Investigation of Yersinia pestis laboratory adaptation through a combined genomics and proteomics approach

Owen P. Leiser, Eric D. Merkley, Brian H. Clowers, Brooke L. Deatherage Kaiser, Andy Lin, Janine R. Hutchison, Angela M. Melville, David M Wagner, Paul S Keim, Jeffrey T Foster, Helen W. Kreuzer

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

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, laboratorygrown 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, LC-MS/MS proteomic analysis, and GC/MS metabolomics. 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/MS 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 and cell envelope biogenesis. 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.

Original languageEnglish (US)
Article numbere0142997
JournalPLoS One
Volume10
Issue number11
DOIs
StatePublished - Nov 1 2015

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Yersinia pestis
Genomics
Proteomics
proteomics
genomics
Pathogens
mutation
Mutation
Genes
Genome
Population
Serial Passage
Siphonaptera
parallel evolution
Mammals
Metabolomics
Plague
genome
pathogens
plague

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Leiser, O. P., Merkley, E. D., Clowers, B. H., Deatherage Kaiser, B. L., Lin, A., Hutchison, J. R., ... Kreuzer, H. W. (2015). Investigation of Yersinia pestis laboratory adaptation through a combined genomics and proteomics approach. PLoS One, 10(11), [e0142997]. https://doi.org/10.1371/journal.pone.0142997

Investigation of Yersinia pestis laboratory adaptation through a combined genomics and proteomics approach. / Leiser, Owen P.; Merkley, Eric D.; Clowers, Brian H.; Deatherage Kaiser, Brooke L.; Lin, Andy; Hutchison, Janine R.; Melville, Angela M.; Wagner, David M; Keim, Paul S; Foster, Jeffrey T; Kreuzer, Helen W.

In: PLoS One, Vol. 10, No. 11, e0142997, 01.11.2015.

Research output: Contribution to journalArticle

Leiser, OP, Merkley, ED, Clowers, BH, Deatherage Kaiser, BL, Lin, A, Hutchison, JR, Melville, AM, Wagner, DM, Keim, PS, Foster, JT & Kreuzer, HW 2015, 'Investigation of Yersinia pestis laboratory adaptation through a combined genomics and proteomics approach', PLoS One, vol. 10, no. 11, e0142997. https://doi.org/10.1371/journal.pone.0142997
Leiser OP, Merkley ED, Clowers BH, Deatherage Kaiser BL, Lin A, Hutchison JR et al. Investigation of Yersinia pestis laboratory adaptation through a combined genomics and proteomics approach. PLoS One. 2015 Nov 1;10(11). e0142997. https://doi.org/10.1371/journal.pone.0142997
Leiser, Owen P. ; Merkley, Eric D. ; Clowers, Brian H. ; Deatherage Kaiser, Brooke L. ; Lin, Andy ; Hutchison, Janine R. ; Melville, Angela M. ; Wagner, David M ; Keim, Paul S ; Foster, Jeffrey T ; Kreuzer, Helen W. / Investigation of Yersinia pestis laboratory adaptation through a combined genomics and proteomics approach. In: PLoS One. 2015 ; Vol. 10, No. 11.
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