Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 25, Number 1—January 2019
Research

Zoonotic Source Attribution of Salmonella enterica Serotype Typhimurium Using Genomic Surveillance Data, United States

Shaokang Zhang, Shaoting Li, Weidong Gu, Henk den Bakker, Dave Boxrud, Angie Taylor, Chandler Roe, Elizabeth Driebe, David M. Engelthaler, Marc Allard, Eric Brown, Patrick McDermott, Shaohua Zhao, Beau B. Bruce, Eija Trees, Patricia I. Fields, and Xiangyu DengComments to Author 
Author affiliations: University of Georgia Center for Food Safety, Griffin, Georgia, USA (S. Zhang, S. Li, H. den Bakker, X. Deng); Centers for Disease Control and Prevention, Atlanta, Georgia, USA (W. Gu, B.B. Bruce, E. Trees, P.I. Fields); Minnesota Department of Health, St. Paul, Minnesota, USA (D. Boxrud, A. Taylor); Translational Genomics Research Institute, Flagstaff, Arizona, USA (C. Roe, E. Driebe, D.M. Engelthaler); US Food and Drug Administration, College Park, Maryland, USA (M. Allard, E.W. Brown); US Food and Drug Administration, Laurel, Maryland, USA (P. McDermott, S. Zhao)

Main Article

Table 2

Selected key genetic features for zoonotic source prediction of Salmonella enterica serotype Typhimurium using a Random Forest classifier

Feature rank* Affected gene Feature type Gene function (reference)
1 fliC Single-nucleotide polymorphism Motility, serotype diversity, intestinal colonization (16)
5 traA Accessory gene Pilin precursor. intestinal colonization (16)
6 spvB Accessory gene Virulence (17), intestinal colonization (16)
9 1930† Accessory gene Intestinal colonization (16)
11 1874† Indel Intestinal colonization (16)
13–15, 28 cusCFBA Accessory gene Putative copper efflux system (18)
16 silP Accessory gene Silver efflux pump (17)
21 yafA Accessory gene Intestinal colonization (16)
24 sspH2 Accessory gene Virulence and potential host range factor (19)
27 0286A† Accessory gene Intestinal colonization (16)
31 pipB2 Accessory gene Virulence (20)
32 proQ Accessory gene Global posttranscription regulation (21), intestinal colonization (16)
34 spvD Accessory gene Virulence (22)
37 Trap Accessory gene Intestinal colonization (16)
39 yhfL Indel Intestinal colonization (16)
41 0835† Accessory gene Intestinal colonization (16)
43 traJ Accessory gene Intestinal colonization (16)
45 yceA Accessory gene Intestinal colonization (16)
46 exc Accessory gene Intestinal colonization (16)

*Features are ranked by the mean decrease of prediction accuracy through randomly permuting values of the feature. The larger the mean decrease, the higher the rank. Only features that are located in genes that have reported involvement in intestinal colonization, virulence, and other functions related to livestock environment adaptation are listed. The full list of analyzed features, including the top 50 for zoonotic source prediction, is provided in Appendix 1 Table 6. Indel, insertion/deletion.
†Locus identification of the reference genome SL1344.

Main Article

References
  1. Scallan  E, Hoekstra  RM, Angulo  FJ, Tauxe  RV, Widdowson  MA, Roy  SL, et al. Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis. 2011;17:715. DOIPubMedGoogle Scholar
  2. Hoffmann  S, Maculloch  B, Batz  M. Economic burden of major foodborne illnesses acquired in the United States [cited 2018 Oct 8]. https://www.ers.usda.gov/webdocs/publications/43984/52807_eib140.pdf
  3. Hendriksen  RS, Vieira  AR, Karlsmose  S, Lo Fo Wong  DM, Jensen  AB, Wegener  HC, et al. Global monitoring of Salmonella serovar distribution from the World Health Organization Global Foodborne Infections Network Country Data Bank: results of quality assured laboratories from 2001 to 2007. Foodborne Pathog Dis. 2011;8:887900. DOIPubMedGoogle Scholar
  4. Rabsch  W, Andrews  HL, Kingsley  RA, Prager  R, Tschäpe  H, Adams  LG, et al. Salmonella enterica serotype Typhimurium and its host-adapted variants. Infect Immun. 2002;70:224955. DOIPubMedGoogle Scholar
  5. Helms  M, Ethelberg  S, Mølbak  K; DT104 Study Group. International Salmonella Typhimurium DT104 infections, 1992-2001. Emerg Infect Dis. 2005;11:85967. DOIPubMedGoogle Scholar
  6. Okoro  CK, Kingsley  RA, Connor  TR, Harris  SR, Parry  CM, Al-Mashhadani  MN, et al. Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nat Genet. 2012;44:121521. DOIPubMedGoogle Scholar
  7. Graham  SM. Nontyphoidal salmonellosis in Africa. Curr Opin Infect Dis. 2010;23:40914. DOIPubMedGoogle Scholar
  8. Yue  M, Han  X, De Masi  L, Zhu  C, Ma  X, Zhang  J, et al. Allelic variation contributes to bacterial host specificity. Nat Commun. 2015;6:8754. DOIPubMedGoogle Scholar
  9. Chaudhuri  RR, Morgan  E, Peters  SE, Pleasance  SJ, Hudson  DL, Davies  HM, et al. Comprehensive assignment of roles for Salmonella typhimurium genes in intestinal colonization of food-producing animals. PLoS Genet. 2013;9:e1003456. DOIPubMedGoogle Scholar
  10. Pires  SM, Evers  EG, van Pelt  W, Ayers  T, Scallan  E, Angulo  FJ, et al.; Med-Vet-Net Workpackage 28 Working Group. Attributing the human disease burden of foodborne infections to specific sources. Foodborne Pathog Dis. 2009;6:41724. DOIPubMedGoogle Scholar
  11. Hald  T, Vose  D, Wegener  HC, Koupeev  T. A Bayesian approach to quantify the contribution of animal-food sources to human salmonellosis. Risk Anal. 2004;24:25569. DOIPubMedGoogle Scholar
  12. Barco  L, Barrucci  F, Olsen  JE, Ricci  A. Salmonella source attribution based on microbial subtyping. Int J Food Microbiol. 2013;163:193203. DOIPubMedGoogle Scholar
  13. Swaminathan  B, Barrett  TJ, Hunter  SB, Tauxe  RV; CDC PulseNet Task Force. PulseNet: the molecular subtyping network for foodborne bacterial disease surveillance, United States. Emerg Infect Dis. 2001;7:3829. DOIPubMedGoogle Scholar
  14. Allard  MW, Strain  E, Melka  D, Bunning  K, Musser  SM, Brown  EW, et al. Practical value of food pathogen traceability through building a whole-genome sequencing network and database. J Clin Microbiol. 2016;54:197583. DOIPubMedGoogle Scholar
  15. Zhang  S, Yin  Y, Jones  MB, Zhang  Z, Deatherage Kaiser  BL, Dinsmore  BA, et al. Salmonella serotype determination utilizing high-throughput genome sequencing data. J Clin Microbiol. 2015;53:168592. DOIPubMedGoogle Scholar
  16. Chaudhuri  RR, Morgan  E, Peters  SE, Pleasance  SJ, Hudson  DL, Davies  HM, et al. Comprehensive assignment of roles for Salmonella typhimurium genes in intestinal colonization of food-producing animals. PLoS Genet. 2013;9:e1003456. DOIPubMedGoogle Scholar
  17. Gupta  A, Matsui  K, Lo  JF, Silver  S. Molecular basis for resistance to silver cations in Salmonella. Nat Med. 1999;5:1838. DOIPubMedGoogle Scholar
  18. Franke  S, Grass  G, Rensing  C, Nies  DH. Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. J Bacteriol. 2003;185:380412. DOIPubMedGoogle Scholar
  19. Tsolis  RM, Townsend  SM, Miao  EA, Miller  SI, Ficht  TA, Adams  LG, et al. Identification of a putative Salmonella enterica serotype typhimurium host range factor with homology to IpaH and YopM by signature-tagged mutagenesis. Infect Immun. 1999;67:638593.PubMedGoogle Scholar
  20. Henry  T, Couillault  C, Rockenfeller  P, Boucrot  E, Dumont  A, Schroeder  N, et al. The Salmonella effector protein PipB2 is a linker for kinesin-1. Proc Natl Acad Sci U S A. 2006;103:13497502. DOIPubMedGoogle Scholar
  21. Smirnov  A, Förstner  KU, Holmqvist  E, Otto  A, Günster  R, Becher  D, et al. Grad-seq guides the discovery of ProQ as a major small RNA-binding protein. Proc Natl Acad Sci U S A. 2016;113:115916. DOIPubMedGoogle Scholar
  22. Grabe  GJ, Zhang  Y, Przydacz  M, Rolhion  N, Yang  Y, Pruneda  JN, et al. The Salmonella effector SpvD Is a cysteine hydrolase with a serovar-specific polymorphism influencing catalytic activity, suppression of immune responses, and bacterial virulence. J Biol Chem. 2016;291:2585363. DOIPubMedGoogle Scholar
  23. Lesnick  ML, Reiner  NE, Fierer  J, Guiney  DG. The Salmonella spvB virulence gene encodes an enzyme that ADP-ribosylates actin and destabilizes the cytoskeleton of eukaryotic cells. Mol Microbiol. 2001;39:146470. DOIPubMedGoogle Scholar
  24. Yazdankhah  S, Rudi  K, Bernhoft  A. Zinc and copper in animal feed - development of resistance and co-resistance to antimicrobial agents in bacteria of animal origin. Microb Ecol Health Dis. 2014;25:25.PubMedGoogle Scholar
  25. Gupta  A, Silver  S. Silver as a biocide: will resistance become a problem? Nat Biotechnol. 1998;16:888. DOIPubMedGoogle Scholar
  26. Thomson  NR, Clayton  DJ, Windhorst  D, Vernikos  G, Davidson  S, Churcher  C, et al. Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res. 2008;18:162437. DOIPubMedGoogle Scholar
  27. Holt  KE, Thomson  NR, Wain  J, Langridge  GC, Hasan  R, Bhutta  ZA, et al. Pseudogene accumulation in the evolutionary histories of Salmonella enterica serovars Paratyphi A and Typhi. BMC Genomics. 2009;10:36. DOIPubMedGoogle Scholar
  28. Langridge  GC, Fookes  M, Connor  TR, Feltwell  T, Feasey  N, Parsons  BN, et al. Patterns of genome evolution that have accompanied host adaptation in Salmonella. Proc Natl Acad Sci U S A. 2015;112:8638. DOIPubMedGoogle Scholar
  29. Feasey  NA, Hadfield  J, Keddy  KH, Dallman  TJ, Jacobs  J, Deng  X, et al. Distinct Salmonella Enteritidis lineages associated with enterocolitis in high-income settings and invasive disease in low-income settings. Nat Genet. 2016;48:12117. DOIPubMedGoogle Scholar
  30. Deng  X, Desai  PT, den Bakker  HC, Mikoleit  M, Tolar  B, Trees  E, et al. Genomic epidemiology of Salmonella enterica serotype Enteritidis based on population structure of prevalent lineages. Emerg Infect Dis. 2014;20:14819. DOIPubMedGoogle Scholar
  31. Lupolova  N, Dallman  TJ, Matthews  L, Bono  JL, Gally  DL. Support vector machine applied to predict the zoonotic potential of E. coli O157 cattle isolates. Proc Natl Acad Sci U S A. 2016;113:113127. DOIPubMedGoogle Scholar
  32. Lupolova  N, Dallman  TJ, Holden  NJ, Gally  DL. Patchy promiscuity: machine learning applied to predict the host specificity of Salmonella enterica and Escherichia coli. Microb Genom. 2017;3:e000135. DOIPubMedGoogle Scholar
  33. Hanning  IB, Nutt  JD, Ricke  SC. Salmonellosis outbreaks in the United States due to fresh produce: sources and potential intervention measures. Foodborne Pathog Dis. 2009;6:63548. DOIPubMedGoogle Scholar

Main Article

Page created: December 18, 2018
Page updated: December 18, 2018
Page reviewed: December 18, 2018
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external