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

Jonathan A. Eisen, Robert S. Coyne, Martin Wu, Dongying Wu, Mathangi Thiagarajan, Jennifer R. Wortman, Jonathan H. Badger, Qinghu Ren, Paolo Amedeo, Kristie M. Jones, Luke J. Tallon, Arthur L. Delcher, Steven L Salzberg, Joana C. Silva, Brian J. Haas, William H. Majoros, Maryam Farzad, Jane M. Carlton, Roger K. Smith, Jyoti Garg & 33 others Ronald E. Pearlman, Kathleen M. Karrer, Lei Sun, Gerard Manning, Nels C. Elde, Aaron P. Turkewitz, David J. Asai, David E. Wilkes, Yufeng Wang, Hong Cai, Kathleen Collins, B. Andrew Stewart, Suzanne R. Lee, Katarzyna Wilamowska, Zasha Weinberg, Walter L. Ruzzo, Dorota Wloga, Jacek Gaertig, Joseph Frankel, Che Chia Tsao, Martin A. Gorovsky, Patrick J. Keeling, Ross F. Waller, Nicola J. Patron, J. Michael Cherry, Nicholas A. Stover, Cynthia J. Krieger, Christina Del Toro, Hilary F. Ryder, Sondra C. Williamson, Rebecca A. Barbeau, Eileen P. Hamilton, Eduardo Orias

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
JournalPLoS Biology
Volume4
Issue number9
DOIs
StatePublished - Sep 2006
Externally publishedYes

Fingerprint

Tetrahymena thermophila
Eukaryota
Ciliophora
eukaryotic cells
Genes
Macronucleus
Genome
genome
organisms
genes
Carisoprodol
functional diversity
Germline Micronucleus
DNA
germ cells
Selenocysteine
Dinoflagellida
Dyneins
Kinesin
Plastids

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)

Cite this

Eisen, J. A., Coyne, R. S., Wu, M., Wu, D., Thiagarajan, M., Wortman, J. R., ... Orias, E. (2006). Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biology, 4(9). https://doi.org/10.1371/journal.pbio.0040286

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

In: PLoS Biology, Vol. 4, No. 9, 09.2006.

Research output: Contribution to journalArticle

Eisen, JA, Coyne, RS, Wu, M, Wu, D, Thiagarajan, M, Wortman, JR, Badger, JH, Ren, Q, Amedeo, P, Jones, KM, Tallon, LJ, Delcher, AL, Salzberg, SL, Silva, JC, Haas, BJ, Majoros, WH, Farzad, M, Carlton, JM, Smith, RK, Garg, J, Pearlman, RE, Karrer, KM, Sun, L, Manning, G, Elde, NC, Turkewitz, AP, Asai, DJ, Wilkes, DE, Wang, Y, Cai, H, Collins, K, Stewart, BA, Lee, SR, Wilamowska, K, Weinberg, Z, Ruzzo, WL, Wloga, D, Gaertig, J, Frankel, J, Tsao, CC, Gorovsky, MA, Keeling, PJ, Waller, RF, Patron, NJ, Cherry, JM, Stover, NA, Krieger, CJ, Del Toro, C, Ryder, HF, Williamson, SC, Barbeau, RA, Hamilton, EP & Orias, E 2006, 'Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote.', PLoS Biology, vol. 4, no. 9. https://doi.org/10.1371/journal.pbio.0040286
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, 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. / Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. In: PLoS Biology. 2006 ; Vol. 4, No. 9.
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T1 - Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote.

AU - Eisen, Jonathan A.

AU - Coyne, Robert S.

AU - Wu, Martin

AU - Wu, Dongying

AU - Thiagarajan, Mathangi

AU - Wortman, Jennifer R.

AU - Badger, Jonathan H.

AU - Ren, Qinghu

AU - Amedeo, Paolo

AU - Jones, Kristie M.

AU - Tallon, Luke J.

AU - Delcher, Arthur L.

AU - Salzberg, Steven L

AU - Silva, Joana C.

AU - Haas, Brian J.

AU - Majoros, William H.

AU - Farzad, Maryam

AU - Carlton, Jane M.

AU - Smith, Roger K.

AU - Garg, Jyoti

AU - Pearlman, Ronald E.

AU - Karrer, Kathleen M.

AU - Sun, Lei

AU - Manning, Gerard

AU - Elde, Nels C.

AU - Turkewitz, Aaron P.

AU - Asai, David J.

AU - Wilkes, David E.

AU - Wang, Yufeng

AU - Cai, Hong

AU - Collins, Kathleen

AU - Stewart, B. Andrew

AU - Lee, Suzanne R.

AU - Wilamowska, Katarzyna

AU - Weinberg, Zasha

AU - Ruzzo, Walter L.

AU - Wloga, Dorota

AU - Gaertig, Jacek

AU - Frankel, Joseph

AU - Tsao, Che Chia

AU - Gorovsky, Martin A.

AU - Keeling, Patrick J.

AU - Waller, Ross F.

AU - Patron, Nicola J.

AU - Cherry, J. Michael

AU - Stover, Nicholas A.

AU - Krieger, Cynthia J.

AU - Del Toro, Christina

AU - Ryder, Hilary F.

AU - Williamson, Sondra C.

AU - Barbeau, Rebecca A.

AU - Hamilton, Eileen P.

AU - Orias, Eduardo

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N2 - 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.

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