The Evolution of the Phage Shock Protein Response System: Interplay between Protein Function, Genomic Organization, and System Function
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2011
Authors
Huvet, M.Toni, T.
Sheng, X.
Thorne, T.
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Jovanović, Goran
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Engl, C.
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Buck, M.
Pinney, J. W.
Stumpf, M. P. H.
Article (Published version)
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Show full item recordAbstract
Here, we use a systematic analysis of the genes that make up and regulate the Psp system in E. coli in order to elucidate the evolutionary history of the system. We compare gene sharing, sequence evolution, and conservation of protein-coding as well as noncoding DNA sequences and link these to comparative analyses of genome/operon organization across 698 bacterial genomes. Finally, we evaluate experimentally the biological advantage/disadvantage of a simplified version of the Psp system under different oxygen-related environments. Our results suggest that the Psp system evolved around a core response mechanism by gradually co-opting genes into the system to provide more nuanced sensory, signaling, and effector functionalities. We find that recruitment of new genes into the response machinery is closely linked to incorporation of these genes into a psp operon as is seen in E. coli, which contains the bulk of genes involved in the response. The organization of this operon allows for surp...rising levels of additional transcriptional control and flexibility. The results discussed here suggest that the components of such signaling systems will only be evolutionarily conserved if the overall functionality of the system can be maintained.
Keywords:
signaling system / signal transduction network / phage shock stress response / comparative genomics / bacteriaSource:
Molecular Biology and Evolution, 2011, 28, 3, 1141-1155Publisher:
- Oxford Univ Press, Oxford
Funding / projects:
- BBSRC
- MRC
- Kwok foundation
- Wellcome Trust
- Royal Society
- BBSRC [BB/G00594X/1, BB/F005210/1, BB/F005210/2, BB/F013566/1] Funding Source: UKRI
- Biotechnology and Biological Sciences Research Council [BB/F005210/1, BB/F013566/1, BB/G00594X/1, BB/F005210/2] Funding Source: researchfish
DOI: 10.1093/molbev/msq301
ISSN: 0737-4038
PubMed: 21059793
WoS: 000287745200003
Scopus: 2-s2.0-79952149017
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Institution/Community
Institut za molekularnu genetiku i genetičko inženjerstvoTY - JOUR AU - Huvet, M. AU - Toni, T. AU - Sheng, X. AU - Thorne, T. AU - Jovanović, Goran AU - Engl, C. AU - Buck, M. AU - Pinney, J. W. AU - Stumpf, M. P. H. PY - 2011 UR - https://imagine.imgge.bg.ac.rs/handle/123456789/483 AB - Here, we use a systematic analysis of the genes that make up and regulate the Psp system in E. coli in order to elucidate the evolutionary history of the system. We compare gene sharing, sequence evolution, and conservation of protein-coding as well as noncoding DNA sequences and link these to comparative analyses of genome/operon organization across 698 bacterial genomes. Finally, we evaluate experimentally the biological advantage/disadvantage of a simplified version of the Psp system under different oxygen-related environments. Our results suggest that the Psp system evolved around a core response mechanism by gradually co-opting genes into the system to provide more nuanced sensory, signaling, and effector functionalities. We find that recruitment of new genes into the response machinery is closely linked to incorporation of these genes into a psp operon as is seen in E. coli, which contains the bulk of genes involved in the response. The organization of this operon allows for surprising levels of additional transcriptional control and flexibility. The results discussed here suggest that the components of such signaling systems will only be evolutionarily conserved if the overall functionality of the system can be maintained. PB - Oxford Univ Press, Oxford T2 - Molecular Biology and Evolution T1 - The Evolution of the Phage Shock Protein Response System: Interplay between Protein Function, Genomic Organization, and System Function EP - 1155 IS - 3 SP - 1141 VL - 28 DO - 10.1093/molbev/msq301 ER -
@article{ author = "Huvet, M. and Toni, T. and Sheng, X. and Thorne, T. and Jovanović, Goran and Engl, C. and Buck, M. and Pinney, J. W. and Stumpf, M. P. H.", year = "2011", abstract = "Here, we use a systematic analysis of the genes that make up and regulate the Psp system in E. coli in order to elucidate the evolutionary history of the system. We compare gene sharing, sequence evolution, and conservation of protein-coding as well as noncoding DNA sequences and link these to comparative analyses of genome/operon organization across 698 bacterial genomes. Finally, we evaluate experimentally the biological advantage/disadvantage of a simplified version of the Psp system under different oxygen-related environments. Our results suggest that the Psp system evolved around a core response mechanism by gradually co-opting genes into the system to provide more nuanced sensory, signaling, and effector functionalities. We find that recruitment of new genes into the response machinery is closely linked to incorporation of these genes into a psp operon as is seen in E. coli, which contains the bulk of genes involved in the response. The organization of this operon allows for surprising levels of additional transcriptional control and flexibility. The results discussed here suggest that the components of such signaling systems will only be evolutionarily conserved if the overall functionality of the system can be maintained.", publisher = "Oxford Univ Press, Oxford", journal = "Molecular Biology and Evolution", title = "The Evolution of the Phage Shock Protein Response System: Interplay between Protein Function, Genomic Organization, and System Function", pages = "1155-1141", number = "3", volume = "28", doi = "10.1093/molbev/msq301" }
Huvet, M., Toni, T., Sheng, X., Thorne, T., Jovanović, G., Engl, C., Buck, M., Pinney, J. W.,& Stumpf, M. P. H.. (2011). The Evolution of the Phage Shock Protein Response System: Interplay between Protein Function, Genomic Organization, and System Function. in Molecular Biology and Evolution Oxford Univ Press, Oxford., 28(3), 1141-1155. https://doi.org/10.1093/molbev/msq301
Huvet M, Toni T, Sheng X, Thorne T, Jovanović G, Engl C, Buck M, Pinney JW, Stumpf MPH. The Evolution of the Phage Shock Protein Response System: Interplay between Protein Function, Genomic Organization, and System Function. in Molecular Biology and Evolution. 2011;28(3):1141-1155. doi:10.1093/molbev/msq301 .
Huvet, M., Toni, T., Sheng, X., Thorne, T., Jovanović, Goran, Engl, C., Buck, M., Pinney, J. W., Stumpf, M. P. H., "The Evolution of the Phage Shock Protein Response System: Interplay between Protein Function, Genomic Organization, and System Function" in Molecular Biology and Evolution, 28, no. 3 (2011):1141-1155, https://doi.org/10.1093/molbev/msq301 . .