA, the only T. thermophila stop codon, is used in some genes to encode selenocysteine, thus making this organism the first known with the potential to translate all 64 codons in nuclear genes into amino acids. We present genomic evidence supporting the hypothesis that the excision of DNA from the MIC to generate the MAC specifically targets foreign DNA as a form of genome self-defense. The combination of the genome sequence, the functional diversity encoded therein, and the presence of some pathways missing from other model organisms makes T. thermophila an ideal model for functional genomic studies to address biological, biomedical, and biotechnological questions of fundamental importance.
doi_str_mv 10.1371/journal.pbio.0040286
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Like other ciliates, this species has separate germline and soma functions that are embodied by distinct nuclei within a single cell. The germline-like micronucleus (MIC) has its genome held in reserve for sexual reproduction. The soma-like macronucleus (MAC), which possesses a genome processed from that of the MIC, is the center of gene expression and does not directly contribute DNA to sexual progeny. We report here the shotgun sequencing, assembly, and analysis of the MAC genome of T. thermophila, which is approximately 104 Mb in length and composed of approximately 225 chromosomes. Overall, the gene set is robust, with more than 27,000 predicted protein-coding genes, 15,000 of which have strong matches to genes in other organisms. The functional diversity encoded by these genes is substantial and reflects the complexity of processes required for a free-living, predatory, single-celled organism. This is highlighted by the abundance of lineage-specific duplications of genes with predicted roles in sensing and responding to environmental conditions (e.g., kinases), using diverse resources (e.g., proteases and transporters), and generating structural complexity (e.g., kinesins and dyneins). In contrast to the other lineages of alveolates (apicomplexans and dinoflagellates), no compelling evidence could be found for plastid-derived genes in the genome. UGA, the only T. thermophila stop codon, is used in some genes to encode selenocysteine, thus making this organism the first known with the potential to translate all 64 codons in nuclear genes into amino acids. We present genomic evidence supporting the hypothesis that the excision of DNA from the MIC to generate the MAC specifically targets foreign DNA as a form of genome self-defense. 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This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Eisen JA, Coyne RS, Wu M, Wu D, Thiagarajan M, et al. (2006) Macronuclear Genome Sequence of the Ciliate Tetrahymena thermophila, a Model Eukaryote. 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Like other ciliates, this species has separate germline and soma functions that are embodied by distinct nuclei within a single cell. The germline-like micronucleus (MIC) has its genome held in reserve for sexual reproduction. The soma-like macronucleus (MAC), which possesses a genome processed from that of the MIC, is the center of gene expression and does not directly contribute DNA to sexual progeny. We report here the shotgun sequencing, assembly, and analysis of the MAC genome of T. thermophila, which is approximately 104 Mb in length and composed of approximately 225 chromosomes. Overall, the gene set is robust, with more than 27,000 predicted protein-coding genes, 15,000 of which have strong matches to genes in other organisms. The functional diversity encoded by these genes is substantial and reflects the complexity of processes required for a free-living, predatory, single-celled organism. This is highlighted by the abundance of lineage-specific duplications of genes with predicted roles in sensing and responding to environmental conditions (e.g., kinases), using diverse resources (e.g., proteases and transporters), and generating structural complexity (e.g., kinesins and dyneins). In contrast to the other lineages of alveolates (apicomplexans and dinoflagellates), no compelling evidence could be found for plastid-derived genes in the genome. UGA, the only T. thermophila stop codon, is used in some genes to encode selenocysteine, thus making this organism the first known with the potential to translate all 64 codons in nuclear genes into amino acids. We present genomic evidence supporting the hypothesis that the excision of DNA from the MIC to generate the MAC specifically targets foreign DNA as a form of genome self-defense. The combination of the genome sequence, the functional diversity encoded therein, and the presence of some pathways missing from other model organisms makes T. thermophila an ideal model for functional genomic studies to address biological, biomedical, and biotechnological questions of fundamental importance.</description><subject>Alveolates</subject><subject>Animals</subject><subject>Cells, Cultured</subject><subject>Chromosome Mapping - methods</subject><subject>Chromosomes</subject><subject>Databases, Genetic</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Eukaryotic Cells - physiology</subject><subject>Evolution, Molecular</subject><subject>Genetics</subject><subject>Genetics/Genomics/Gene Therapy</subject><subject>Genome, Protozoan</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Macronucleus - genetics</subject><subject>Micronucleus, Germline - genetics</subject><subject>Microorganisms</subject><subject>Models, 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genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote</title><author>Eisen, Jonathan A ; Coyne, Robert S ; Wu, Martin ; Wu, Dongying ; Thiagarajan, Mathangi ; Wortman, Jennifer R ; Badger, Jonathan H ; Ren, Qinghu ; Amedeo, Paolo ; Jones, Kristie M ; Tallon, Luke J ; Delcher, Arthur L ; Salzberg, Steven L ; Silva, Joana C ; Haas, Brian J ; Majoros, William H ; Farzad, Maryam ; Carlton, Jane M ; Smith, Jr, Roger K ; Garg, Jyoti ; Pearlman, Ronald E ; Karrer, Kathleen M ; Sun, Lei ; Manning, Gerard ; Elde, Nels C ; Turkewitz, Aaron P ; Asai, David J ; Wilkes, David E ; Wang, Yufeng ; Cai, Hong ; Collins, Kathleen ; Stewart, B Andrew ; Lee, Suzanne R ; Wilamowska, Katarzyna ; Weinberg, Zasha ; Ruzzo, Walter L ; Wloga, Dorota ; Gaertig, Jacek ; Frankel, Joseph ; Tsao, Che-Chia ; Gorovsky, Martin A ; Keeling, Patrick J ; Waller, Ross F ; Patron, Nicola J ; Cherry, J Michael ; Stover, Nicholas A ; Krieger, Cynthia J ; del Toro, Christina ; Ryder, Hilary F ; Williamson, Sondra C ; Barbeau, Rebecca A ; Hamilton, Eileen P ; Orias, Eduardo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c625t-445568fb8ee5696fc06c558b23c528a6c019bfe95e8c3ec226b3a46985fcdfc53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2006</creationdate><topic>Alveolates</topic><topic>Animals</topic><topic>Cells, Cultured</topic><topic>Chromosome Mapping - methods</topic><topic>Chromosomes</topic><topic>Databases, Genetic</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>Eukaryotic Cells - physiology</topic><topic>Evolution, Molecular</topic><topic>Genetics</topic><topic>Genetics/Genomics/Gene Therapy</topic><topic>Genome, Protozoan</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Macronucleus - genetics</topic><topic>Micronucleus, Germline - genetics</topic><topic>Microorganisms</topic><topic>Models, Animal</topic><topic>Models, Biological</topic><topic>Phylogenetics</topic><topic>Phylogeny</topic><topic>Signal Transduction</topic><topic>Tetrahymena thermophila</topic><topic>Tetrahymena thermophila - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Eisen, Jonathan A</creatorcontrib><creatorcontrib>Coyne, Robert S</creatorcontrib><creatorcontrib>Wu, Martin</creatorcontrib><creatorcontrib>Wu, Dongying</creatorcontrib><creatorcontrib>Thiagarajan, Mathangi</creatorcontrib><creatorcontrib>Wortman, Jennifer R</creatorcontrib><creatorcontrib>Badger, Jonathan H</creatorcontrib><creatorcontrib>Ren, Qinghu</creatorcontrib><creatorcontrib>Amedeo, Paolo</creatorcontrib><creatorcontrib>Jones, Kristie M</creatorcontrib><creatorcontrib>Tallon, Luke J</creatorcontrib><creatorcontrib>Delcher, Arthur L</creatorcontrib><creatorcontrib>Salzberg, Steven L</creatorcontrib><creatorcontrib>Silva, Joana C</creatorcontrib><creatorcontrib>Haas, Brian J</creatorcontrib><creatorcontrib>Majoros, William H</creatorcontrib><creatorcontrib>Farzad, Maryam</creatorcontrib><creatorcontrib>Carlton, Jane M</creatorcontrib><creatorcontrib>Smith, Jr, Roger K</creatorcontrib><creatorcontrib>Garg, Jyoti</creatorcontrib><creatorcontrib>Pearlman, Ronald E</creatorcontrib><creatorcontrib>Karrer, Kathleen M</creatorcontrib><creatorcontrib>Sun, Lei</creatorcontrib><creatorcontrib>Manning, Gerard</creatorcontrib><creatorcontrib>Elde, Nels C</creatorcontrib><creatorcontrib>Turkewitz, Aaron P</creatorcontrib><creatorcontrib>Asai, David J</creatorcontrib><creatorcontrib>Wilkes, David E</creatorcontrib><creatorcontrib>Wang, Yufeng</creatorcontrib><creatorcontrib>Cai, Hong</creatorcontrib><creatorcontrib>Collins, Kathleen</creatorcontrib><creatorcontrib>Stewart, B Andrew</creatorcontrib><creatorcontrib>Lee, Suzanne R</creatorcontrib><creatorcontrib>Wilamowska, Katarzyna</creatorcontrib><creatorcontrib>Weinberg, Zasha</creatorcontrib><creatorcontrib>Ruzzo, Walter L</creatorcontrib><creatorcontrib>Wloga, Dorota</creatorcontrib><creatorcontrib>Gaertig, Jacek</creatorcontrib><creatorcontrib>Frankel, Joseph</creatorcontrib><creatorcontrib>Tsao, Che-Chia</creatorcontrib><creatorcontrib>Gorovsky, Martin A</creatorcontrib><creatorcontrib>Keeling, Patrick J</creatorcontrib><creatorcontrib>Waller, Ross F</creatorcontrib><creatorcontrib>Patron, Nicola J</creatorcontrib><creatorcontrib>Cherry, J Michael</creatorcontrib><creatorcontrib>Stover, Nicholas A</creatorcontrib><creatorcontrib>Krieger, Cynthia J</creatorcontrib><creatorcontrib>del Toro, Christina</creatorcontrib><creatorcontrib>Ryder, Hilary F</creatorcontrib><creatorcontrib>Williamson, Sondra C</creatorcontrib><creatorcontrib>Barbeau, Rebecca A</creatorcontrib><creatorcontrib>Hamilton, Eileen P</creatorcontrib><creatorcontrib>Orias, Eduardo</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection 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Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science &amp; Fisheries Abstracts (ASFA) 1: Biological Sciences &amp; Living Resources</collection><collection>Aquatic Science &amp; Fisheries Abstracts (ASFA) Professional</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><collection>PLoS Biology</collection><jtitle>PLoS biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Eisen, Jonathan A</au><au>Coyne, Robert S</au><au>Wu, Martin</au><au>Wu, Dongying</au><au>Thiagarajan, Mathangi</au><au>Wortman, Jennifer R</au><au>Badger, Jonathan H</au><au>Ren, Qinghu</au><au>Amedeo, Paolo</au><au>Jones, Kristie M</au><au>Tallon, Luke J</au><au>Delcher, Arthur L</au><au>Salzberg, Steven L</au><au>Silva, Joana C</au><au>Haas, Brian J</au><au>Majoros, William H</au><au>Farzad, Maryam</au><au>Carlton, Jane M</au><au>Smith, Jr, Roger K</au><au>Garg, Jyoti</au><au>Pearlman, Ronald E</au><au>Karrer, Kathleen M</au><au>Sun, Lei</au><au>Manning, Gerard</au><au>Elde, Nels C</au><au>Turkewitz, Aaron P</au><au>Asai, David J</au><au>Wilkes, David E</au><au>Wang, Yufeng</au><au>Cai, Hong</au><au>Collins, Kathleen</au><au>Stewart, B Andrew</au><au>Lee, Suzanne R</au><au>Wilamowska, Katarzyna</au><au>Weinberg, Zasha</au><au>Ruzzo, Walter L</au><au>Wloga, Dorota</au><au>Gaertig, Jacek</au><au>Frankel, Joseph</au><au>Tsao, Che-Chia</au><au>Gorovsky, Martin A</au><au>Keeling, Patrick J</au><au>Waller, Ross F</au><au>Patron, Nicola J</au><au>Cherry, J Michael</au><au>Stover, Nicholas A</au><au>Krieger, Cynthia J</au><au>del Toro, Christina</au><au>Ryder, Hilary F</au><au>Williamson, Sondra C</au><au>Barbeau, Rebecca A</au><au>Hamilton, Eileen P</au><au>Orias, Eduardo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote</atitle><jtitle>PLoS biology</jtitle><addtitle>PLoS Biol</addtitle><date>2006-09-01</date><risdate>2006</risdate><volume>4</volume><issue>9</issue><spage>e286</spage><epage>e286</epage><pages>e286-e286</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>The ciliate Tetrahymena thermophila is a model organism for molecular and cellular biology. Like other ciliates, this species has separate germline and soma functions that are embodied by distinct nuclei within a single cell. The germline-like micronucleus (MIC) has its genome held in reserve for sexual reproduction. The soma-like macronucleus (MAC), which possesses a genome processed from that of the MIC, is the center of gene expression and does not directly contribute DNA to sexual progeny. We report here the shotgun sequencing, assembly, and analysis of the MAC genome of T. thermophila, which is approximately 104 Mb in length and composed of approximately 225 chromosomes. Overall, the gene set is robust, with more than 27,000 predicted protein-coding genes, 15,000 of which have strong matches to genes in other organisms. The functional diversity encoded by these genes is substantial and reflects the complexity of processes required for a free-living, predatory, single-celled organism. This is highlighted by the abundance of lineage-specific duplications of genes with predicted roles in sensing and responding to environmental conditions (e.g., kinases), using diverse resources (e.g., proteases and transporters), and generating structural complexity (e.g., kinesins and dyneins). In contrast to the other lineages of alveolates (apicomplexans and dinoflagellates), no compelling evidence could be found for plastid-derived genes in the genome. UGA, the only T. thermophila stop codon, is used in some genes to encode selenocysteine, thus making this organism the first known with the potential to translate all 64 codons in nuclear genes into amino acids. We present genomic evidence supporting the hypothesis that the excision of DNA from the MIC to generate the MAC specifically targets foreign DNA as a form of genome self-defense. The combination of the genome sequence, the functional diversity encoded therein, and the presence of some pathways missing from other model organisms makes T. thermophila an ideal model for functional genomic studies to address biological, biomedical, and biotechnological questions of fundamental importance.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>16933976</pmid><doi>10.1371/journal.pbio.0040286</doi><oa>free_for_read</oa></addata></record>
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subjects Alveolates
Animals
Cells, Cultured
Chromosome Mapping - methods
Chromosomes
Databases, Genetic
Deoxyribonucleic acid
DNA
Eukaryotic Cells - physiology
Evolution, Molecular
Genetics
Genetics/Genomics/Gene Therapy
Genome, Protozoan
Genomes
Genomics
Macronucleus - genetics
Micronucleus, Germline - genetics
Microorganisms
Models, Animal
Models, Biological
Phylogenetics
Phylogeny
Signal Transduction
Tetrahymena thermophila
Tetrahymena thermophila - genetics
title Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote
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