Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Transcriptome Complexity in a Genome-Reduced Bacterium
Marc Güell,1
Vera van Noort,2
Eva Yus,1
Wei-Hua Chen,2
Justine Leigh-Bell,1
Konstantinos Michalodimitrakis,1
Takuji Yamada,2
Manimozhiyan Arumugam,2
Tobias Doerks,2
Sebastian Kühner,2
Michaela Rode,2
Mikita Suyama,2,*
Sabine Schmidt,2
Anne-Claude Gavin,2
Peer Bork,2,
Luis Serrano1,3,
Abstract:
To study basic principles of transcriptome organization in bacteria,we analyzed one of the smallest self-replicating organisms,Mycoplasma pneumoniae. We combined strand-specific tiling arrays,complemented by transcriptome sequencing, with more than 252spotted arrays. We detected 117 previously undescribed, mostlynoncoding transcripts, 89 of them in antisense configurationto known genes. We identified 341 operons, of which 139 arepolycistronic; almost half of the latter show decaying expressionin a staircase-like manner. Under various conditions, operonscould be divided into 447 smaller transcriptional units, resultingin many alternative transcripts. Frequent antisense transcripts,alternative transcripts, and multiple regulators per gene implya highly dynamic transcriptome, more similar to that of eukaryotesthan previously thought.
1 Centre for Genomic Regulation (CRG), Universitat Pompeu Fabra, Barcelona, Spain. 2 European Molecular Biology Laboratory (EMBL), Heidelberg, Germany. 3 Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
* Present address: Center for Genomic Medicine, Graduate Schoolof Medicine, University of Kyoto, Kyoto, Japan.
To whom correspondence should be addressed. E-mail: bork{at}embl.de (P.B.); luis.serrano{at}crg.es (L.S.)
The editors suggest the following Related Resources on Science sites:
In Science Magazine
PERSPECTIVES
Howard Ochman and Rahul Raghavan (27 November 2009) Science326 (5957), 1200.
[DOI: 10.1126/science.1183757] |Summary »|Full Text »|PDF »
RESEARCH ARTICLES
Sebastian Kühner, Vera van Noort, Matthew J. Betts, Alejandra Leo-Macias, Claire Batisse, Michaela Rode, Takuji Yamada, Tobias Maier, Samuel Bader, Pedro Beltran-Alvarez, Daniel Castaño-Diez, Wei-Hua Chen, Damien Devos, Marc Güell, Tomas Norambuena, Ines Racke, Vladimir Rybin, Alexander Schmidt, Eva Yus, Ruedi Aebersold, Richard Herrmann, Bettina Böttcher, Achilleas S. Frangakis, Robert B. Russell, Luis Serrano, Peer Bork, and Anne-Claude Gavin (27 November 2009) Science326 (5957), 1235.
[DOI: 10.1126/science.1176343] |Abstract »|Full Text »|PDF »|Supporting Online Material »
REPORTS
Eva Yus, Tobias Maier, Konstantinos Michalodimitrakis, Vera van Noort, Takuji Yamada, Wei-Hua Chen, Judith A. H. Wodke, Marc Güell, Sira Martínez, Ronan Bourgeois, Sebastian Kühner, Emanuele Raineri, Ivica Letunic, Olga V. Kalinina, Michaela Rode, Richard Herrmann, Ricardo Gutiérrez-Gallego, Robert B. Russell, Anne-Claude Gavin, Peer Bork, and Luis Serrano (27 November 2009) Science326 (5957), 1263.
[DOI: 10.1126/science.1177263] |Abstract »|Full Text »|PDF »|Supporting Online Material »
In Science Signaling
EDITORS' CHOICE
L. Bryan Ray (1 December 2009) Sci. Signal.2 (99), ec386.
[DOI: 10.1126/scisignal.299ec386] |Abstract »
THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Non-coding RNAs in homeostasis, disease and stress responses: an evolutionary perspective.
P. P. Amaral, M. E. Dinger, and J. S. Mattick (2013)
Briefings in Functional Genomics
12, 254-278
|Abstract »|Full Text »|PDF »
Next-generation sequencing technologies and their impact on microbial genomics.
Global Network Reorganization During Dynamic Adaptations of Bacillus subtilis Metabolism.
J. M. Buescher, W. Liebermeister, M. Jules, M. Uhr, J. Muntel, E. Botella, B. Hessling, R. J. Kleijn, L. Le Chat, F. Lecointe, et al. (2012)
Science
335, 1099-1103
|Abstract »|Full Text »|PDF »
Condition-Dependent Transcriptome Reveals High-Level Regulatory Architecture in Bacillus subtilis.
P. Nicolas, U. Mader, E. Dervyn, T. Rochat, A. Leduc, N. Pigeonneau, E. Bidnenko, E. Marchadier, M. Hoebeke, S. Aymerich, et al. (2012)
Science
335, 1103-1106
|Abstract »|Full Text »|PDF »
Comprehensive Transcriptome Analysis of the Periodontopathogenic Bacterium Porphyromonas gingivalis W83.
H. Hovik, W.-H. Yu, I. Olsen, and T. Chen (2012)
J. Bacteriol.
194, 100-114
|Abstract »|Full Text »|PDF »
Genome-wide antisense transcription drives mRNA processing in bacteria.
I. Lasa, A. Toledo-Arana, A. Dobin, M. Villanueva, I. R. de los Mozos, M. Vergara-Irigaray, V. Segura, D. Fagegaltier, J. R. Penades, J. Valle, et al. (2011)
PNAS
108, 20172-20177
|Abstract »|Full Text »|PDF »
Mycoplasma hyopneumoniae Transcription Unit Organization: Genome Survey and Prediction.
Bacterial Small RNA Regulators: Versatile Roles and Rapidly Evolving Variations.
S. Gottesman and G. Storz (2011)
Cold Spring Harb Perspect Biol
3, a003798
|Abstract »|Full Text »|PDF »
Parallel evolution of transcriptome architecture during genome reorganization.
S. H. Yoon, D. J. Reiss, J. C. Bare, D. Tenenbaum, M. Pan, J. Slagel, R. L. Moritz, S. Lim, M. Hackett, A. L. Menon, et al. (2011)
Genome Res.
21, 1892-1904
|Abstract »|Full Text »|PDF »
Evidence-Based Annotation of Transcripts and Proteins in the Sulfate-Reducing Bacterium Desulfovibrio vulgaris Hildenborough.
M. N. Price, A. M. Deutschbauer, J. V. Kuehl, H. Liu, H. E. Witkowska, and A. P. Arkin (2011)
J. Bacteriol.
193, 5716-5727
|Abstract »|Full Text »|PDF »
Expression and Characterization of a Mycoplasma genitalium Glycosyltransferase in Membrane Glycolipid Biosynthesis: POTENTIAL TARGET AGAINST MYCOPLASMA INFECTIONS.
E. Andres, N. Martinez, and A. Planas (2011)
J. Biol. Chem.
286, 35367-35379
|Abstract »|Full Text »|PDF »
Complete Genome and Proteome of Acholeplasma laidlawii.
V. N. Lazarev, S. A. Levitskii, Y. I. Basovskii, M. M. Chukin, T. A. Akopian, V. V. Vereshchagin, E. S. Kostrjukova, G. Y. Kovaleva, M. D. Kazanov, D. B. Malko, et al. (2011)
J. Bacteriol.
193, 4943-4953
|Abstract »|Full Text »|PDF »
The minimal genome--a metabolic and environmental comparison.
M. T. DeWall and D. W. Cheng (2011)
Briefings in Functional Genomics
10, 312-315
|Abstract »|Full Text »|PDF »
Convergent transcription confers a bistable switch in Enterococcus faecalis conjugation.
A. Chatterjee, C. M. Johnson, C.-C. Shu, Y. N. Kaznessis, D. Ramkrishna, G. M. Dunny, and W.-S. Hu (2011)
PNAS
108, 9721-9726
|Abstract »|Full Text »|PDF »
cis-Antisense RNA, Another Level of Gene Regulation in Bacteria.
Antisense RNA protects mRNA from RNase E degradation by RNA-RNA duplex formation during phage infection.
D. Stazic, D. Lindell, and C. Steglich (2011)
Nucleic Acids Res.
39, 4890-4899
|Abstract »|Full Text »|PDF »
Clostridium difficile Transcriptome Analysis Using Pig Ligated Loop Model Reveals Modulation of Pathways Not Modulated In Vitro.
J. Scaria, T. Janvilisri, S. Fubini, R. D. Gleed, S. P. McDonough, and Y.-F. Chang (2011)
The Journal of Infectious Disease
203, 1613-1620
|Abstract »|Full Text »|PDF »
A simple and efficient method to search for selected primary transcripts: non-coding and antisense RNAs in the human pathogen Enterococcus faecalis.
A. Fouquier d'Herouel, F. Wessner, D. Halpern, J. Ly-Vu, S. P. Kennedy, P. Serror, E. Aurell, and F. Repoila (2011)
Nucleic Acids Res.
39, e46
|Abstract »|Full Text »|PDF »
The pseudogenes of Mycobacterium leprae reveal the functional relevance of gene order within operons.
E. M. Muro, N. Mah, G. Moreno-Hagelsieb, and M. A. Andrade-Navarro (2011)
Nucleic Acids Res.
39, 1732-1738
|Abstract »|Full Text »|PDF »
Direct and indirect effects of H-NS and Fis on global gene expression control in Escherichia coli.
C. Kahramanoglou, A. S. N. Seshasayee, A. I. Prieto, D. Ibberson, S. Schmidt, J. Zimmermann, V. Benes, G. M. Fraser, and N. M. Luscombe (2011)
Nucleic Acids Res.
39, 2073-2091
|Abstract »|Full Text »|PDF »
Transcriptional response of Mycoplasma genitalium to osmotic stress.
Targeted Chromosomal Knockouts in Mycoplasma pneumoniae.
R. Krishnakumar, N. Assad-Garcia, G. A. Benders, Q. Phan, M. G. Montague, and J. I. Glass (2010)
Appl. Envir. Microbiol.
76, 5297-5299
|Abstract »|Full Text »|PDF »
Strand-specific deep sequencing of the transcriptome.
A. P. Vivancos, M. Guell, J. C. Dohm, L. Serrano, and H. Himmelbauer (2010)
Genome Res.
20, 989-999
|Abstract »|Full Text »|PDF »
Widespread Antisense Transcription in Escherichia coli.
J. E. Dornenburg, A. M. DeVita, M. J. Palumbo, and J. T. Wade (2010)
mBio
1, e00024-10
|Abstract »|Full Text »|PDF »
Excavating the Functional Landscape of Bacterial Cells.
Proteome Organization in a Genome-Reduced Bacterium.
S. Kuhner, V. van Noort, M. J. Betts, A. Leo-Macias, C. Batisse, M. Rode, T. Yamada, T. Maier, S. Bader, P. Beltran-Alvarez, et al. (2009)
Science
326, 1235-1240
|Abstract »|Full Text »|PDF »
Impact of Genome Reduction on Bacterial Metabolism and Its Regulation.
E. Yus, T. Maier, K. Michalodimitrakis, V. van Noort, T. Yamada, W.-H. Chen, J. A. H. Wodke, M. Guell, S. Martinez, R. Bourgeois, et al. (2009)
Science
326, 1263-1268
|Abstract »|Full Text »|PDF »