Multilevel comparative analysis of the contributions of genome reduction and heat shock to the Escherichia coli transcriptome

被引:23
作者
Ying, Bei-Wen [1 ]
Seno, Shigeto [1 ]
Kaneko, Fuyuro [1 ]
Matsuda, Hideo [1 ]
Yomo, Tetsuya [1 ,2 ,3 ]
机构
[1] Osaka Univ, Grad Sch Informat Sci & Technol, Suita, Osaka 5650871, Japan
[2] Osaka Univ, Grad Sch Frontier Biosci, Suita, Osaka 5650871, Japan
[3] Japan Sci & Technol Agcy JST, Exploratory Res Adv Technol ERATO, Suita, Osaka 5650871, Japan
来源
BMC GENOMICS | 2013年 / 14卷
关键词
Transcriptome; Negative epistasis; Genome reduction; Chromosomal periodicity; Regulatory network; Transcriptional change; Genomic interruption; Environmental perturbation; Heat shock; Directionality; DENSITY OLIGONUCLEOTIDE MICROARRAYS; CHROMOSOMAL PERIODICITY; STRINGENT RESPONSE; EXPRESSION; GENES; K-12; ORGANIZATION; COMPLEXITY; SEQUENCE; STRESS;
D O I
10.1186/1471-2164-14-25
中图分类号
Q81 [生物工程学(生物技术)]; Q93 [微生物学];
学科分类号
071005 ; 0836 ; 090102 ; 100705 ;
摘要
Background: Both large deletions in genome and heat shock stress would lead to alterations in the gene expression profile; however, whether there is any potential linkage between these disturbances to the transcriptome have not been discovered. Here, the relationship between the genomic and environmental contributions to the transcriptome was analyzed by comparing the transcriptomes of the bacterium Escherichia coli (strain MG1655 and its extensive genomic deletion derivative, MDS42) grown in regular and transient heat shock conditions. Results: The transcriptome analysis showed the following: (i) there was a reorganization of the transcriptome in accordance with preferred chromosomal periodicity upon genomic or heat shock perturbation; (ii) there was a considerable overlap between the perturbed regulatory networks and the categories enriched for differentially expressed genes (DEGs) following genome reduction and heat shock; (iii) the genes sensitive to genome reduction tended to be located close to genomic scars, and some were also highly responsive to heat shock; and (iv) the genomic and environmental contributions to the transcriptome displayed not only a positive correlation but also a negatively compensated relationship (i.e., antagonistic epistasis). Conclusion: The contributions of genome reduction and heat shock to the Escherichia coli transcriptome were evaluated at multiple levels. The observations of overlapping perturbed networks, directional similarity in transcriptional changes, positive correlation and epistatic nature linked the two contributions and suggest somehow a crosstalk guiding transcriptional reorganization in response to both genetic and environmental disturbances in bacterium E. coli.
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相关论文
共 48 条
[21]   Role of SeqA and Dam in Escherichia coli gene expression:: A global/microarray analysis [J].
Lobner-Olesen, A ;
Marinus, MG ;
Hansen, FG .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2003, 100 (08) :4672-4677
[22]   Chromosomal periodicity and positional networks of genes in Escherichia coli [J].
Mathelier, Anthony ;
Carbone, Alessandra .
MOLECULAR SYSTEMS BIOLOGY, 2010, 6
[23]   Quantifying epistatic interactions among the components constituting the protein translation system [J].
Matsuura, Tomoaki ;
Kazuta, Yasuaki ;
Aita, Takuyo ;
Adachi, Jiro ;
Yomo, Tetsuya .
MOLECULAR SYSTEMS BIOLOGY, 2009, 5
[24]   A DISTINCT SEGMENT OF THE SIGMA(32) POLYPEPTIDE IS INVOLVED IN DNAK-MEDIATED NEGATIVE CONTROL OF THE HEAT-SHOCK RESPONSE IN ESCHERICHIA-COLI [J].
NAGAI, H ;
YUZAWA, H ;
KANEMORI, M ;
YURA, T .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1994, 91 (22) :10280-10284
[25]   Condition-Dependent Transcriptome Reveals High-Level Regulatory Architecture in Bacillus subtilis [J].
Nicolas, Pierre ;
Maeder, Ulrike ;
Dervyn, Etienne ;
Rochat, Tatiana ;
Leduc, Aurelie ;
Pigeonneau, Nathalie ;
Bidnenko, Elena ;
Marchadier, Elodie ;
Hoebeke, Mark ;
Aymerich, Stephane ;
Becher, Doerte ;
Bisicchia, Paola ;
Botella, Eric ;
Delumeau, Olivier ;
Doherty, Geoff ;
Denham, Emma L. ;
Fogg, Mark J. ;
Fromion, Vincent ;
Goelzer, Anne ;
Hansen, Annette ;
Haertig, Elisabeth ;
Harwood, Colin R. ;
Homuth, Georg ;
Jarmer, Hanne ;
Jules, Matthieu ;
Klipp, Edda ;
Le Chat, Ludovic ;
Lecointe, Francois ;
Lewis, Peter ;
Liebermeister, Wolfram ;
March, Anika ;
Mars, Ruben A. T. ;
Nannapaneni, Priyanka ;
Noone, David ;
Pohl, Susanne ;
Rinn, Bernd ;
Ruegheimer, Frank ;
Sappa, Praveen K. ;
Samson, Franck ;
Schaffer, Marc ;
Schwikowski, Benno ;
Steil, Leif ;
Stuelke, Joerg ;
Wiegert, Thomas ;
Devine, Kevin M. ;
Wilkinson, Anthony J. ;
van Dijl, Jan Maarten ;
Hecker, Michael ;
Voelker, Uwe ;
Bessieres, Philippe .
SCIENCE, 2012, 335 (6072) :1103-1106
[26]   An improved physico-chemical model of hybridization on high-density oligonucleotide microarrays [J].
Ono, Naoaki ;
Suzuki, Shingo ;
Furusawa, Chikara ;
Agata, Tomoharu ;
Kashiwagi, Akiko ;
Shimizu, Hiroshi ;
Yomo, Tetsuya .
BIOINFORMATICS, 2008, 24 (10) :1278-1285
[27]   Structure and Complexity of a Bacterial Transcriptome [J].
Passalacqua, Karla D. ;
Varadarajan, Anjana ;
Ondov, Brian D. ;
Okou, David T. ;
Zwick, Michael E. ;
Bergman, Nicholas H. .
JOURNAL OF BACTERIOLOGY, 2009, 191 (10) :3203-3211
[28]   Genomic transcriptional response to loss of chromosomal supercoiling in Escherichia coli -: art. no. R87 [J].
Peter, BJ ;
Arsuaga, J ;
Breier, AM ;
Khodursky, AB ;
Brown, PO ;
Cozzarelli, NR .
GENOME BIOLOGY, 2004, 5 (11)
[29]   Emergent properties of reduced-genome Escherichia coli [J].
Pósfai, G ;
Plunkett, G ;
Fehér, T ;
Frisch, D ;
Keil, GM ;
Umenhoffer, K ;
Kolisnychenko, V ;
Stahl, B ;
Sharma, SS ;
de Arruda, M ;
Burland, V ;
Harcum, SW ;
Blattner, FR .
SCIENCE, 2006, 312 (5776) :1044-1046
[30]   Genome-wide expression profiling in Escherichia coli K-12 [J].
Richmond, CS ;
Glasner, JD ;
Mau, R ;
Jin, HF ;
Blattner, FR .
NUCLEIC ACIDS RESEARCH, 1999, 27 (19) :3821-3835