Investigation of Yersinia pestis laboratory adaptation through a combined genomics and proteomics approach
Abstract
Here, the bacterial pathogen Yersinia pestis, the cause of plague in humans and animals, normally has a sylvatic lifestyle, cycling between fleas and mammals. In contrast, laboratory-grown Y. pestis experiences a more constant environment and conditions that it would not normally encounter. The transition from the natural environment to the laboratory results in a vastly different set of selective pressures, and represents what could be considered domestication. Understanding the kinds of adaptations Y. pestis undergoes as it becomes domesticated will contribute to understanding the basic biology of this important pathogen. In this study, we performed a Parallel Serial Passage Experiment (PSPE) to explore the mechanisms by which Y. pestis adapts to laboratory conditions, hypothesizing that cells would undergo significant changes in virulence and nutrient acquisition systems. Two wild strains were serially passaged in 12 independent populations each for ~750 generations, after which each population was analyzed using whole-genome sequencing. We observed considerable parallel evolution in the endpoint populations, detecting multiple independent mutations in ail, pepA, and zwf, suggesting that specific selective pressures are shaping evolutionary responses. Complementary LC-MS-based proteomic data provide physiological context to the observed mutations, and reveal regulatory changes not necessarily associated with specific mutations, including changes inmore »
- Authors:
-
- Northern Arizona Univ., Flagstaff, AZ (United States)
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Washington State Univ., Pullman, WA (United States)
- Northern Arizona Univ., Flagstaff, AZ (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1228344
- Report Number(s):
- PNNL-SA-113471
Journal ID: ISSN 1932-6203
- Grant/Contract Number:
- AC05-76RL01830
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 11; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Yersinia pestis; LC-MS/MS; proteomics; genomics; evolution; domestication; adaptation
Citation Formats
Leiser, Owen P., Merkley, Eric D., Clowers, Brian H., Kaiser, Brooke L. Deatherage, Lin, Andy, Hutchison, Janine R., Melville, Angela M., Wagner, David M., Keim, Paul S., Foster, Jeff, and Kreuzer, Helen W. Investigation of Yersinia pestis laboratory adaptation through a combined genomics and proteomics approach. United States: N. p., 2015.
Web. doi:10.1371/journal.pone.0142997.
Leiser, Owen P., Merkley, Eric D., Clowers, Brian H., Kaiser, Brooke L. Deatherage, Lin, Andy, Hutchison, Janine R., Melville, Angela M., Wagner, David M., Keim, Paul S., Foster, Jeff, & Kreuzer, Helen W. Investigation of Yersinia pestis laboratory adaptation through a combined genomics and proteomics approach. United States. https://doi.org/10.1371/journal.pone.0142997
Leiser, Owen P., Merkley, Eric D., Clowers, Brian H., Kaiser, Brooke L. Deatherage, Lin, Andy, Hutchison, Janine R., Melville, Angela M., Wagner, David M., Keim, Paul S., Foster, Jeff, and Kreuzer, Helen W. Tue .
"Investigation of Yersinia pestis laboratory adaptation through a combined genomics and proteomics approach". United States. https://doi.org/10.1371/journal.pone.0142997. https://www.osti.gov/servlets/purl/1228344.
@article{osti_1228344,
title = {Investigation of Yersinia pestis laboratory adaptation through a combined genomics and proteomics approach},
author = {Leiser, Owen P. and Merkley, Eric D. and Clowers, Brian H. and Kaiser, Brooke L. Deatherage and Lin, Andy and Hutchison, Janine R. and Melville, Angela M. and Wagner, David M. and Keim, Paul S. and Foster, Jeff and Kreuzer, Helen W.},
abstractNote = {Here, the bacterial pathogen Yersinia pestis, the cause of plague in humans and animals, normally has a sylvatic lifestyle, cycling between fleas and mammals. In contrast, laboratory-grown Y. pestis experiences a more constant environment and conditions that it would not normally encounter. The transition from the natural environment to the laboratory results in a vastly different set of selective pressures, and represents what could be considered domestication. Understanding the kinds of adaptations Y. pestis undergoes as it becomes domesticated will contribute to understanding the basic biology of this important pathogen. In this study, we performed a Parallel Serial Passage Experiment (PSPE) to explore the mechanisms by which Y. pestis adapts to laboratory conditions, hypothesizing that cells would undergo significant changes in virulence and nutrient acquisition systems. Two wild strains were serially passaged in 12 independent populations each for ~750 generations, after which each population was analyzed using whole-genome sequencing. We observed considerable parallel evolution in the endpoint populations, detecting multiple independent mutations in ail, pepA, and zwf, suggesting that specific selective pressures are shaping evolutionary responses. Complementary LC-MS-based proteomic data provide physiological context to the observed mutations, and reveal regulatory changes not necessarily associated with specific mutations, including changes in amino acid metabolism, envelope biogenesis, iron storage and acquisition, and a type VI secretion system. Proteomic data support hypotheses generated by genomic data in addition to suggesting future mechanistic studies, indicating that future whole-genome sequencing studies be designed to leverage proteomics as a critical complement.},
doi = {10.1371/journal.pone.0142997},
journal = {PLoS ONE},
number = 11,
volume = 10,
place = {United States},
year = {Tue Nov 24 00:00:00 EST 2015},
month = {Tue Nov 24 00:00:00 EST 2015}
}
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Biomarker Candidate Identification in Yersinia p estis Using Organism-Wide Semiquantitative Proteomics
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Identification of Yersinia pestis and Escherichia coli Strains by Whole Cell and Outer Membrane Protein Extracts with Mass Spectrometry-Based Proteomics
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Genome sequence of Yersinia pestis, the causative agent of plague
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ProteomeXchange provides globally coordinated proteomics data submission and dissemination
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- Vizcaíno, Juan A.; Deutsch, Eric W.; Wang, Rui
- Nature Biotechnology, Vol. 32, Issue 3
Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity
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- Morelli, Giovanna; Song, Yajun; Mazzoni, Camila J.
- Nature Genetics, Vol. 42, Issue 12
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