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

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.

doi:10.1371/journal.pone.0142997

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

Journal Article · Tue Nov 24 00:00:00 EST 2015 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0142997· OSTI ID:1228344

Leiser, Owen P. ^[1]; Merkley, Eric D. ^[2]; Clowers, Brian H. ^[3]; Kaiser, Brooke L. Deatherage ^[2]; Lin, Andy ^[2]; Hutchison, Janine R. ^[2]; Melville, Angela M. ^[2]; Wagner, David M. ^[1]; Keim, Paul S. ^[1]; Foster, Jeff ^[4]; Kreuzer, Helen W. ^[2]

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)

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.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1228344

Report Number(s):: PNNL-SA-113471

Journal Information:: PLoS ONE, Vol. 10, Issue 11; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 13 works

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References (92)

Versatile and open software for comparing large genomes Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L. Genome Biology, Vol. 5, Issue 2, R12 https://doi.org/10.1186/gb-2004-5-2-r12	journal	January 2004
Prokaryotic toxin–antitoxin stress response loci Gerdes, Kenn; Christensen, Susanne K.; Løbner-Olesen, Anders Nature Reviews Microbiology, Vol. 3, Issue 5 https://doi.org/10.1038/nrmicro1147	journal	May 2005
NATURAL HISTORY OF PLAGUE: Perspectives from More than a Century of Research Gage, Kenneth L.; Kosoy, Michael Y. Annual Review of Entomology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev.ento.50.071803.130337	journal	January 2005
Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis Chain, P. S. G.; Carniel, E.; Larimer, F. W. Proceedings of the National Academy of Sciences, Vol. 101, Issue 38 https://doi.org/10.1073/pnas.0404012101	journal	September 2004
DAnTE: a statistical tool for quantitative analysis of -omics data Polpitiya, A. D.; Qian, W. -J.; Jaitly, N. Bioinformatics, Vol. 24, Issue 13 https://doi.org/10.1093/bioinformatics/btn217	journal	May 2008
Identification of Yersinia pestis and Escherichia coli Strains by Whole Cell and Outer Membrane Protein Extracts with Mass Spectrometry-Based Proteomics Jabbour, Rabih E.; Wade, Mary Margaret; Deshpande, Samir V. Journal of Proteome Research, Vol. 9, Issue 7 https://doi.org/10.1021/pr100402y	journal	July 2010
Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity Morelli, Giovanna; Song, Yajun; Mazzoni, Camila J. Nature Genetics, Vol. 42, Issue 12 https://doi.org/10.1038/ng.705	journal	October 2010
A global model of carbon, nitrogen and phosphorus cycles for the terrestrial biosphere Wang, Y. P.; Law, R. M.; Pak, B. Biogeosciences, Vol. 7, Issue 7 https://doi.org/10.5194/bg-7-2261-2010	journal	January 2010
Regulation by destruction: design of the σE envelope stress response Ades, Sarah E. Current Opinion in Microbiology, Vol. 11, Issue 6 https://doi.org/10.1016/j.mib.2008.10.004	journal	December 2008
ArgR and PepA, accessory proteins for XerCD-mediated resolution of ColE1 dimers, are also required for stable maintenance of the P1 prophage Paul, Sunirmal; Summers, David Plasmid, Vol. 52, Issue 1 https://doi.org/10.1016/j.plasmid.2004.04.003	journal	July 2004
Loss of the pigmentation phenotype in Yersinia pestis is due to the spontaneous deletion of 102 kb of chromosomal DNA which is flanked by a repetitive element Fetherston, Jacqueline D.; Schuetze, Paul; Perry, Robert D. Molecular Microbiology, Vol. 6, Issue 18 https://doi.org/10.1111/j.1365-2958.1992.tb01446.x	journal	September 1992
Mutational Analysis of Intervening Sequences Connecting the Binding Sites for Integration Host Factor, PepA, PurR, and RNA Polymerase in the Control Region of the Escherichia coli carAB Operon, Encoding Carbamoylphosphate Synthase Devroede, N.; Huysveld, N.; Charlier, D. Journal of Bacteriology, Vol. 188, Issue 9 https://doi.org/10.1128/JB.188.9.3236-3245.2006	journal	April 2006
ProteomeXchange provides globally coordinated proteomics data submission and dissemination Vizcaíno, Juan A.; Deutsch, Eric W.; Wang, Rui Nature Biotechnology, Vol. 32, Issue 3 https://doi.org/10.1038/nbt.2839	journal	March 2014
An experimentally-supported genome-scale metabolic network reconstruction for Yersinia pestis CO92 Charusanti, Pep; Chauhan, Sadhana; McAteer, Kathleen BMC Systems Biology, Vol. 5, Issue 1 https://doi.org/10.1186/1752-0509-5-163	journal	January 2011
Biomarker Candidate Identification in Yersinia p estis Using Organism-Wide Semiquantitative Proteomics Hixson, Kim K.; Adkins, Joshua N.; Baker, Scott E. Journal of Proteome Research, Vol. 5, Issue 11 https://doi.org/10.1021/pr060179y	journal	November 2006
Molecular transformers in the cell: lessons learned from the DegP protease–chaperone Sawa, Justyna; Heuck, Alexander; Ehrmann, Michael Current Opinion in Structural Biology, Vol. 20, Issue 2 https://doi.org/10.1016/j.sbi.2010.01.014	journal	April 2010
In silico comparison of Yersinia pestis and Yersinia pseudotuberculosis transcriptomes reveals a higher expression level of crucial virulence determinants in the plague bacillus Chauvaux, Sylvie; Dillies, Marie-Agnès; Marceau, Michaël International Journal of Medical Microbiology, Vol. 301, Issue 2 https://doi.org/10.1016/j.ijmm.2010.08.013	journal	February 2011
Expression, refolding, and initial structural characterization of the Y. pestis Ail outer membrane protein in lipids Plesniak, Leigh A.; Mahalakshmi, Radhakrishnan; Rypien, Candace Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1808, Issue 1 https://doi.org/10.1016/j.bbamem.2010.09.017	journal	January 2011
The Small Heat-shock Protein IbpB from Escherichia coli Stabilizes Stress-denatured Proteins for Subsequent Refolding by a Multichaperone Network Veinger, Lea; Diamant, Sophia; Buchner, Johannes Journal of Biological Chemistry, Vol. 273, Issue 18 https://doi.org/10.1074/jbc.273.18.11032	journal	May 1998
The nature of laboratory domestication changes in freshly isolated Escherichia coli strains : Laboratory domestication of Eydallin, Gustavo; Ryall, Ben; Maharjan, Ram Environmental Microbiology, Vol. 16, Issue 3 https://doi.org/10.1111/1462-2920.12208	journal	July 2013
Intracellular Yersinia pestis expresses general stress response and tellurite resistance proteins in mouse macrophages Ponnusamy, Duraisamy; Hartson, Steven D.; Clinkenbeard, Kenneth D. Veterinary Microbiology, Vol. 150, Issue 1-2 https://doi.org/10.1016/j.vetmic.2010.12.025	journal	May 2011
Whole-Genome Sequencing Reveals Distinct Mutational Patterns in Closely Related Laboratory and Naturally Propagated Francisella tularensis Strains Sjödin, Andreas; Svensson, Kerstin; Lindgren, Marie PLoS ONE, Vol. 5, Issue 7 https://doi.org/10.1371/journal.pone.0011556	journal	July 2010
The Plasmid-Encoded Outer-Membrane Proteins of Yersinia pestis Straley, S. C. Clinical Infectious Diseases, Vol. 10, Issue Supplement 2 https://doi.org/10.1093/cid/10.Supplement_2.S323	journal	May 1988
Chemically Etched Open Tubular and Monolithic Emitters for Nanoelectrospray Ionization Mass Spectrometry Kelly, Ryan T.; Page, Jason S.; Luo, Quanzhou Analytical Chemistry, Vol. 78, Issue 22, p. 7796-7801 https://doi.org/10.1021/ac061133r	journal	November 2006
Mutations, mutation rates, and evolution at the hypervariable VNTR loci of Yersinia pestis Vogler, Amy J.; Keys, Christine E.; Allender, Christopher Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 616, Issue 1-2 https://doi.org/10.1016/j.mrfmmm.2006.11.007	journal	March 2007
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
Trace analysis of muramic acid in indoor air using an automated derivatization instrument and GC–MS2 or GC–MS3 Harley, William M.; Kozar, Michael P.; Fox, Alvin Journal of Microbiological Methods, Vol. 51, Issue 1 https://doi.org/10.1016/S0167-7012(02)00064-7	journal	September 2002
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
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
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
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
The Soil Microbial Biomass: Concept, Measurement and Applications in Soil Ecosystem Research Brookes, Philip Microbes and Environments, Vol. 16, Issue 3 https://doi.org/10.1264/jsme2.2001.131	journal	January 2001
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
carP, Involved in Pyrimidine Regulation of theEscherichia coliCarbamoylphosphate Synthetase Operon Encodes a Sequence-specific DNA-binding Protein Identical to XerB and PepA, also Required for Resolution of ColEl Multimers Charlier, Daniel; Hassanzadeh Gh., Gholamreza; Kholti, Abdelaziz Journal of Molecular Biology, Vol. 250, Issue 4 https://doi.org/10.1006/jmbi.1995.0385	journal	July 1995
Mechanism of GroEL action: Productive release of polypeptide from a sequestered position under groes Weissman, Jonathan S.; Hohl, Corinne M.; Kovalenko, Oleg Cell, Vol. 83, Issue 4 https://doi.org/10.1016/0092-8674(95)90098-5	journal	November 1995
The Escherichia coli Extracellular Death Factor EDF Induces the Endoribonucleolytic Activities of the Toxins MazF and ChpBK Belitsky, Maria; Avshalom, Haim; Erental, Ariel Molecular Cell, Vol. 41, Issue 6 https://doi.org/10.1016/j.molcel.2011.02.023	journal	March 2011
Chaperone function of FkpA, a heat shock prolyl isomerase, in the periplasm of Escherichia coli Arié, Jean-Philippe; Sassoon, Nathalie; Betton, Jean-Michel Molecular Microbiology, Vol. 39, Issue 1 https://doi.org/10.1046/j.1365-2958.2001.02250.x	journal	January 2001
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
Mutational analysis of Escherichia coli PepA, a multifunctional DNA-binding aminopeptidase 1 1Edited by M. Yaniv Charlier, Daniel; Kholti, Abdelaziz; Huysveld, Nadine Journal of Molecular Biology, Vol. 302, Issue 2 https://doi.org/10.1006/jmbi.2000.4067	journal	September 2000
The RAST Server: Rapid Annotations using Subsystems Technology Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A. BMC Genomics, Vol. 9, Issue 1, Article No. 75 https://doi.org/10.1186/1471-2164-9-75	journal	January 2008
A post-assembly genome-improvement toolkit (PAGIT) to obtain annotated genomes from contigs Swain, Martin T.; Tsai, Isheng J.; Assefa, Samual A. Nature Protocols, Vol. 7, Issue 7 https://doi.org/10.1038/nprot.2012.068	journal	June 2012
Response of the central metabolism of Escherichia coli to modified expression of the gene encoding the glucose-6-phosphate dehydrogenase Nicolas, Cécile; Kiefer, Patrick; Letisse, Fabien FEBS Letters, Vol. 581, Issue 20 https://doi.org/10.1016/j.febslet.2007.06.066	journal	July 2007
Quantitative Proteomics Reveals Subset-Specific Viral Recognition in Dendritic Cells Luber, Christian A.; Cox, Jürgen; Lauterbach, Henning Immunity, Vol. 32, Issue 2 https://doi.org/10.1016/j.immuni.2010.01.013	journal	February 2010
X-ray structure of aminopeptidase A from Escherichia coli and a model for the nucleoprotein complex in Xer site-specific recombination Strater, N. The EMBO Journal, Vol. 18, Issue 16 https://doi.org/10.1093/emboj/18.16.4513	journal	August 1999
Andromeda: A Peptide Search Engine Integrated into the MaxQuant Environment Cox, Jürgen; Neuhauser, Nadin; Michalski, Annette Journal of Proteome Research, Vol. 10, Issue 4 https://doi.org/10.1021/pr101065j	journal	April 2011
Characterizing the dynamic nature of theYersinia pestis periplasmic proteome in response to nutrient exhaustion and temperature change Pieper, Rembert; Huang, Shih-Ting; Clark, David J. PROTEOMICS, Vol. 8, Issue 7 https://doi.org/10.1002/pmic.200700923	journal	April 2008
Effect of zwf gene knockout on the metabolism of Escherichia coli grown on glucose or acetate Zhao, J. Metabolic Engineering, Vol. 6, Issue 2 https://doi.org/10.1016/j.ymben.2004.02.004	journal	April 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
Detection of Novel <I>Bartonella</I> Strains and <I>Yersinia pestis</I> in Prairie Dogs and Their Fleas (Siphonaptera: Ceratophyllidae and Pulicidae) Using Multiplex Polymerase Chain Reaction Stevenson, Heather L.; Bai, Ying; Kosoy, Michael Y. Journal of Medical Entomology, Vol. 40, Issue 3 https://doi.org/10.1603/0022-2585-40.3.329	journal	May 2003
Growth-rate recovery of Escherichia coli cultures carrying a multicopy plasmid, by engineering of the pentose-phosphate pathway : Growth-Rate Recovery by Flores, Salvador; de Anda-Herrera, Ramón; Gosset, Guillermo Biotechnology and Bioengineering, Vol. 87, Issue 4 https://doi.org/10.1002/bit.20137	journal	July 2004
SlyD Proteins from Different Species Exhibit High Prolyl Isomerase and Chaperone Activities ^† Scholz, Christian; Eckert, Barbara; Hagn, Franz Biochemistry, Vol. 45, Issue 1 https://doi.org/10.1021/bi051922n	journal	January 2006
eggNOG v4.0: nested orthology inference across 3686 organisms Powell, Sean; Forslund, Kristoffer; Szklarczyk, Damian Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1253	journal	December 2013
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
Characterization of degP, a gene required for proteolysis in the cell envelope and essential for growth of Escherichia coli at high temperature. Strauch, K. L.; Johnson, K.; Beckwith, J. Journal of Bacteriology, Vol. 171, Issue 5 https://doi.org/10.1128/jb.171.5.2689-2696.1989	journal	May 1989
mazEF: a chromosomal toxin-antitoxin module that triggers programmed cell death in bacteria Engelberg-Kulka, H. Journal of Cell Science, Vol. 118, Issue 19 https://doi.org/10.1242/jcs.02619	journal	September 2005
Integral and peripheral association of proteins and protein complexes with Yersinia pestis inner and outer membranes Pieper, Rembert; Huang, Shih-Ting; Clark, David J. Proteome Science, Vol. 7, Issue 1 https://doi.org/10.1186/1477-5956-7-5	journal	January 2009
The thioredoxin antioxidant system Lu, Jun; Holmgren, Arne Free Radical Biology and Medicine, Vol. 66 https://doi.org/10.1016/j.freeradbiomed.2013.07.036	journal	January 2014
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Discrimination Among the B. Cereus Group, in Comparison to B. Subtilis, by Structural Carbohydrate Profiles and Ribosomal RNA Spacer Region PCR Wunschel, David; Fox, Karen F.; Black, Gavin E. Systematic and Applied Microbiology, Vol. 17, Issue 4 https://doi.org/10.1016/S0723-2020(11)80085-8	journal	February 1995
Complete Genome Sequence of Yersinia pestis Strains Antiqua and Nepal516: Evidence of Gene Reduction in an Emerging Pathogen Chain, P. S. G.; Hu, P.; Malfatti, S. A. Journal of Bacteriology, Vol. 188, Issue 12 https://doi.org/10.1128/JB.00124-06	journal	June 2006
Transcriptome analysis of Yersinia pestis in human plasma: an approach for discovering bacterial genes involved in septicaemic plague Chauvaux, S.; Rosso, M. -L.; Frangeul, L. Microbiology, Vol. 153, Issue 9 https://doi.org/10.1099/mic.0.2007/006213-0	journal	September 2007
Mutagenesis of PepA suggests a new model for the Xer/cer synaptic complex: DNA-binding mutants of PepA Reijns, Martin; Lu, Yangjie; Leach, Stephen Molecular Microbiology, Vol. 57, Issue 4 https://doi.org/10.1111/j.1365-2958.2005.04716.x	journal	June 2005
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
Yersinia pestis and the Plague of Justinian 541–543 AD: a genomic analysis Wagner, David M.; Klunk, Jennifer; Harbeck, Michaela The Lancet Infectious Diseases, Vol. 14, Issue 4 https://doi.org/10.1016/S1473-3099(13)70323-2	journal	April 2014
ABySS: A parallel assembler for short read sequence data Simpson, J. T.; Wong, K.; Jackman, S. D. Genome Research, Vol. 19, Issue 6 https://doi.org/10.1101/gr.089532.108	journal	February 2009
Human Plague in the Southwestern United States, 1957–2004: Spatial Models of Elevated Risk of Human Exposure to Yersinia pestis Eisen, Rebecca J.; Enscore, Russell E.; Biggerstaff, Brad J. Journal of Medical Entomology, Vol. 44, Issue 3 https://doi.org/10.1093/jmedent/44.3.530	journal	May 2007
The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST) Overbeek, Ross; Olson, Robert; Pusch, Gordon D. Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1226	journal	November 2013
Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli Sklar, J. G.; Wu, T.; Kahne, D. Genes & Development, Vol. 21, Issue 19 https://doi.org/10.1101/gad.1581007	journal	October 2007
Yersinia pestis Ail: multiple roles of a single protein Kolodziejek, Anna M.; Hovde, Carolyn J.; Minnich, Scott A. Frontiers in Cellular and Infection Microbiology, Vol. 2 https://doi.org/10.3389/fcimb.2012.00103	journal	January 2012
Structure and reactivity of LpxD, the N-acyltransferase of lipid A biosynthesis Buetow, L.; Smith, T. K.; Dawson, A. Proceedings of the National Academy of Sciences, Vol. 104, Issue 11 https://doi.org/10.1073/pnas.0606356104	journal	March 2007
RseP (YaeL), an Escherichia coli RIP protease, cleaves transmembrane sequences Akiyama, Yoshinori; Kanehara, Kazue; Ito, Koreaki The EMBO Journal, Vol. 23, Issue 22 https://doi.org/10.1038/sj.emboj.7600449	journal	October 2004
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
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
Control of Cre recombination by regulatory elements from Xer recombination systems: Effect of PepA on Cre recombination Gourlay, Sarah C.; Colloms, Sean D. Molecular Microbiology, Vol. 52, Issue 1 https://doi.org/10.1111/j.1365-2958.2003.03962.x	journal	February 2004
Spatial Organization of Microbial Biofilm Communities Tolker-Nielsen, T.; Molin, S. Microbial Ecology, Vol. 40, Issue 2 https://doi.org/10.1007/s002480000057	journal	August 2000
Biosynthesis and metabolism of arginine in bacteria. Cunin, R.; Glansdorff, N.; Piérard, A. Microbiological Reviews, Vol. 50, Issue 3 https://doi.org/10.1128/MMBR.50.3.314-352.1986	journal	January 1986
Genetics and biochemistry of carbamoyl phosphate biosynthesis and its utilization in the pyrimidine biosynthetic pathway. Makoff, A. J.; Radford, A. Microbiological Reviews, Vol. 42, Issue 2 https://doi.org/10.1128/MMBR.42.2.307-328.1978	journal	January 1978
DNA Sequencing and Analysis of the Low-Ca2+-Response Plasmid pCD1 of Yersinia pestis KIM5 Perry, Robert D.; Straley, Susan C.; Fetherston, Jacqueline D. Infection and Immunity, Vol. 66, Issue 10 https://doi.org/10.1128/IAI.66.10.4611-4623.1998	journal	October 1998
Yersinia pestis: one pandemic, two pandemics, three pandemics, more? Gilbert, M. Thomas P. The Lancet Infectious Diseases, Vol. 14, Issue 4 https://doi.org/10.1016/s1473-3099(14)70002-7	journal	April 2014
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
Accurate Proteome-wide Label-free Quantification by Delayed Normalization and Maximal Peptide Ratio Extraction, Termed MaxLFQ Cox, Jürgen; Hein, Marco Y.; Luber, Christian A. Molecular & Cellular Proteomics, Vol. 13, Issue 9 https://doi.org/10.1074/mcp.m113.031591	journal	June 2014
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
Virulence genes regulated at the transcriptional level by Ca2+ in Yersinia pestis include structural genes for outer membrane proteins. Straley, S. C.; Bowmer, W. S. Infection and Immunity, Vol. 51, Issue 2 https://doi.org/10.1128/iai.51.2.445-454.1986	journal	January 1986
The Extracellular Death Factor: Physiological and Genetic Factors Influencing Its Production and Response in Escherichia coli Kolodkin-Gal, I.; Engelberg-Kulka, H. Journal of Bacteriology, Vol. 190, Issue 9 https://doi.org/10.1128/jb.01918-07	journal	February 2008
Structural Organization of Virulence-Associated Plasmids of Yersinia pestis Hu, Ping; Elliott, Jeffrey; McCready, Paula Journal of Bacteriology, Vol. 180, Issue 19 https://doi.org/10.1128/jb.180.19.5192-5202.1998	journal	October 1998
Deletion of lolB, Encoding an Outer Membrane Lipoprotein, Is Lethal for Escherichia coli and Causes Accumulation of Lipoprotein Localization Intermediates in the Periplasm Tanaka, K.; Matsuyama, S. -I.; Tokuda, H. Journal of Bacteriology, Vol. 183, Issue 22 https://doi.org/10.1128/jb.183.22.6538-6542.2001	journal	November 2001
New method for plague surveillance using polymerase chain reaction to detect Yersinia pestis in fleas. Hinnebusch, J.; Schwan, T. G. Journal of Clinical Microbiology, Vol. 31, Issue 6 https://doi.org/10.1128/jcm.31.6.1511-1514.1993	journal	January 1993
Genetics and biochemistry of carbamoyl phosphate biosynthesis and its utilization in the pyrimidine biosynthetic pathway Makoff, A. J.; Radford, A. Microbiological Reviews, Vol. 42, Issue 2 https://doi.org/10.1128/mr.42.2.307-328.1978	journal	June 1978
Biosynthesis and metabolism of arginine in bacteria Cunin, R.; Glansdorff, N.; Piérard, A. Microbiological Reviews, Vol. 50, Issue 3 https://doi.org/10.1128/mr.50.3.314-352.1986	journal	September 1986
Adaptation, Clonal Interference, and Frequency-Dependent Interactions in a Long-Term Evolution Experiment with Escherichia coli Maddamsetti, Rohan; Lenski, Richard E.; Barrick, Jeffrey E. Genetics, Vol. 200, Issue 2 https://doi.org/10.1534/genetics.115.176677	journal	April 2015
Differences in the stability of the plasmids of Yersinia pestis cultures in vitro: impact on virulence Leal-Balbino, Tc; Leal, Nc; Lopes, Cv Memórias do Instituto Oswaldo Cruz, Vol. 99, Issue 7 https://doi.org/10.1590/s0074-02762004000700011	journal	November 2004

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Shotgun proteomic analysis of Yersinia ruckeri strains under normal and iron-limited conditions Kumar, Gokhlesh; Hummel, Karin; Ahrens, Maike Veterinary Research, Vol. 47, Issue 1 https://doi.org/10.1186/s13567-016-0384-3	journal	October 2016
Laboratory strains of Bacillus anthracis exhibit pervasive alteration in expression of proteins related to sporulation under laboratory conditions relative to genetically related wild strains Leiser, Owen P.; Blackburn, Jason K.; Hadfield, Ted L. PLOS ONE, Vol. 13, Issue 12 https://doi.org/10.1371/journal.pone.0209120	journal	December 2018
Exopolysaccharide production in Caulobacter crescentus: A resource allocation trade-off between protection and proliferation Herr, Kathryn L.; Carey, Alexis M.; Heckman, Taylor I. PLOS ONE, Vol. 13, Issue 1 https://doi.org/10.1371/journal.pone.0190371	journal	January 2018
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 PLOS ONE, Vol. 12, Issue 8 https://doi.org/10.1371/journal.pone.0183478	journal	August 2017

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59 BASIC BIOLOGICAL SCIENCES
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