Protein abundances can distinguish between naturally-occurring and laboratory strains of Yersinia pestis, the causative agent of plague

Merkley, Eric D.; Sego, Landon H.; Lin, Andy; Leiser, Owen P.; Kaiser, Brooke L. Deatherage; Adkins, Joshua N.; Keim, Paul S.; Wagner, David M.; Kreuzer, Helen W.; Hakami, Ramin M.

doi:10.1371/journal.pone.0183478

Protein abundances can distinguish between naturally-occurring and laboratory strains of Yersinia pestis, the causative agent of plague

Journal Article · Wed Aug 30 00:00:00 EDT 2017 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0183478· OSTI ID:1393747

Merkley, Eric D. ^[1]; Sego, Landon H. ^[1]; ^[2]; Leiser, Owen P. ^[3]; Kaiser, Brooke L. Deatherage ^[1]; Adkins, Joshua N. ^[1]; Keim, Paul S. ^[3]; Wagner, David M. ^[3]; Kreuzer, Helen W. ^[1]; Hakami, Ramin M. ^[4]

Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Univ. of Washington, Seattle, WA (United States)
Northern Arizona Univ., Flagstaff, AZ (United States)
George Mason Univ., Fairfax, VA (United States)

Adaptive processes in bacterial species can occur rapidly in laboratory culture, leading to genetic divergence between naturally occurring and laboratory-adapted strains. Differentiating wild and closely-related laboratory strains is clearly important for biodefense and bioforensics; however, DNA sequence data alone has thus far not provided a clear signature, perhaps due to lack of understanding of how diverse genome changes lead to adapted phenotypes. Protein abundance profiles from mass spectrometry-based proteomics analyses are a molecular measure of phenotype. Proteomics data contains sufficient information that powerful statistical methods can uncover signatures that distinguish wild strains of Yersinia pestis from laboratory-adapted strains.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1393747

Report Number(s):: PNNL-SA--123853; 49532

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 8 Vol. 12; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (56)

PRISM: A data management system for high-throughput proteomics Kiebel, Gary R.; Auberry, Ken J.; Jaitly, Navdeep PROTEOMICS, Vol. 6, Issue 6 https://doi.org/10.1002/pmic.200500500	journal	March 2006
Identifying novel biomarkers through data mining—A realistic scenario? Griss, Johannes; Perez‐Riverol, Yasset; Hermjakob, Henning PROTEOMICS – Clinical Applications, Vol. 9, Issue 3-4 https://doi.org/10.1002/prca.201400107	journal	January 2015
Proteomics of hosts and pathogens in cystic fibrosis Kamath, Karthik Shantharam; Kumar, Sheemal Shanista; Kaur, Jashanpreet PROTEOMICS - Clinical Applications, Vol. 9, Issue 1-2 https://doi.org/10.1002/prca.201400122	journal	January 2015
ProteinLasso: A Lasso regression approach to protein inference problem in shotgun proteomics Huang, Ting; Gong, Haipeng; Yang, Can Computational Biology and Chemistry, Vol. 43 https://doi.org/10.1016/j.compbiolchem.2012.12.008	journal	April 2013
Selective isolation of Yersinia pestis from plague-infected fleas Sarovich, Derek S.; Colman, Rebecca E.; Price, Erin P. Journal of Microbiological Methods, Vol. 82, Issue 1 https://doi.org/10.1016/j.mimet.2010.03.019	journal	July 2010
Effects of bacterial inactivation methods on downstream proteomic analysis Lin, Andy; Merkley, Eric D.; Clowers, Brian H. Journal of Microbiological Methods, Vol. 112 https://doi.org/10.1016/j.mimet.2015.01.015	journal	May 2015
Mass-Spectrometry-Based Proteomics Reveals Organ-Specific Expression Patterns To Be Used as Forensic Evidence Dammeier, Sascha; Nahnsen, Sven; Veit, Johannes Journal of Proteome Research, Vol. 15, Issue 1 https://doi.org/10.1021/acs.jproteome.5b00704	journal	December 2015
Signatures for Mass Spectrometry Data Quality Amidan, Brett G.; Orton, Daniel J.; LaMarche, Brian L. Journal of Proteome Research, Vol. 13, Issue 4 https://doi.org/10.1021/pr401143e	journal	March 2014
Respiratory Proteomics: From Descriptive Studies to Personalized Medicine Teran, Luis M.; Montes-Vizuet, Rosalia; Li, Xinping Journal of Proteome Research, Vol. 14, Issue 1 https://doi.org/10.1021/pr500935s	journal	October 2014
Genome sequence of Yersinia pestis, the causative agent of plague Parkhill, J.; Wren, B. W.; Thomson, N. R. Nature, Vol. 413, Issue 6855 https://doi.org/10.1038/35097083	journal	October 2001
Methods of integrating data to uncover genotype–phenotype interactions Ritchie, Marylyn D.; Holzinger, Emily R.; Li, Ruowang Nature Reviews Genetics, Vol. 16, Issue 2 https://doi.org/10.1038/nrg3868	journal	January 2015
Interactome analysis reveals that lncRNA HULC promotes aerobic glycolysis through LDHA and PKM2 Wang, Chunqing; Li, Yongmei; Yan, Shuai Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16966-3	journal	June 2020
Hepatitis C virus enhances Rubicon expression, leading to autophagy inhibition and intracellular innate immune activation Shiode, Yuto; Hikita, Hayato; Tanaka, Satoshi Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-72294-y	journal	September 2020
The Pacific Northwest National Laboratory library of bacterial and archaeal proteomic biodiversity Payne, Samuel H.; Monroe, Matthew E.; Overall, Christopher C. Scientific Data, Vol. 2, Issue 1 https://doi.org/10.1038/sdata.2015.41	journal	August 2015
From The Cover: Differential plague-transmission dynamics determine Yersinia pestis population genetic structure on local, regional, and global scales Girard, J. M.; Wagner, D. M.; Vogler, A. J. Proceedings of the National Academy of Sciences, Vol. 101, Issue 22 https://doi.org/10.1073/pnas.0401561101	journal	May 2004
Microevolution and history of the plague bacillus, Yersinia pestis Achtman, M.; Morelli, G.; Zhu, P. Proceedings of the National Academy of Sciences, Vol. 101, Issue 51 https://doi.org/10.1073/pnas.0408026101	journal	December 2004
Temperature and growth phase influence the outer-membrane proteome and the expression of a type VI secretion system in Yersinia pestis Pieper, R.; Huang, S. -T.; Robinson, J. M. Microbiology, Vol. 155, Issue 2 https://doi.org/10.1099/mic.0.022160-0	journal	February 2009
A missense mutation causes aspartase deficiency in Yersinia pestis Viola, Ronald E.; Yerman, Lyudmyla; Fowler, Janet M. Microbiology, Vol. 154, Issue 5 https://doi.org/10.1099/mic.0.2007/015529-0	journal	May 2008
A Surface-Focused Biotinylation Procedure Identifies the Yersinia pestis Catalase KatY as a Membrane-Associated but Non-Surface-Located Protein Myers-Morales, Tanya; Cowan, Clarissa; Gray, Michael E. Applied and Environmental Microbiology, Vol. 73, Issue 18 https://doi.org/10.1128/aem.02968-06	journal	July 2007
Yersinia pestis--etiologic agent of plague. Perry, R. D.; Fetherston, J. D. Clinical Microbiology Reviews, Vol. 10, Issue 1 https://doi.org/10.1128/cmr.10.1.35	journal	January 1997
Resistance of Yersinia pestis to Complement-Dependent Killing Is Mediated by the Ail Outer Membrane Protein Bartra, Sara Schesser; Styer, Katie L.; O'Bryant, Deanna M. Infection and Immunity, Vol. 76, Issue 2 https://doi.org/10.1128/iai.01125-07	journal	November 2007
In vivo comparison of avirulent Vwa- and Pgm- or Pstr phenotypes of yersiniae. Une, T.; Brubaker, R. R. Infection and Immunity, Vol. 43, Issue 3 https://doi.org/10.1128/iai.43.3.895-900.1984	journal	January 1984
Physiological basis of the low calcium response in Yersinia pestis. Fowler, J. M.; Brubaker, R. R. Infection and Immunity, Vol. 62, Issue 12 https://doi.org/10.1128/iai.62.12.5234-5241.1994	journal	January 1994
Silencing and Reactivation of Urease in Yersinia pestis Is Determined by One G Residue at a Specific Position in the ureD Gene Sebbane, F.; Devalckenaere, A.; Foulon, J. Infection and Immunity, Vol. 69, Issue 1 https://doi.org/10.1128/iai.69.1.170-176.2001	journal	January 2001
A NAC for Regulating Metabolism: the Nitrogen Assimilation Control Protein (NAC) from Klebsiella pneumoniae Bender, R. A. Journal of Bacteriology, Vol. 192, Issue 19 https://doi.org/10.1128/jb.00266-10	journal	July 2010
Proteomic Characterization of Yersinia pestis Virulence Chromy, B. A.; Choi, M. W.; Murphy, G. A. Journal of Bacteriology, Vol. 187, Issue 23 https://doi.org/10.1128/jb.187.23.8172-8180.2005	journal	November 2005
Identifying Sources of Human Exposure to Plague Lowell, Jennifer L.; Wagner, David M.; Atshabar, Bakyt Journal of Clinical Microbiology, Vol. 43, Issue 4 https://doi.org/10.1128/jcm.43.4.2040.2005	journal	April 2005
Nitrogen control in bacteria Merrick, M. J.; Edwards, R. A. Microbiological Reviews, Vol. 59, Issue 4 https://doi.org/10.1128/mr.59.4.604-622.1995	journal	December 1995
The evolution of transposable elements in natural populations of self-fertilizing Arabidopsis thaliana and its outcrossing relative Arabidopsis lyrata Lockton, Steven; Gaut, Brandon S. BMC Evolutionary Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2148-10-10	journal	January 2010
Comparative Omics-Driven Genome Annotation Refinement: Application across Yersiniae Schrimpe-Rutledge, Alexandra C.; Jones, Marcus B.; Chauhan, Sadhana PLoS ONE, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pone.0033903	journal	March 2012
Investigation of Yersinia pestis Laboratory Adaptation through a Combined Genomics and Proteomics Approach Leiser, Owen P.; Merkley, Eric D.; Clowers, Brian H. PLOS ONE, Vol. 10, Issue 11 https://doi.org/10.1371/journal.pone.0142997	journal	November 2015
Fine-scale Identification of the Most Likely Source of a Human Plague Infection Colman, Rebecca E.; Vogler, Amy J.; Lowell, Jennifer L. Emerging Infectious Diseases, Vol. 15, Issue 10 https://doi.org/10.3201/eid1510.090188	journal	October 2009
A Review of the “Omics” Approach to Biomarkers of Oxidative Stress in Oryza sativa Ma, Nyuk; Rahmat, Zaidah; Lam, Su International Journal of Molecular Sciences, Vol. 14, Issue 4 https://doi.org/10.3390/ijms14047515	journal	April 2013
Exploring the potential of public proteomics data Vaudel, Marc; Verheggen, Kenneth; Csordas, Attila PROTEOMICS, Vol. 16, Issue 2 https://doi.org/10.1002/pmic.201500295	journal	December 2015
In vitro catalysis of oxidative folding of disulfide-bonded proteins by the Escherichia coli dsbA (ppfA) gene product. Akiyama, Y.; Kamitani, S.; Kusukawa, N. Journal of Biological Chemistry, Vol. 267, Issue 31 https://doi.org/10.1016/S0021-9258(18)41691-2	journal	November 1992
Characterization of the Flavoprotein Moieties of NADPH-Sulfite Reductase from Salmonella typhimurium and Escherichia coli Ostrowski, J.; Barber, M. J.; Rueger, D. C. Journal of Biological Chemistry, Vol. 264, Issue 27 https://doi.org/10.1016/S0021-9258(18)71547-0	journal	September 1989
Temperature-regulated expression of bacterial virulence genes Konkel, Michael E.; Tilly, Kit Microbes and Infection, Vol. 2, Issue 2 https://doi.org/10.1016/S1286-4579(00)00272-0	journal	February 2000
Application of Multi-Omics Techniques for Bioprocess Design and Optimization in Chinese Hamster Ovary Cells Farrell, Amy; McLoughlin, Niaobh; Milne, John J. Journal of Proteome Research, Vol. 13, Issue 7 https://doi.org/10.1021/pr500219b	journal	June 2014
MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Cox, Jürgen; Mann, Matthias Nature Biotechnology, Vol. 26, Issue 12 https://doi.org/10.1038/nbt.1511	journal	November 2008
A multi-omic systems approach to elucidating Yersinia virulence mechanisms Ansong, Charles; Schrimpe-Rutledge, Alexandra C.; Mitchell, Hugh D. Mol. BioSyst., Vol. 9, Issue 1 https://doi.org/10.1039/C2MB25287B	journal	January 2013
2016 update of the PRIDE database and its related tools Vizcaíno, Juan Antonio; Csordas, Attila; del-Toro, Noemi Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1145	journal	November 2015
A Surface-Focused Biotinylation Procedure Identifies the Yersinia pestis Catalase KatY as a Membrane-Associated but Non-Surface-Located Protein Myers-Morales, Tanya; Cowan, Clarissa; Gray, Michael E. Applied and Environmental Microbiology, Vol. 73, Issue 18 https://doi.org/10.1128/AEM.02968-06	journal	July 2007
Yersinia pestis--etiologic agent of plague. Perry, R. D.; Fetherston, J. D. Clinical Microbiology Reviews, Vol. 10, Issue 1 https://doi.org/10.1128/CMR.10.1.35	journal	January 1997
Resistance of Yersinia pestis to Complement-Dependent Killing Is Mediated by the Ail Outer Membrane Protein Bartra, Sara Schesser; Styer, Katie L.; O'Bryant, Deanna M. Infection and Immunity, Vol. 76, Issue 2 https://doi.org/10.1128/IAI.01125-07	journal	November 2007
In vivo comparison of avirulent Vwa- and Pgm- or Pstr phenotypes of yersiniae. Une, T.; Brubaker, R. R. Infection and Immunity, Vol. 43, Issue 3 https://doi.org/10.1128/IAI.43.3.895-900.1984	journal	January 1984
Physiological basis of the low calcium response in Yersinia pestis. Fowler, J. M.; Brubaker, R. R. Infection and Immunity, Vol. 62, Issue 12 https://doi.org/10.1128/IAI.62.12.5234-5241.1994	journal	January 1994
Silencing and Reactivation of Urease in Yersinia pestis Is Determined by One G Residue at a Specific Position in the ureD Gene Sebbane, F.; Devalckenaere, A.; Foulon, J. Infection and Immunity, Vol. 69, Issue 1 https://doi.org/10.1128/IAI.69.1.170-176.2001	journal	January 2001
A NAC for Regulating Metabolism: the Nitrogen Assimilation Control Protein (NAC) from Klebsiella pneumoniae Bender, R. A. Journal of Bacteriology, Vol. 192, Issue 19 https://doi.org/10.1128/JB.00266-10	journal	July 2010
Proteomic Characterization of Yersinia pestis Virulence Chromy, B. A.; Choi, M. W.; Murphy, G. A. Journal of Bacteriology, Vol. 187, Issue 23 https://doi.org/10.1128/JB.187.23.8172-8180.2005	journal	November 2005
Identifying Sources of Human Exposure to Plague Lowell, J. L.; Wagner, D. M.; Atshabar, B. Journal of Clinical Microbiology, Vol. 43, Issue 2 https://doi.org/10.1128/JCM.43.2.650-656.2005	journal	February 2005
Nitrogen control in bacteria. Merrick, M. J.; Edwards, R. A. Microbiological reviews, Vol. 59, Issue 4 https://doi.org/10.1128/MMBR.59.4.604-622.1995	journal	January 1995
Nitrogen Assimilation and Global Regulation in Escherichia coli Reitzer, Larry Annual Review of Microbiology, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.micro.57.030502.090820	journal	October 2003
Proteomic analysis of iron acquisition, metabolic and regulatory responses of Yersinia pestis to iron starvation Pieper, Rembert; Huang, Shih-Ting; Parmar, Prashanth P. BMC Microbiology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2180-10-30	journal	January 2010
Mutations in Global Regulators Lead to Metabolic Selection during Adaptation to Complex Environments Saxer, Gerda; Krepps, Michael D.; Merkley, Eric D. PLoS Genetics, Vol. 10, Issue 12 https://doi.org/10.1371/journal.pgen.1004872	journal	December 2014
Regularization Paths for Generalized Linear Models via Coordinate Descent Friedman, Jerome; Hastie, Trevor; Tibshirani, Robert Journal of Statistical Software, Vol. 33, Issue 1 https://doi.org/10.18637/jss.v033.i01	journal	January 2010
Cat-Transmitted Fatal Pneumonic Plague in a Person who Traveled from Colorado to Arizona * Davis, Ted; Doll, John M.; Ettestad, Paul The American Journal of Tropical Medicine and Hygiene, Vol. 51, Issue 1 https://doi.org/10.4269/ajtmh.1994.51.109	journal	July 1994

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