Allelic variation contributes to bacterial host specificity
Abstract
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.
- Authors:
-
[9];
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- 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)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1258603
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Volume: 6; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES
Citation Formats
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., and Schifferli, Dieter M. Allelic variation contributes to bacterial host specificity. United States: N. p., 2015.
Web. doi:10.1038/ncomms9754.
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. Allelic variation contributes to bacterial host specificity. United States. https://doi.org/10.1038/ncomms9754
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., and Schifferli, Dieter M. Fri .
"Allelic variation contributes to bacterial host specificity". United States. https://doi.org/10.1038/ncomms9754. https://www.osti.gov/servlets/purl/1258603.
@article{osti_1258603,
title = {Allelic variation contributes to bacterial host specificity},
author = {Yue, Min and Han, Xiangan and Masi, Leon De and Zhu, Chunhong and Ma, Xun and Zhang, Junjie and Wu, Renwei and Schmieder, Robert and Kaushik, Radhey S. and Fraser, George P. and Zhao, Shaohua and McDermott, Patrick F. and Weill, François-Xavier and Mainil, Jacques G. and Arze, Cesar and Fricke, W. Florian and Edwards, Robert A. and Brisson, Dustin and Zhang, Nancy R. and Rankin, Shelley C. and Schifferli, Dieter M.},
abstractNote = {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.},
doi = {10.1038/ncomms9754},
journal = {Nature Communications},
number = ,
volume = 6,
place = {United States},
year = {Fri Oct 30 00:00:00 EDT 2015},
month = {Fri Oct 30 00:00:00 EDT 2015}
}
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DnaSP v5: a software for comprehensive analysis of DNA polymorphism data
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Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology
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journal, November 2013
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journal, March 2013
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FimH alleles direct preferential binding of Salmonella to distinct mammalian cells or to avian cells
journal, April 2009
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The high-adhesive properties of the FimH adhesin of Salmonella enterica serovar Enteritidis are determined by a single F118S substitution
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Immunochemical, biomolecular and biochemical characterization of bovine epithelial intestinal primocultures
journal, January 2005
- Rusu, Dorina; Loret, Suzanne; Peulen, Olivier
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Genome wide evolutionary analyses reveal serotype specific patterns of positive selection in selected Salmonella serotypes
journal, January 2009
- Soyer, Yeşim; Orsi, Renato H.; Rodriguez-Rivera, Lorraine D.
- BMC Evolutionary Biology, Vol. 9, Issue 1
Invasive Non-Typhoidal Salmonella Typhimurium ST313 Are Not Host-Restricted and Have an Invasive Phenotype in Experimentally Infected Chickens
journal, October 2013
- Parsons, Bryony N.; Humphrey, Suzanne; Salisbury, Anne Marie
- PLoS Neglected Tropical Diseases, Vol. 7, Issue 10
progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement
journal, June 2010
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- PLoS ONE, Vol. 5, Issue 6
MultiPhen: Joint Model of Multiple Phenotypes Can Increase Discovery in GWAS
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- PLoS ONE, Vol. 7, Issue 5
Diversification of the Salmonella Fimbriae: A Model of Macro- and Microevolution
journal, June 2012
- Yue, Min; Rankin, Shelley C.; Blanchet, Ryan T.
- PLoS ONE, Vol. 7, Issue 6
Evolution of Salmonella enterica Virulence via Point Mutations in the Fimbrial Adhesin
journal, June 2012
- Kisiela, Dagmara I.; Chattopadhyay, Sujay; Libby, Stephen J.
- PLoS Pathogens, Vol. 8, Issue 6
Role of receptor binding specificity in influenza A virus transmission and pathogenesis
journal, July 2014
- Graaf, Miranda; Fouchier, Ron A. M.
- The EMBO Journal, Vol. 33, Issue 14
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