Allelic variation contributes to bacterial host specificity

Yue, Min; Han, Xiangan; Masi, Leon De; Zhu, Chunhong; Ma, Xun; Zhang, Junjie; Wu, Renwei; Schmieder, Robert; Kaushik, Radhey S.; Fraser, George P.; Zhao, Shaohua; McDermott, Patrick F.; Weill, François-Xavier; Mainil, Jacques G.; Arze, Cesar; Fricke, W. Florian; Edwards, Robert A.; Brisson, Dustin; Zhang, Nancy R.; Rankin, Shelley C.; Schifferli, Dieter M.

doi:10.1038/ncomms9754

Title: Allelic variation contributes to bacterial host specificity

Journal Article · Fri Oct 30 00:00:00 EDT 2015 · Nature Communications

DOI:https://doi.org/10.1038/ncomms9754· OSTI ID:1258603

Yue, Min ^[1]; Han, Xiangan ^[1]; Masi, Leon De ^[1]; Zhu, Chunhong ^[1]; Ma, Xun ^[1]; Zhang, Junjie ^[1]; Wu, Renwei ^[1]; Schmieder, Robert ^[2]; Kaushik, Radhey S. ^[3]; Fraser, George P. ^[4]; Zhao, Shaohua ^[5]; McDermott, Patrick F. ^[5]; Weill, François-Xavier ^[6]; Mainil, Jacques G. ^[7]; Arze, Cesar ^[8]; Fricke, W. Florian ^[8];

^[9]; Brisson, Dustin ^[10]; Zhang, Nancy R. ^[10]; Rankin, Shelley C. ^[1] more »

Univ. of Pennsylvania School of Veterinary Medicine, Philadelphia, PA (United States)
San Diego State Univ., San Diego, CA (United States)
South Dakota State Univ., Brookings, SD (United States)
Pennsylvania Department of Health, Exton, PA (United States)
US FDA Office of Research, Laurel, MD (United States). Center for Veterinary Medicine
Pasteur Institute, Paris (France)
Univ. of Liege, (Belgium)
Univ. of Maryland School of Medicine, Baltimore, MD (United States). Institute for Genome Sciences
San Diego State Univ., San Diego, CA (United States); Argonne National Lab. (ANL), Argonne, IL (United States)
Univ. of Pennsylvania, Philadelphia, PA (United States)

Understanding the molecular parameters that regulate cross-species transmission and host adaptation of potential pathogens is crucial to control emerging infectious disease. Although microbial pathotype diversity is conventionally associated with gene gain or loss, the role of pathoadaptive nonsynonymous single-nucleotide polymorphisms (nsSNPs) has not been systematically evaluated. Here, our genome-wide analysis of core genes within Salmonella enterica serovar Typhimurium genomes reveals a high degree of allelic variation in surface-exposed molecules, including adhesins that promote host colonization. Subsequent multinomial logistic regression, MultiPhen and Random Forest analyses of known/suspected adhesins from 580 independent Typhimurium isolates identifies distinct host-specific nsSNP signatures. Moreover, population and functional analyses of host-associated nsSNPs for FimH, the type 1 fimbrial adhesin, highlights the role of key allelic residues in host-specific adherence in vitro. In conclusion, together, our data provide the first concrete evidence that functional differences between allelic variants of bacterial proteins likely contribute to pathoadaption to diverse hosts.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE

OSTI ID:: 1258603

Journal Information:: Nature Communications, Vol. 6; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 65 works

Citation information provided by
Web of Science

References (62)

Allosteric Catch Bond Properties of the FimH Adhesin from Salmonella enterica Serovar Typhimurium Kisiela, Dagmara I.; Kramer, Jeremy J.; Tchesnokova, Veronika Journal of Biological Chemistry, Vol. 286, Issue 44 https://doi.org/10.1074/jbc.M111.237511	journal	July 2011
Preliminary characterization of jejunocyte and colonocyte cell lines isolated by enzymatic digestion from adult and young cattle Loret, Suzanne; Rusu, Dorina; Moualij, Benaissa El Research in Veterinary Science, Vol. 87, Issue 1 https://doi.org/10.1016/j.rvsc.2008.12.002	journal	August 2009
Evolution of Salmonella enterica Virulence via Point Mutations in the Fimbrial Adhesin Kisiela, Dagmara I.; Chattopadhyay, Sujay; Libby, Stephen J. PLoS Pathogens, Vol. 8, Issue 6 https://doi.org/10.1371/journal.ppat.1002733	journal	June 2012
FimH alleles direct preferential binding of Salmonella to distinct mammalian cells or to avian cells Guo, A.; Cao, S.; Tu, L. Microbiology, Vol. 155, Issue 5 https://doi.org/10.1099/mic.0.026286-0	journal	April 2009
Primary Cultures of Fully Differentiated and Pure Human Intestinal Epithelial Cells Perreault, Nathalie; Beaulieu, Jean-François Experimental Cell Research, Vol. 245, Issue 1 https://doi.org/10.1006/excr.1998.4221	journal	November 1998
Protein–ligand binding site recognition using complementary binding-specific substructure comparison and sequence profile alignment Yang, Jianyi; Roy, Ambrish; Zhang, Yang Bioinformatics, Vol. 29, Issue 20 https://doi.org/10.1093/bioinformatics/btt447	journal	August 2013
Genome and Transcriptome Adaptation Accompanying Emergence of the Definitive Type 2 Host-Restricted Salmonella enterica Serovar Typhimurium Pathovar Kingsley, Robert A.; Kay, Sally; Connor, Thomas mBio, Vol. 4, Issue 5 https://doi.org/10.1128/mBio.00565-13	journal	August 2013
Enabling the 'host jump': structural determinants of receptor-binding specificity in influenza A viruses Shi, Yi; Wu, Ying; Zhang, Wei Nature Reviews Microbiology, Vol. 12, Issue 12 https://doi.org/10.1038/nrmicro3362	journal	November 2014
Genome wide evolutionary analyses reveal serotype specific patterns of positive selection in selected Salmonella serotypes Soyer, Yeşim; Orsi, Renato H.; Rodriguez-Rivera, Lorraine D. BMC Evolutionary Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2148-9-264	journal	January 2009
FimH adhesin from host unrestricted Salmonella Enteritidis binds to different glycoprotein ligands expressed by enterocytes from sheep, pig and cattle than FimH adhesins from host restricted Salmonella Abortus-ovis, Salmonella Choleraesuis and Salmonella Dublin Grzymajło, Krzysztof; Ugorski, Maciej; Kolenda, Rafał Veterinary Microbiology, Vol. 166, Issue 3-4 https://doi.org/10.1016/j.vetmic.2013.07.004	journal	October 2013
Type 1 fimbriae mutants of Escherichia coli K12: characterization of recognized afimbriate strains and construction of new fim deletion mutants Blomfjeld, I. C.; McClain, M. S.; Eisenstein, B. I. Molecular Microbiology, Vol. 5, Issue 6 https://doi.org/10.1111/j.1365-2958.1991.tb00790.x	journal	June 1991
I-TASSER: a unified platform for automated protein structure and function prediction Roy, Ambrish; Kucukural, Alper; Zhang, Yang Nature Protocols, Vol. 5, Issue 4 https://doi.org/10.1038/nprot.2010.5	journal	March 2010
SNPsFinder--a web-based application for genome-wide discovery of single nucleotide polymorphisms in microbial genomes Song, J.; Xu, Y.; White, S. Bioinformatics, Vol. 21, Issue 9 https://doi.org/10.1093/bioinformatics/bti176	journal	February 2005
Patterns of genome evolution that have accompanied host adaptation in Salmonella Langridge, Gemma C.; Fookes, Maria; Connor, Thomas R. Proceedings of the National Academy of Sciences, Vol. 112, Issue 3 https://doi.org/10.1073/pnas.1416707112	journal	December 2014
Murine thymocytes with ability to inhibit I1-2 production: I. Genetic differences between mouse strains and characterization of the model system Gigliotti, Dulceaydee; Nihlmark, Eva Lotta; Wigzell, Hans APMIS, Vol. 100, Issue 1-6 https://doi.org/10.1111/j.1699-0463.1992.tb00842.x	journal	January 1992
Comprehensive Assignment of Roles for Salmonella Typhimurium Genes in Intestinal Colonization of Food-Producing Animals Chaudhuri, Roy R.; Morgan, Eirwen; Peters, Sarah E. PLoS Genetics, Vol. 9, Issue 4 https://doi.org/10.1371/journal.pgen.1003456	journal	April 2013
Differential binding to and biofilm formation on, HEp-2 cells by Salmonella enterica Serovar Typhimurium is dependent upon allelic variation in the fimH gene of the fim gene cluster: Allelic variation in the Salmonella fimH gene Boddicker, Jennifer D.; Ledeboer, Nathan A.; Jagnow, Jennifer Molecular Microbiology, Vol. 45, Issue 5 https://doi.org/10.1046/j.1365-2958.2002.03121.x	journal	September 2002
Illustration of a Common Framework for Relating Multiple Typing Methods by Application to Macrolide-Resistant Streptococcus pyogenes Carrico, J. A.; Silva-Costa, C.; Melo-Cristino, J. Journal of Clinical Microbiology, Vol. 44, Issue 7 https://doi.org/10.1128/JCM.02536-05	journal	July 2006
Host Adaptation of a Bacterial Toxin from the Human Pathogen Salmonella Typhi Deng, Lingquan; Song, Jeongmin; Gao, Xiang Cell, Vol. 159, Issue 6 https://doi.org/10.1016/j.cell.2014.10.057	journal	December 2014
Interdomain Interaction in the FimH Adhesin of Escherichia coli Regulates the Affinity to Mannose Aprikian, Pavel; Tchesnokova, Veronika; Kidd, Brian Journal of Biological Chemistry, Vol. 282, Issue 32 https://doi.org/10.1074/jbc.M702037200	journal	June 2007
Immunochemical, biomolecular and biochemical characterization of bovine epithelial intestinal primocultures Rusu, Dorina; Loret, Suzanne; Peulen, Olivier BMC Cell Biology https://doi.org/10.1186/1471-2121-6-42	journal	January 2005
Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa Okoro, Chinyere K.; Kingsley, Robert A.; Connor, Thomas R. Nature Genetics, Vol. 44, Issue 11 https://doi.org/10.1038/ng.2423	journal	September 2012
Exploratory Multivariate Analysis Venables, W. N.; Ripley, B. D. Modern Applied Statistics with S https://doi.org/10.1007/978-0-387-21706-2_11	book	January 2002
LOMETS: A local meta-threading-server for protein structure prediction Wu, Sitao; Zhang, Yang Nucleic Acids Research, Vol. 35, Issue 10 https://doi.org/10.1093/nar/gkm251	journal	May 2007
Role of receptor binding specificity in influenza A virus transmission and pathogenesis de Graaf, M.; Fouchier, R. A. M. The EMBO Journal, Vol. 33, Issue 8 https://doi.org/10.1002/embj.201387442	journal	March 2014
progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement Darling, Aaron E.; Mau, Bob; Perna, Nicole T. PLoS ONE, Vol. 5, Issue 6 https://doi.org/10.1371/journal.pone.0011147	journal	June 2010
Salmonella enterica Serovars Gallinarum and Pullorum Expressing Salmonella enterica Serovar Typhimurium Type 1 Fimbriae Exhibit Increased Invasiveness for Mammalian Cells Wilson, R. L.; Elthon, J.; Clegg, S. Infection and Immunity, Vol. 68, Issue 8 https://doi.org/10.1128/IAI.68.8.4782-4785.2000	journal	August 2000
Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology Delport, W.; Poon, A. F. Y.; Frost, S. D. W. Bioinformatics, Vol. 26, Issue 19 https://doi.org/10.1093/bioinformatics/btq429	journal	July 2010
MultiPhen: Joint Model of Multiple Phenotypes Can Increase Discovery in GWAS O’Reilly, Paul F.; Hoggart, Clive J.; Pomyen, Yotsawat PLoS ONE, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pone.0034861	journal	May 2012
CloVR: A virtual machine for automated and portable sequence analysis from the desktop using cloud computing Angiuoli, Samuel V.; Matalka, Malcolm; Gussman, Aaron BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-356	journal	August 2011
Invasive Non-Typhoidal Salmonella Typhimurium ST313 Are Not Host-Restricted and Have an Invasive Phenotype in Experimentally Infected Chickens Parsons, Bryony N.; Humphrey, Suzanne; Salisbury, Anne Marie PLoS Neglected Tropical Diseases, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pntd.0002487	journal	October 2013
DnaSP v5: a software for comprehensive analysis of DNA polymorphism data Librado, P.; Rozas, J. Bioinformatics, Vol. 25, Issue 11 https://doi.org/10.1093/bioinformatics/btp187	journal	April 2009
Distinguishable Epidemics of Multidrug-Resistant Salmonella Typhimurium DT104 in Different Hosts Mather, A. E.; Reid, S. W. J.; Maskell, D. J. Science, Vol. 341, Issue 6153 https://doi.org/10.1126/science.1240578	journal	September 2013
Comparison of genome degradation in Paratyphi A and Typhi, human-restricted serovars of Salmonella enterica that cause typhoid McClelland, Michael; Sanderson, Kenneth E.; Clifton, Sandra W. Nature Genetics, Vol. 36, Issue 12 https://doi.org/10.1038/ng1470	journal	November 2004
Estimating Nucleotide Diversity From Random Amplified Polymorphic DNA and Amplified Fragment Length Polymorphism Data Borowsky, Richard L. Molecular Phylogenetics and Evolution, Vol. 18, Issue 1 https://doi.org/10.1006/mpev.2000.0865	journal	January 2001
The combination of CRISPR-MVLST and PFGE provides increased discriminatory power for differentiating human clinical isolates of Salmonella enterica subsp. enterica serovar Enteritidis Shariat, Nikki; DiMarzio, Michael J.; Yin, Shuang Food Microbiology, Vol. 34, Issue 1 https://doi.org/10.1016/j.fm.2012.11.012	journal	May 2013
The high-adhesive properties of the FimH adhesin of Salmonella enterica serovar Enteritidis are determined by a single F118S substitution Grzymajlo, K.; Kuzminska-Bajor, M.; Jaworski, J. Microbiology, Vol. 156, Issue 6 https://doi.org/10.1099/mic.0.039206-0	journal	March 2010
Subtyping of Salmonella enterica Serovar Newport Outbreak Isolates by CRISPR-MVLST and Determination of the Relationship between CRISPR-MVLST and PFGE Results Shariat, N.; Kirchner, M. K.; Sandt, C. H. Journal of Clinical Microbiology, Vol. 51, Issue 7 https://doi.org/10.1128/JCM.00608-13	journal	May 2013
Single nucleotide polypmorphisms of fimH associated with adherence and biofilm formation by serovars of Salmonella enterica Dwyer, B. E.; Newton, K. L.; Kisiela, D. Microbiology, Vol. 157, Issue 11 https://doi.org/10.1099/mic.0.051425-0	journal	August 2011
Allelic variation in Salmonella: an underappreciated driver of adaptation and virulence Yue, Min; Schifferli, Dieter M. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00419	journal	January 2014
Diversification of the Salmonella Fimbriae: A Model of Macro- and Microevolution Yue, Min; Rankin, Shelley C.; Blanchet, Ryan T. PLoS ONE, Vol. 7, Issue 6 https://doi.org/10.1371/journal.pone.0038596	journal	June 2012
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
A comparison of dense transposon insertion libraries in the Salmonella serovars Typhi and Typhimurium Barquist, Lars; Langridge, Gemma C.; Turner, Daniel J. Nucleic Acids Research, Vol. 41, Issue 8 https://doi.org/10.1093/nar/gkt148	journal	March 2013
Catch-Bond Mechanism of Force-Enhanced Adhesion: Counterintuitive, Elusive, but … Widespread? Sokurenko, Evgeni V.; Vogel, Viola; Thomas, Wendy E. Cell Host & Microbe, Vol. 4, Issue 4 https://doi.org/10.1016/j.chom.2008.09.005	journal	October 2008
A single natural nucleotide mutation alters bacterial pathogen host tropism Viana, David; Comos, María; McAdam, Paul R. Nature Genetics, Vol. 47, Issue 4 https://doi.org/10.1038/ng.3219	journal	February 2015
PHAST: A Fast Phage Search Tool Zhou, Y.; Liang, Y.; Lynch, K. H. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr485	journal	June 2011
Sequence type analysis and recombinational tests (START) Jolley, K. A.; Feil, E. J.; Chan, M. -S. Bioinformatics, Vol. 17, Issue 12 https://doi.org/10.1093/bioinformatics/17.12.1230	journal	December 2001
Characterization of FimH Adhesins Expressed by Salmonella enterica Serovar Gallinarum Biovars Gallinarum and Pullorum: Reconstitution of Mannose-Binding Properties by Single Amino Acid Substitution Kisiela, D.; Sapeta, A.; Kuczkowski, M. Infection and Immunity, Vol. 73, Issue 9 https://doi.org/10.1128/IAI.73.9.6187-6190.2005	journal	August 2005
Decreased colonization of chicks by Salmonella enterica serovar Gallinarum expressing mannose-sensitive FimH adhesin from Salmonella enterica serovar Enteritidis Kuźmińska-Bajor, Marta; Kuczkowski, Maciej; Grzymajło, Krzysztof Veterinary Microbiology, Vol. 158, Issue 1-2 https://doi.org/10.1016/j.vetmic.2012.01.029	journal	July 2012
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
A Rab32-Dependent Pathway Contributes to Salmonella Typhi Host Restriction Spano, S.; Galan, J. E. Science, Vol. 338, Issue 6109 https://doi.org/10.1126/science.1229224	journal	November 2012
Exploratory Multivariate Analysis Cornillon, Pierre-Andre R for Statistics https://doi.org/10.1201/b11828-15	book	March 2012
Role of receptor binding specificity in influenza A virus transmission and pathogenesis Graaf, Miranda; Fouchier, Ron A. M. The EMBO Journal, Vol. 33, Issue 14 https://doi.org/10.15252/embj.201489251	journal	July 2014
Patterns of genome evolution that have accompanied host adaptation in Salmonella Langridge, Gemma C.; Fookes, Maria; Connor, Thomas R. National Academy of Sciences https://doi.org/10.5167/uzh-120453	text	January 2015
Salmonella enterica Serovar Typhimurium Binds to HeLa Cells via Fim-Mediated Reversible Adhesion and Irreversible Type Three Secretion System 1-Mediated Docking Misselwitz, Benjamin; Kreibich, Saskia K.; Rout, Samuel American Society for Microbiology https://doi.org/10.5167/uzh-79548	text	January 2011
Antibiotic Resistance in Salmonella enterica Serovar Typhimurium Associates with CRISPR Sequence Type DiMarzio, Michael; Shariat, Nikki; Kariyawasam, Subhashinie Antimicrobial Agents and Chemotherapy, Vol. 57, Issue 9 https://doi.org/10.1128/aac.00913-13	journal	June 2013
Microfluidic PCR Combined with Pyrosequencing for Identification of Allelic Variants with Phenotypic Associations among Targeted Salmonella Genes Yue, Min; Schmieder, Robert; Edwards, Robert A. Applied and Environmental Microbiology, Vol. 78, Issue 20 https://doi.org/10.1128/aem.01703-12	journal	August 2012
Novel Virulence Gene and Clustered Regularly Interspaced Short Palindromic Repeat (CRISPR) Multilocus Sequence Typing Scheme for Subtyping of the Major Serovars of Salmonella enterica subsp. enterica Liu, Fenyun; Barrangou, Rodolphe; Gerner-Smidt, Peter Applied and Environmental Microbiology, Vol. 77, Issue 6 https://doi.org/10.1128/aem.02625-10	journal	January 2011
Salmonella enterica Serovar Typhimurium Binds to HeLa Cells via Fim-Mediated Reversible Adhesion and Irreversible Type Three Secretion System 1-Mediated Docking Misselwitz, Benjamin; Kreibich, Saskia K.; Rout, Samuel Infection and Immunity, Vol. 79, Issue 1 https://doi.org/10.1128/iai.00581-10	journal	October 2010
Identification of a Putative Salmonella enterica Serotype Typhimurium Host Range Factor with Homology to IpaH and YopM by Signature-Tagged Mutagenesis Tsolis, Renée M.; Townsend, Stacy M.; Miao, Edward A. Infection and Immunity, Vol. 67, Issue 12 https://doi.org/10.1128/iai.67.12.6385-6393.1999	journal	December 1999
L-glutamine and L-asparagine stimulate Na+ -H+ exchange in porcine jejunal enterocytes Rhoads, J. M.; Chen, W.; Chu, P. American Journal of Physiology-Gastrointestinal and Liver Physiology, Vol. 266, Issue 5 https://doi.org/10.1152/ajpgi.1994.266.5.g828	journal	May 1994
Lipoprotein and apolipoprotein secretion by a newborn piglet intestinal cell line (IPEC-1) Gonzalez-Vallina, R.; Wang, H.; Zhan, R. American Journal of Physiology-Gastrointestinal and Liver Physiology, Vol. 271, Issue 2 https://doi.org/10.1152/ajpgi.1996.271.2.g249	journal	August 1996

Cited By (21)

Three-dimensional organotypic co-culture model of intestinal epithelial cells and macrophages to study Salmonella enterica colonization patterns Barrila, Jennifer; Yang, Jiseon; Crabbé, Aurélie npj Microgravity, Vol. 3, Issue 1 https://doi.org/10.1038/s41526-017-0011-2	journal	February 2017
Population genomics of bacterial host adaptation Sheppard, Samuel K.; Guttman, David S.; Fitzgerald, J. Ross Nature Reviews Genetics, Vol. 19, Issue 9 https://doi.org/10.1038/s41576-018-0032-z	journal	July 2018
Epigenome-Microbiome crosstalk: A potential new paradigm influencing neonatal susceptibility to disease Cortese, Rene; Lu, Lei; Yu, Yueyue Epigenetics, Vol. 11, Issue 3 https://doi.org/10.1080/15592294.2016.1155011	journal	February 2016
Comparative genomics reveals different population structures associated with host and geographic origin in antimicrobial-resistant Salmonella enterica Liao, Jingqiu; Orsi, Renato Hohl; Carroll, Laura bioRxiv https://doi.org/10.1101/2020.01.28.923664	posted_content	April 2020
Transcriptomic basis of genome by genome variation in a legume‐rhizobia mutualism Burghardt, Liana T.; Guhlin, Joseph; Chun, Chan Lan Molecular Ecology, Vol. 26, Issue 21 https://doi.org/10.1111/mec.14285	journal	September 2017
Diversified sources for human infections by Salmonella enterica serovar newport Pan, Hang; Zhou, Xin; Chai, Wenqin Transboundary and Emerging Diseases, Vol. 66, Issue 2 https://doi.org/10.1111/tbed.13099	journal	January 2019
Cooperation of Adhesin Alleles in Salmonella-Host Tropism De Masi, Leon; Yue, Min; Hu, Changmin mSphere, Vol. 2, Issue 2 https://doi.org/10.1128/msphere.00066-17	journal	March 2017
Association of Salmonella virulence factor alleles with intestinal and invasive serovars Rakov, Alexey V.; Mastriani, Emilio; Liu, Shu-Lin BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5809-8	journal	May 2019
A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance Jajere, Saleh Mohammed Veterinary World, Vol. 12, Issue 4 https://doi.org/10.14202/vetworld.2019.504-521	journal	April 2019
Comprehensive Analysis Reveals Two Distinct Evolution Patterns of Salmonella Flagellin Gene Clusters Liu, Yue; Zhang, Dao-Feng; Zhou, Xiujuan Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02604	journal	December 2017
Multiple Food-Animal-Borne Route in Transmission of Antibiotic-Resistant Salmonella Newport to Humans Pan, Hang; Paudyal, Narayan; Li, Xiaoliang Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00023	journal	January 2018
Embracing Diversity: Differences in Virulence Mechanisms, Disease Severity, and Host Adaptations Contribute to the Success of Nontyphoidal Salmonella as a Foodborne Pathogen Cheng, Rachel A.; Eade, Colleen R.; Wiedmann, Martin Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01368	journal	June 2019
Global Burden of Colistin-Resistant Bacteria: Mobilized Colistin Resistance Genes Study (1980–2018) Elbediwi, Mohammed; Li, Yan; Paudyal, Narayan Microorganisms, Vol. 7, Issue 10, p. 461 https://doi.org/10.3390/microorganisms7100461	journal	October 2019
Comparative genomics reveals different population structures associated with host and geographic origin in antimicrobial‐resistant Salmonella enterica Liao, Jingqiu; Orsi, Renato Hohl; Carroll, Laura M. Environmental Microbiology, Vol. 22, Issue 7 https://doi.org/10.1111/1462-2920.15014	journal	April 2020
Pan-genome Analysis of Ancient and Modern Salmonella enterica Demonstrates Genomic Stability of the Invasive Para C Lineage for Millennia Zhou, Zhemin; Lundstrøm, Inge; Tran-Dien, Alicia Current Biology, Vol. 28, Issue 15 https://doi.org/10.1016/j.cub.2018.05.058	journal	August 2018
A profile-based method for identifying functional divergence of orthologous genes in bacterial genomes Wheeler, Nicole E.; Barquist, Lars; Kingsley, Robert A. Bioinformatics, Vol. 32, Issue 23 https://doi.org/10.1093/bioinformatics/btw518	journal	August 2016
Zoonotic Source Attribution of Salmonella enterica Serotype Typhimurium Using Genomic Surveillance Data, United States Zhang, Shaokang; Li, Shaoting; Gu, Weidong Emerging Infectious Diseases, Vol. 25, Issue 1 https://doi.org/10.3201/eid2501.180835	journal	January 2019
The Novel Type 1 Fimbriae FimH Receptor Calreticulin Plays a Role in Salmonella Host Specificity Grzymajlo, Krzysztof; Ugorski, Maciej; Suchanski, Jaroslaw Frontiers in Cellular and Infection Microbiology, Vol. 7 https://doi.org/10.3389/fcimb.2017.00326	journal	July 2017
Allelic Variation in Outer Membrane Protein A and Its Influence on Attachment of Escherichia coli to Corn Stover Liao, Chunyu; Liang, Xiao; Yang, Fan Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00708	journal	May 2017
Polyphyletic Nature of Salmonella enterica Serotype Derby and Lineage-Specific Host-Association Revealed by Genome-Wide Analysis Sévellec, Yann; Vignaud, Marie-Léone; Granier, Sophie A. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00891	journal	May 2018
Adhesion of Salmonella to Pancreatic Secretory Granule Membrane Major Glycoprotein GP2 of Human and Porcine Origin Depends on FimH Sequence Variation Kolenda, Rafał; Burdukiewicz, Michał; Schiebel, Juliane Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01905	journal	August 2018

Similar Records

Diversification of the Salmonella Fimbriae: A Model of Macro- and Microevolution

Journal Article · Tue Jun 12 00:00:00 EDT 2012 · PLoS ONE · OSTI ID:1258603

Yue, Min; Rankin, Shelley C.; Blanchet, Ryan T.; +3 more

Genotypic and Phenotypic Characterization of Incompatibility Group FIB Positive Salmonella enterica Serovar Typhimurium Isolates from Food Animal Sources

Journal Article · Wed Nov 04 00:00:00 EST 2020 · Genes · OSTI ID:1258603

Aljahdali, Nesreen H.; Khajanchi, Bijay K.; Weston, Kennedi; +8 more

The genetic basis of phage susceptibility, cross-resistance and host-range in Salmonella

Journal Article · Wed Dec 15 00:00:00 EST 2021 · Microbiology · OSTI ID:1258603

Adler, Benjamin A.; Kazakov, Alexey E.; Zhong, Crystal; +8 more

Related Subjects

60 APPLIED LIFE SCIENCES

Title: Allelic variation contributes to bacterial host specificity

Citation Formats

References (62)

Cited By (21)

Similar Records

Related Subjects