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Volume 4, Issue 8

Comparative genomics of Salmonella enterica serovar Montevideo reveals lineage-specific gene differences that may influence ecological niche association Open Access

Abstract

Salmonella enterica serovar Montevideo has been linked to recent foodborne illness outbreaks resulting from contamination of products such as fruits, vegetables, seeds and spices. Studies have shown that Montevideo also is frequently associated with healthy cattle and can be isolated from ground beef, yet human salmonellosis outbreaks of Montevideo associated with ground beef contamination are rare. This disparity fuelled our interest in characterizing the genomic differences between Montevideo strains isolated from healthy cattle and beef products, and those isolated from human patients and outbreak sources. To that end, we sequenced 13 Montevideo strains to completion, producing high-quality genome assemblies of isolates from human patients (n=8) or from healthy cattle at slaughter (n=5). Comparative analysis of sequence data from this study and publicly available sequences (n=72) shows that Montevideo falls into four previously established clades, differentially occupied by cattle and human strains. The results of these analyses reveal differences in metabolic islands, environmental adhesion determinants and virulence factors within each clade, and suggest explanations for the infrequent association between bovine isolates and human illnesses.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): cattle , comparative genomics , CRISPR-Cas , phylogenetic and Salmonella enterica serovar Montevideo
© Microbiology Society
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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2018-07-27
2024-04-20
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References

  1. Chen L, Zheng D, Liu B, Yang J, Jin Q. VFDB 2016: hierarchical and refined dataset for big data analysis—10 years on. Nucleic Acids Res 2016; 44:D694–D697 [View Article]
     [Google Scholar]
  2. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA et al. Foodborne illness acquired in the United States–major pathogens. Emerg Infect Dis 2011; 17:7–15 [View Article][PubMed]
     [Google Scholar]
  3. CDC National Salmonella Surveillance Overview Atlanta, GA: US Department of Health and Human Services, CDC; 2011
     [Google Scholar]
  4. Stevens EL, Timme R, Brown EW, Allard MW, Strain E et al. The public health impact of a publically available, environmental database of microbial genomes. Front Microbiol 2017; 8:808 [View Article][PubMed]
     [Google Scholar]
  5. CDC National Salmonella Surveillance Annual Report, 2014 Atlanta, GA: US Department of Health and Human Services, CDC; 2017
     [Google Scholar]
  6. Gieraltowski L, Julian E, Pringle J, Macdonald K, Quilliam D et al. Nationwide outbreak of Salmonella Montevideo infections associated with contaminated imported black and red pepper: warehouse membership cards provide critical clues to identify the source. Epidemiol Infect 2013; 141:1244–1252 [View Article][PubMed]
     [Google Scholar]
  7. Centers for Disease Control and Prevention (CDC) Salmonella montevideo infections associated with salami products made with contaminated imported black and red pepper – United States, July 2009-April 2010. MMWR Morb Mortal Wkly Rep 2010; 59:1647–1650[PubMed]
     [Google Scholar]
  8. Unicomb LE, Simmons G, Merritt T, Gregory J, Nicol C et al. Sesame seed products contaminated with Salmonella: three outbreaks associated with tahini. Epidemiol Infect 2005; 133:1065–1072 [View Article][PubMed]
     [Google Scholar]
  9. Allard MW, Luo Y, Strain E, Li C, Keys CE et al. High resolution clustering of Salmonella enterica serovar Montevideo strains using a next-generation sequencing approach. BMC Genomics 2012; 13:32 [View Article][PubMed]
     [Google Scholar]
  10. Gragg SE, Loneragan GH, Brashears MM, Arthur TM, Bosilevac JM et al. Cross-sectional study examining Salmonella enterica carriage in subiliac lymph nodes of cull and feedlot cattle at harvest. Foodborne Pathog Dis 2013; 10:368–374 [View Article][PubMed]
     [Google Scholar]
  11. Bosilevac JM, Guerini MN, Kalchayanand N, Koohmaraie M. Prevalence and characterization of Salmonellae in commercial ground beef in the United States. Appl Environ Microbiol 2009; 75:1892–1900 [View Article][PubMed]
     [Google Scholar]
  12. Center for Disease Control and Prevention 2011 Foodborne Outbreak Online Database Atlanta, GA: US Department of Health and Human Services, CDC; https://wwwn.cdc.gov/norsdashboard/ accessed 17 July 2017
    [Google Scholar]
  13. Harhay DM, Bono JL, Smith TP, Fields PI, Dinsmore BA et al. Complete closed genome sequences of Salmonella enterica subsp. enterica serotypes Anatum, Montevideo, Typhimurium, and Newport, isolated from beef, cattle, and humans. Genome Announc 2016; 4:e01683-15 [View Article][PubMed]
     [Google Scholar]
  14. Bertelli C, Laird MR, Williams KP, Lau BY, Hoad G et al. IslandViewer 4: expanded prediction of genomic islands for larger-scale datasets. Nucleic Acids Res 2017; 45:W30–W35 [View Article][PubMed]
     [Google Scholar]
  15. Chatterjee R, Chaudhuri K, Chaudhuri P. On detection and assessment of statistical significance of Genomic Islands. BMC Genomics 2008; 9:150 [View Article][PubMed]
     [Google Scholar]
  16. Fàbrega A, Vila J. Salmonella enterica serovar Typhimurium skills to succeed in the host: virulence and regulation. Clin Microbiol Rev 2013; 26:308–341 [View Article][PubMed]
     [Google Scholar]
  17. Garai P, Gnanadhas DP, Chakravortty D. Salmonella enterica serovars Typhimurium and Typhi as model organisms: revealing paradigm of host-pathogen interactions. Virulence 2012; 3:377–388 [View Article][PubMed]
     [Google Scholar]
  18. Whitaker RJ, Vanderpool CK. CRISPR-Cas gatekeeper: slow on the uptake but gets the job done. Cell Host Microbe 2016; 19:135–137 [View Article][PubMed]
     [Google Scholar]
  19. Naderer M, Brust JR, Knowle D, Blumenthal RM. Mobility of a restriction-modification system revealed by its genetic contexts in three hosts. J Bacteriol 2002; 184:2411–2419 [View Article][PubMed]
     [Google Scholar]
  20. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007; 315:1709–1712 [View Article][PubMed]
     [Google Scholar]
  21. Vasu K, Nagaraja V. Diverse functions of restriction-modification systems in addition to cellular defense. Microbiol Mol Biol Rev 2013; 77:53–72 [View Article][PubMed]
     [Google Scholar]
  22. Gao F, Zhang CT. Ori-Finder: a web-based system for finding oriCs in unannotated bacterial genomes. BMC Bioinformatics 2008; 9:79 [View Article][PubMed]
     [Google Scholar]
  23. Tatusova T, Dicuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article][PubMed]
     [Google Scholar]
  24. Roberts RJ, Vincze T, Posfai J, Macelis D. REBASE–a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Res 2015; 43:D298–D299 [View Article][PubMed]
     [Google Scholar]
  25. Treangen TJ, Ondov BD, Koren S, Phillippy AM. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 2014; 15:524 [View Article][PubMed]
     [Google Scholar]
  26. Alikhan NF, Zhou Z, Sergeant MJ, Achtman M. A genomic overview of the population structure of Salmonella. PLoS Genet 2018; 14:e1007261 [View Article][PubMed]
     [Google Scholar]
  27. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010; 5:e11147 [View Article][PubMed]
     [Google Scholar]
  28. Darling AE, Treangen TJ, Messeguer X, Perna NT. Analyzing patterns of microbial evolution using the mauve genome alignment system. Methods Mol Biol 2007; 396:135–152 [View Article][PubMed]
     [Google Scholar]
  29. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics 2011; 27:1009–1010 [View Article][PubMed]
     [Google Scholar]
  30. Arndt D, Grant JR, Marcu A, Sajed T, Pon A et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 2016; 44:W16–W21 [View Article][PubMed]
     [Google Scholar]
  31. Betley JN, Frith MC, Graber JH, Choo S, Deshler JO. A ubiquitous and conserved signal for RNA localization in chordates. Curr Biol 2002; 12:1756–1761 [View Article][PubMed]
     [Google Scholar]
  32. Stothard P, Grant JR, van Domselaar G. Visualizing and comparing circular genomes using the CGView family of tools. Brief Bioinform 2017 [View Article][PubMed]
     [Google Scholar]
  33. Grant JR, Stothard P. The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Res 2008; 36:W181–W184 [View Article][PubMed]
     [Google Scholar]
  34. Biswas A, Staals RH, Morales SE, Fineran PC, Brown CM. CRISPRDetect: a flexible algorithm to define CRISPR arrays. BMC Genomics 2016; 17:356 [View Article][PubMed]
     [Google Scholar]
  35. Biswas A, Gagnon JN, Brouns SJ, Fineran PC, Brown CM. CRISPRTarget: bioinformatic prediction and analysis of crRNA targets. RNA Biol 2013; 10:817–827 [View Article][PubMed]
     [Google Scholar]
  36. Shariat N, Timme RE, Pettengill JB, Barrangou R, Dudley EG. Characterization and evolution of Salmonella CRISPR-Cas systems. Microbiology 2015; 161:374–386 [View Article][PubMed]
     [Google Scholar]
  37. Frossard SM, Khan AA, Warrick EC, Gately JM, Hanson AD et al. Identification of a third osmoprotectant transport system, the osmU system, in Salmonella enterica. J Bacteriol 2012; 194:3861–3871 [View Article][PubMed]
     [Google Scholar]
  38. Randall LP, Woodward MJ. The multiple antibiotic resistance (mar) locus and its significance. Res Vet Sci 2002; 72:87–93 [View Article][PubMed]
     [Google Scholar]
  39. Sánchez-Carrón G, Martínez-Moñino AB, Sola-Carvajal A, Takami H, García-Carmona F et al. New insights into the phylogeny and molecular classification of nicotinamide mononucleotide deamidases. PLoS One 2013; 8:e82705 [View Article][PubMed]
     [Google Scholar]
  40. Zhang S, Santos RL, Tsolis RM, Mirold S, Hardt WD et al. Phage mediated horizontal transfer of the sopE1 gene increases enteropathogenicity of Salmonella enterica serotype Typhimurium for calves. FEMS Microbiol Lett 2002; 217:243–247 [View Article][PubMed]
     [Google Scholar]
  41. Pelludat C, Mirold S, Hardt WD. The SopEPhi phage integrates into the ssrA gene of Salmonella enterica serovar Typhimurium A36 and is closely related to the Fels-2 prophage. J Bacteriol 2003; 185:5182–5191 [View Article][PubMed]
     [Google Scholar]
  42. Staehlin BM, Gibbons JG, Rokas A, O'Halloran TV, Slot JC. Evolution of a heavy metal homeostasis/resistance island reflects increasing copper stress in Enterobacteria. Genome Biol Evol 2016; 8:evw031 [View Article][PubMed]
     [Google Scholar]
  43. Ong CL, Beatson SA, Totsika M, Forestier C, McEwan AG et al. Molecular analysis of type 3 fimbrial genes from Escherichia coli, Klebsiella and Citrobacter species. BMC Microbiol 2010; 10:183 [View Article][PubMed]
     [Google Scholar]
  44. Seth-Smith HM, Fookes MC, Okoro CK, Baker S, Harris SR et al. Structure, diversity, and mobility of the Salmonella pathogenicity island 7 family of integrative and conjugative elements within Enterobacteriaceae. J Bacteriol 2012; 194:1494–1504 [View Article][PubMed]
     [Google Scholar]
  45. Yue M, Rankin SC, Blanchet RT, Nulton JD, Edwards RA et al. Diversification of the Salmonella fimbriae: a model of macro- and microevolution. PLoS One 2012; 7:e38596 [View Article][PubMed]
     [Google Scholar]
  46. Joerger RD, Hanning IB, Ricke SC. Presence of arsenic resistance in Salmonella enterica serovar Kentucky and other serovars isolated from poultry. Avian Dis 2010; 54:1178–1182 [View Article][PubMed]
     [Google Scholar]
  47. Nolle N, Felsl A, Heermann R, Fuchs TM. Genetic characterization of the galactitol utilization pathway of Salmonella enterica serovar Typhimurium. J Bacteriol 2017; 199:e00595-16 [View Article][PubMed]
     [Google Scholar]
  48. Marzel A, Desai PT, Nissan I, Schorr YI, Suez J et al. Integrative analysis of Salmonellosis in Israel reveals association of Salmonella enterica serovar 9,12:l,v:- with extraintestinal infections, dissemination of endemic S. enterica serovar Typhimurium DT104 biotypes, and severe underreporting of outbreaks. J Clin Microbiol 2014; 52:2078–2088 [View Article][PubMed]
     [Google Scholar]
  49. Thomson NR, Clayton DJ, Windhorst D, Vernikos G, Davidson S 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; 18:1624–1637 [View Article][PubMed]
     [Google Scholar]
  50. Coward C, Sait L, Williams L, Humphrey TJ, Cogan T et al. Investigation into the role of five Salmonella enterica serovar Enteritidis genomic islands in colonization of the chicken reproductive tract and other organs following oral challenge. FEMS Microbiol Lett 2012; 336:73–78 [View Article][PubMed]
     [Google Scholar]
  51. Matiasovicova J, Havlickova H, Sisak F, Pilousova L, Rychlik I. allB, allantoin utilisation and Salmonella enterica serovar Enteritidis and Typhimurium colonisation of poultry and mice. Folia Microbiol 2011; 56:264–269 [View Article][PubMed]
     [Google Scholar]
  52. Chou HC, Lee CZ, Ma LC, Fang CT, Chang SC et al. Isolation of a chromosomal region of Klebsiella pneumoniae associated with allantoin metabolism and liver infection. Infect Immun 2004; 72:3783–3792 [View Article][PubMed]
     [Google Scholar]
  53. Reizer J, Reizer A, Saier MH. Novel phosphotransferase system genes revealed by bacterial genome analysis–a gene cluster encoding a unique Enzyme I and the proteins of a fructose-like permease system. Microbiology 1995; 141:961–971 [View Article][PubMed]
     [Google Scholar]
  54. Porwollik S, Wong RM, McClelland M. Evolutionary genomics of Salmonella: gene acquisitions revealed by microarray analysis. Proc Natl Acad Sci USA 2002; 99:8956–8961 [View Article][PubMed]
     [Google Scholar]
  55. Porwollik S, McClelland M. Lateral gene transfer in Salmonella. Microbes Infect 2003; 5:977–989 [View Article][PubMed]
     [Google Scholar]
  56. Kröger C, Fuchs TM. Characterization of the myo-inositol utilization island of Salmonella enterica serovar Typhimurium. J Bacteriol 2009; 191:545–554 [View Article][PubMed]
     [Google Scholar]
  57. Rotger R, Casadesús J. The virulence plasmids of Salmonella. Int Microbiol 1999; 2:177–184[PubMed]
     [Google Scholar]
  58. Hensel M. Evolution of pathogenicity islands of Salmonella enterica. Int J Med Microbiol 2004; 294:95–102 [View Article][PubMed]
     [Google Scholar]
  59. Hardt WD, Galán JE. A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria. Proc Natl Acad Sci USA 1997; 94:9887–9892 [View Article][PubMed]
     [Google Scholar]
  60. Lalsiamthara J, Lee JH. Pathogenic traits of Salmonella Montevideo in experimental infections in vivo and in vitro. Sci Rep 2017; 7:46232 [View Article][PubMed]
     [Google Scholar]
  61. Blanc-Potard AB, Solomon F, Kayser J, Groisman EA. The SPI-3 pathogenicity island of Salmonella enterica. J Bacteriol 1999; 181:998–1004[PubMed]
     [Google Scholar]
  62. Knodler LA, Vallance BA, Hensel M, Jäckel D, Finlay BB et al. Salmonella type III effectors PipB and PipB2 are targeted to detergent-resistant microdomains on internal host cell membranes. Mol Microbiol 2003; 49:685–704 [View Article][PubMed]
     [Google Scholar]
  63. Mulder DT, Cooper CA, Coombes BK. Type VI secretion system-associated gene clusters contribute to pathogenesis of Salmonella enterica serovar Typhimurium. Infect Immun 2012; 80:1996–2007 [View Article][PubMed]
     [Google Scholar]
  64. Figueira R, Holden DW. Functions of the Salmonella pathogenicity island 2 (SPI-2) type III secretion system effectors. Microbiology 2012; 158:1147–1161 [View Article][PubMed]
     [Google Scholar]
  65. Kingsley RA, Humphries AD, Weening EH, de Zoete MR, Winter S et al. Molecular and phenotypic analysis of the CS54 island of Salmonella enterica serotype Typhimurium: identification of intestinal colonization and persistence determinants. Infect Immun 2003; 71:629–640 [View Article][PubMed]
     [Google Scholar]
  66. Rajashekar R, Liebl D, Chikkaballi D, Liss V, Hensel M. Live cell imaging reveals novel functions of Salmonella enterica SPI2-T3SS effector proteins in remodeling of the host cell endosomal system. PLoS One 2014; 9:e115423 [View Article][PubMed]
     [Google Scholar]
  67. Sly LM, Guiney DG, Reiner NE. Salmonella enterica serovar Typhimurium periplasmic superoxide dismutases SodCI and SodCII are required for protection against the phagocyte oxidative burst. Infect Immun 2002; 70:5312–5315 [View Article][PubMed]
     [Google Scholar]
  68. Miller RA, Wiedmann M. The cytolethal distending toxin produced by nontyphoidal Salmonella serotypes Javiana, Montevideo, Oranienburg, and Mississippi induces DNA damage in a manner similar to that of serotype typhi. MBio 2016; 7:e02109-16 [View Article]
     [Google Scholar]
  69. Rodriguez-Rivera LD, Bowen BM, den Bakker HC, Duhamel GE, Wiedmann M. Characterization of the cytolethal distending toxin (typhoid toxin) in non-typhoidal Salmonella serovars. Gut Pathog 2015; 7:19 [View Article][PubMed]
     [Google Scholar]
  70. Ho TD, Figueroa-Bossi N, Wang M, Uzzau S, Bossi L et al. Identification of GtgE, a novel virulence factor encoded on the Gifsy-2 bacteriophage of Salmonella enterica serovar Typhimurium. J Bacteriol 2002; 184:5234–5239[PubMed]
     [Google Scholar]
  71. D'Costa VM, Braun V, Landekic M, Shi R, Proteau A et al. Salmonella disrupts host endocytic trafficking by SopD2-mediated inhibition of Rab7. Cell Rep 2015; 12:1508–1518 [View Article][PubMed]
     [Google Scholar]
  72. Weening EH, Barker JD, Laarakker MC, Humphries AD, Tsolis RM et al. The Salmonella enterica serotype Typhimurium lpf, bcf, stb, stc, std, and sth fimbrial operons are required for intestinal persistence in mice. Infect Immun 2005; 73:3358–3366 [View Article][PubMed]
     [Google Scholar]
  73. Xia P, Song Y, Zou Y, Yang Y, Zhu G. F4+ enterotoxigenic Escherichia coli (ETEC) adhesion mediated by the major fimbrial subunit FaeG. J Basic Microbiol 2015; 55:1118–1124 [View Article][PubMed]
     [Google Scholar]
  74. Aviv G, Elpers L, Mikhlin S, Cohen H, Vitman Zilber S et al. The plasmid-encoded Ipf and Klf fimbriae display different expression and varying roles in the virulence of Salmonella enterica serovar Infantis in mouse vs. avian hosts. PLoS Pathog 2017; 13:e1006559 [View Article][PubMed]
     [Google Scholar]
  75. Medina-Aparicio L, Rebollar-Flores JE, Gallego-Hernández AL, Vázquez A, Olvera L et al. The CRISPR/Cas immune system is an operon regulated by LeuO, H-NS, and leucine-responsive regulatory protein in Salmonella enterica serovar Typhi. J Bacteriol 2011; 193:2396–2407 [View Article][PubMed]
     [Google Scholar]
  76. Medina-Aparicio L, Rebollar-Flores JE, Beltrán-Luviano AA, Vázquez A, Gutiérrez-Ríos RM et al. CRISPR-Cas system presents multiple transcriptional units including antisense RNAs that are expressed in minimal medium and upregulated by pH in Salmonella enterica serovar Typhi. Microbiology 2017; 163:253–265 [View Article][PubMed]
     [Google Scholar]
  77. Pirone-Davies C, Hoffmann M, Roberts RJ, Muruvanda T, Timme RE et al. Genome-wide methylation patterns in Salmonella enterica subsp. enterica serovars. PLoS One 2015; 10:e0123639 [View Article][PubMed]
     [Google Scholar]
  78. Thiaville JJ, Kellner SM, Yuan Y, Hutinet G, Thiaville PC et al. Novel genomic island modifies DNA with 7-deazaguanine derivatives. Proc Natl Acad Sci USA 2016; 113:E1452E1459 [View Article][PubMed]
     [Google Scholar]
  79. Moreno Switt AI, den Bakker HC, Cummings CA, Rodriguez-Rivera LD, Govoni G et al. Identification and characterization of novel Salmonella mobile elements involved in the dissemination of genes linked to virulence and transmission. PLoS One 2012; 7:e41247 [View Article][PubMed]
     [Google Scholar]
  80. Pettengill JB, Timme RE, Barrangou R, Toro M, Allard MW et al. The evolutionary history and diagnostic utility of the CRISPR-Cas system within Salmonella enterica ssp. enterica. PeerJ 2014; 2:e340 [View Article][PubMed]
     [Google Scholar]
  81. Fricke WF, Mammel MK, McDermott PF, Tartera C, White DG et al. Comparative genomics of 28 Salmonella enterica isolates: evidence for CRISPR-mediated adaptive sublineage evolution. J Bacteriol 2011; 193:3556–3568 [View Article][PubMed]
     [Google Scholar]
  82. Malik-Kale P, Jolly CE, Lathrop S, Winfree S, Luterbach C et al. Salmonella - at home in the host cell. Front Microbiol 2011; 2:125 [View Article][PubMed]
     [Google Scholar]
  83. Chaudhuri RR, Morgan E, Peters SE, Pleasance SJ, Hudson DL et al. Comprehensive assignment of roles for Salmonella Typhimurium genes in intestinal colonization of food-producing animals. PLoS Genet 2013; 9:e1003456 [View Article][PubMed]
     [Google Scholar]
  84. Dhawi AA, Elazomi A, Jones MA, Lovell MA, Li H et al. Adaptation to the chicken intestine in Salmonella Enteritidis PT4 studied by transcriptional analysis. Vet Microbiol 2011; 153:198–204 [View Article][PubMed]
     [Google Scholar]
  85. Langridge GC, Fookes M, Connor TR, Feltwell T, Feasey N et al. Patterns of genome evolution that have accompanied host adaptation in Salmonella. Proc Natl Acad Sci USA 2015; 112:863–868 [View Article][PubMed]
     [Google Scholar]
  86. Cidre I, Pulido RP, Burgos MJG, Gálvez A, Lucas R. Copper and zinc tolerance in bacteria isolated from fresh produce. J Food Prot 2017; 80:969–975 [View Article][PubMed]
     [Google Scholar]
  87. Haahtela K, Laakso T, Korhonen TK. Associative nitrogen fixation by Klebsiella spp.: adhesion sites and inoculation effects on grass roots. Appl Environ Microbiol 1986; 52:1074–1079[PubMed]
     [Google Scholar]
  88. Korhonen TK, Tarkka E, Ranta H, Haahtela K. Type 3 fimbriae of Klebsiella sp.: molecular characterization and role in bacterial adhesion to plant roots. J Bacteriol 1983; 155:860–865[PubMed]
     [Google Scholar]
  89. Old DC. Temperature-dependent utilization of meso-inositol: a useful biotyping marker in the genealogy of Salmonella Typhimurium. J Bacteriol 1972; 112:779–783[PubMed]
     [Google Scholar]
  90. Clements RS, Darnell B. Myo-inositol content of common foods: development of a high-myo-inositol diet. Am J Clin Nutr 1980; 33:1954–1967 [View Article][PubMed]
     [Google Scholar]
  91. Amavisit P, Lightfoot D, Browning GF, Markham PF. Variation between pathogenic serovars within Salmonella pathogenicity islands. J Bacteriol 2003; 185:3624–3635 [View Article][PubMed]
     [Google Scholar]
  92. Wu H, Jones RM, Neish AS. The Salmonella effector AvrA mediates bacterial intracellular survival during infection in vivo. Cell Microbiol 2012; 14:28–39 [View Article][PubMed]
     [Google Scholar]
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Comparative genomics of Salmonella enterica serovar Montevideo reveals lineage-specific gene differences that may influence ecological niche association
M Gen 4, e000202 (2018); https://doi.org/10.1099/mgen.0.000202
/content/journal/mgen/10.1099/mgen.0.000202
/content/journal/mgen/10.1099/mgen.0.000202
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