Evolutionary trends in two strains of Salmonella enterica subsp. I serovar Enteritidis PT13a that vary in virulence potential.


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This is version 7 of a comparative whole genomic database that lists confirmed and putative polymorphisms ranging in size from single nucleotide polymorphisms (SNPs) to small deletions that differentiate two clonally related strains of Salmonella enterica serovar Enteritidis (S. Enteritidis) that nonetheless vary in phenotype. Users are advised to confirm the presence or absence of any polymorphism selected for further analysis in their strains. The database is subject to change at a moment's notice.

Updated on Jan 31, 2010 (DISCLAIMER NOTICES).


Researchers at the Egg Safety and Quality Research Unit (ESQRU) of the U. S. Department of Agriculture, Agricultural Research Service (USDA-ARS) have used microarray technology to identify a set of single nucleotide polymorphisms (SNPs) that distinguish two PT13a strains of S. Enteritidis that are genetically related but phenotypically divergent. Using the S. Enteritidis PT4 genomic sequence from the Sanger Institute as a starting point, a set of overlapping primers were generated and used in conjunction with Nimblegen Systems technology to distinguish S. Enteritidis PT13a 21027, which forms biofilm but does not contaminate eggs, from S. Enteritidis PT13a 21046, which contaminates eggs but does not form biofilm. BLAST comparisons of the polymorphisms with other Salmonella enterica annotated databases potentially matched relevant phenotypic traits to genetic loci. Version 7 contains results from confirmation of polymorphisms by primer-based sequencing of PCR-amplified DNA (PCR sequencing) in forward and reverse orientations from the two target PT13a strains and from a PT4 strain that has high similarity to the Sanger reference strain. In comparison to previous versions, all polymorphisms were confirmed by sequencing for this database. Version 7 includes results to evaluate if a single nucleotide polymorphism (SNP) occurred within an open reading frame (ORF), if it altered amino acid sequence, and what class of amino acid substitution occurred if any. Version 7 also includes dbSNP accession numbers, which are planned to be released in dbSNP Build B131 during August 2009. Version 7 defines a single SNP as any small scale polymorphism comprised of single or contiguous nucleotides that are likely to be missed by DNA-DNA microarray hybridization. Thus, SNPs in this database range in size from simple base pair substitutions to a 215 base pair deletion. SNPs are assigned location in comparison to a reference sequence according to the first nucleotide in the SNP.

Nimblegen states that combining mutational mapping with high-throughput resequencing detects within 5% of true SNP content. Mutational mapping alone previously detected 3 of 3 SNPs previously detected by ribotype analysis and PCR sequencing (rrlC, rrlA, cyaA); thus, mutational mapping was reliable for detection of SNPs. Some false positives occurred; for example, a SNP reported as present in only one of the two PT13a subpopulations in comparison to the PT4 genome was sometimes present in both PT13a strains. However, in a group of 48 regions that were recently analyzed by PCR-based sequencing, 47 were true SNPs that differentiated PT13a strains from each other. In contrast to mutational mapping, high-throughput resequencing methodology missed identifying all three control polymorphisms. The control polymorphisms and many true SNPs that differentiated PT13a strains were moved to a category referred to as "non-called ROI". For this reason, high-throughput resequencing at first looked like it had a strong tendency towards reporting false negative results. However, sequencing of polymorphisms in the non-called ROI category indicated that high-throughput sequencing produced more false positives than did mutational mapping alone. For these reasons, the decision was made to resequence all putative SNPs in F/R directions in all 3 strains that had been detected by mutational mapping. Locations of SNPs and other polymorphisms are subject to change if the genomic database for S. Enteritidis PT4 is revised by the Sanger Institute after May 22, 2006.


Salmonella enterica subsp. I serovar Enteritidis (S. Enteritidis) is the world's leading cause of salmonellosis. Eggs contaminated by apparently healthy hens can result in illness in humans who consume them. Although the incidence of this pathogen within the United States has not been as high as it has been in Europe, current estimates from the Centers for Disease Control and from the USDA-Food Safety Inspection Service respectively suggest that this pathogen has the capacity to contaminate meat as well as eggs. It is considered a persistent threat to the safety of the food supply (1). It has prevented export of breeding stock to other countries. To investigate the genetic basis for the ability of the pathogen to contaminate eggs as well as to identify other evolutionary trends associated with growth potential and colonization of the avian host, the genomes of two monomorphic strains of S. Enteritidis PT13a with variant phenotypes were subjected to virtual subtraction hybridization against dimorphic S. Enteritidis PT4 (3). Direct comparison of the closely related genomes was possible by using the genome database for S.Enteritidis PT4 NCTC 13349 to generate overlapping sets of primers (Nimblegen, Inc.) that were capable of detecting single nucleotide polymorphisms (SNPs). The database of the S. Enteritidis PT4 reference genome is from the Pathogen Sequencing Group at the Sanger Institute and can be obtained from http://www.sanger.ac.uk/Projects/Salmonella/ and at NCBI under EMBL Accession Number AM933172 and in NCBI RefSeq Accession Number NC_011294. Version 7 lists 247 confirmed polymorphisms in the chromosome, one of which changes an amino acid and introduces a deletion (248 line entries). The large virulence plasmid had 3 additional SNPs. Version 7 is the endpoint of analysis. Future updates to this website will focus on editorial content rather than de novo discovery. Users of this information are asked to contact the principle investigator if corrections are needed or if additional information becomes available that should be linked to this website.

Some strains of S. Enteritidis are monomorphic subpopulations that have the potential to complement each other in the infection pathway that results in egg contamination (2). However, other strains evolved dimorphism, which is the ability of a single strain to exhibit multiple phenotypes from one genome in response to environmental conditions. To investigate the genetic basis for the emergence of subpopulation biology that alters virulence potential, the genomes of two monomorphic strains of S. Enteritidis PT13a that could not be distinguished by DNA-DNA microarray hybridization were subjected to virtual subtraction hybridization against dimorphic S. Enteritidis PT4 (3). Direct comparison of the closely related genomes was possible by using the genome database for S. Enteritidis PT4 NCTC 13349 to generate overlapping sets of primers (Nimblegen, Inc.) that were capable of detecting single nucleotide polymorphisms (SNPs). The database of the S. Enteritidis PT4 reference genome is from the Pathogen Sequencing Group at the Sanger Institute and can be obtained from http://www.sanger.ac.uk/Projects/Salmonella/. Version 7 shows polymorphisms as they are located in the virulence plasmids and chromosomes of PT13a strains 21027 and 21046 in reference to the location in the reference PT4 strain. Recent analysis of these genomes by pulsed-field-gel-electrophoresis (PFGE) indicates that PT13a 21046, previously designated wild-type (wt), is less prevalent than the PFGE pattern associated with PT13a 21027. For this reason, the terms "wild-type" and "biofilm-forming" are no longer used when describing strains within tables; instead, each strain is referred to by its respective accession number 21046 and 21027. Of the 136 confirmed chromosomal polymorphisms in PT13a 21027, 67 (48.9%) altered amino acid sequence and 4 were terminations (Table S1). One SNP in SEN1464 (ydcZ) changed an amino acid and introduced a deletion, which accounts for two line entries and results in a total of 137 line entries for PT13a 21027. Genes cysN, SEN1576, putP and ydjN had early terminations introduced. There were 8 deletions involving the 9 genes foxA, kdgM, dsdA, pgk, lrfB, sefD, ydcZ and yjfK and yjfL. The single deletion affecting both yjfK and yjfL produced a fused ORF. PT13a 21027 had 22 intergenic SNPs, 4 RNA gene SNPs, and 43 synonymous SNPs. For PT13a 21046, 48 of 111 polymorphisms (43.2%) altered ORFs and two of these were terminations. A premature termination codon was observed in fhuA; in addition, SEN4256 also had a termination codon that differentiated strains; however, this SNP is most likely of low consequence since it occurred in a pseudogene. SEN4316 (a diguanylate cyclase) and SEN3898 (a mocR subfamily gene) had the two largest deletions encountered in the project, which were 215 and 92bp, respectively. PT13a 21046 had 16 intergenic SNPs, 8 RNA gene SNPs and 39 synonymous SNPs. The virulence plasmid had 3 SNPs that differentiated PT13a plasmids, but none of these altered ORFs. These data have been used to construct a theory for the evolution of egg contamination by Salmonella Enteritidis, which was first presented as a Proceedings paper at the 110th U. S. Animal Health Salmonella Committee Meeting (Oct. 16, 2006) and as an oral presentation at the 49th AAVLD Bacteriology Session (Oct. 15, 2006). Briefly, the theory states that: 1. Two strains of different phage types evolved in separate hosts, possibly the chicken and the house mouse Mus musculus. 2. The two strains sometimes crossed host boundaries and shared environments. 3. The strains underwent homologous recombination. 4. A new strain emerged that had growth advantages and the new ability to contaminate eggs. It had both of the bacteriophages that were associated with the initial strains. 5. The new strain was inherently unstable due to phage incompatibility and quickly split into two lineages that shared a similar genome but that differed in phage type. 6. The two phage lineages, now known to be defined by phages ST64b and Fels2, evolved further and generated stable subpopulations that varied in phenotype, virulence attributes and growth properties. Some strains had dimorphism, which is the ability to express multiple phenotypes from a single genome in response to environmental conditions. Others evolved into monomorphic strains, which could synergistically contribute to infection resulting in egg contamination. 7. The evolution of pandemic S. Enteritidis that impacts egg contamination thus resulted from a series of genetic drift and genetic shift events, but is today observable by analysis of patterns of genetic drift. The chromosomes of pandemic strains of S. Enteritidis have remained highly similar in spite of having split into two phage lineages.


Related Publications:

  1. Altekruse, et al, 2006. Salmonella Enteritidis in broiler chickens, United States, 2000-2005. Emerging Infec. Dis. 12:1848-52.
  2. Morales, et al. 2005. Correlation of phenotype with the genotype of egg-contaminating Salmonella enterica serovar Enteritidis. Appl. Environ. Microbiol. 71: 4388-99.
  3. Morales, et al, 2007. Pathotyping of Salmonella enterica by analysis of single-nucleotide polymorphisms in cyaA and flanking 23S ribosomal sequences. Environ. Microbiol. 2007 Apr;9(4):1047-59.
  4. Guard, J. 2006. Comparative Genome Sequencing of Salmonella Enteritidis Isolates that Vary in Virulence Characteristics. Proceedings of the 110th U.S. Animal Health Association, p. 97-101.
  5. Gantois, et al. 2008. Salmonella Enteritidis genes induced during oviduct colonization and egg contamination in laying hens. Applied. Environ. Microbiol. Sep 5.
  6. Porwollik, et al, 2005. Differences in gene content between Salmonella enterica serovar Enteritidis isolates and comparison to closely related serovars Gallinarum and Dublin. J. Bacteriol. 187 (18):6545-6555.
  7. Thomson, et al 2008. Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res. Oct. 1 2008 18:1624-1637.
  8. Pan et al, 2009. Identification of genetic and phenotypic differences associated with prevalent and non-prevalent Salmonella Enteritidis phage types: analysis of variation in amino acid transport. Microbiology Jul 2. Epub ahead of print

Table S1. Single nucleotide polymorphisms (SNPs) of Salmonella enterica subsp. I Serovar Enteritidis PT13a That Differentiate Pathotypesa

SNP locationb,c PT4 P125109 dbSNP IDd PT4 P125109 protein Salmonella enteritidis annotation Salmonella typhimurium annotation gene name mutated PT13a 21046 straine nucleotide substitutiona(PT4 P125109/PT13a 21046) amino acid substitutiona(PT4 P125109/PT13a 21046) class of amino acid substitutiona(PT4 P125109/PT13a 21046) KEGG pathway other information
Large Virulence Plasmid SNPs
Chromosomal SNPs
74552153929104CAR31655.1SEN0065STM0064dapB21027G/AAA asp to asn 263ap to np00300reduces 2,3-dihydrodipicolinate to 2,3,4,5-tetrahydrodipicolinate in lysine and diaminopimelate biosynthesis
82917153929758CAR31661.1SEN0072STM0071caiC21046C/TAA val to ile 258nn to nn-AMP-binding enzyme;L-carnitine production
129592141096998CAR31701.1SEN0112STM0111leuC21046C/Tsynonymousna00290valine, leucine and isoleucine biosynthesis
196607153929107CAR31758.1SEN0170STM0165speD21027T/CAA thr to ala 55np to nn00271, 00220spermidine biosynthesis from putrescine
204450153929760CAR31765.1SEN0177STM0172yadG21046G/AAA gly to ser 166nn to np02010ABC-type multidrug transport system
226922153929762CAR31784.1SEN0196SeAg_B0227fhuA21046C/TAA TER at gln 470np to TER-ferrichrome-iron receptor, colicin M, and phages; pseudogene
237853153929109CAR31793.1SEN0205STM0200stfG21027A/CAA thr to pro 98np to nn02010High-affiinity transport of Fe (3+) ferrichrome
241034141100738CAR31796.1 SEN0208STM0203yadQ21027G/Asynonymousna-chloride channel protein important for extreme acid resistance
255011141100740CAR31807.1SEN0219STM0213dapD21027A/Gsynonymousna003002,3,4,5-tetrahydropyridine-2-carboxylate N-succinyltransferase
267017141096999CAR31818.1SEN0230STM0223yaeL21046G/Asynonymousna-zinc metallopeptidase
304365153929764CAR31848.1SEN0261STM0259yafE21046G/AAA ala to thr 101nn to np00620menaquinone/biotin biosynthesis
393529153929111CAR31933.1SEN0347STM0364foxA21027Del G/-DEL 1 bpDel-ferrioxamine receptor
399525141100744CAR31939.1SEN0353STM0370prpD21027C/Tsynonymousna00790, 005002-methylcitrate dehydratase; propionate catabolism
401171153929113CAR31940.1SEN0354STM0371prpE21027C/GAA arg to gly 60bp+ to nn00640forms propionyl-CoA from propionate
466363153929766CAR32002.1SEN0416STM0434apbA21046C/TAA ser to asn 237np to np00770Pantothenate and CoA biosynthesis
505777153929768CAR32036.1SEN0450STM0469rpmE221046C/AAA ser to arg 18np to bp+0301050S ribosomal protein L31 type B
513535153929115CAR32044.1SEN0458STM0477acrR21027A/GAA ser to gly 137np to nn-regulates acrAB operon; TetR/AcrR family (dephalothin and cephaloridine)
533246153929117CAR32061.1SEN0475STM0494ushA21027T/GAA asp to glu 41ap to ap00760, 00230, 00240nicotinate/nicoinamide/purine/pyrimidine metabolism;
562921153929770CAR32088.1SEN0503STM0522allP21046C/TAA ala to val 268nn to nn-Cytosine/uracil/thiamine/allantoin permeases
565589153929119CAR32090.1SEN0505STM0524ybbY21027T/C AA pro to leu 238nn to nn-purine permease
633202141097001CAR32157.1SEN0569STM0600cstA21046C/Tsynonymousna-carbon starvation protein
643964153929772CAR32166.1SEN0578STM0609ahpF21046C/AAA asp to glu 281ap to ap-protects DNA from alkyl hydroperoxides
661305141100746CAR32182.1SEN0594STM0625dpiB21027G/Tsynonymousna02020sensory histidine kinase; regulation of cit operon and plasmid inheritance genes
684875141097004CAR32207.1SEN0619STM0650uxaA21046C/Asynonymousna00040pentose and glucuronate interconversions
696522153929774naSEN0629STM0660pseudo21046G/AAA arg to cys 288bp to np-pseudogene in SEN after AA 171
789332141097005 CAR31646.1 SEN0712STM0767dcoA-221046C/Tsynonymousna-pseudogene in STM; biotin requiring enzyme; forms oxaloacetate from pyruvate and CO2; repeated at 63302-66643 and complement 3400450 to 3403870
789335141097007 CAR31646.1 SEN0712STM0767dcoA-221046T/Gsynonymousna-pseudogene in STM; biotin requiring enzyme; forms oxaloacetate from pyruvate and CO2; repeated at 63302-66643 and complement 3400450 to 3403871
789347141097010 CAR31646.1 SEN0712STM0767dcoA-221046T/Csynonymousna-pseudogene in STM; biotin requiring enzyme; forms oxaloacetate from pyruvate and CO2; repeated at 63302-66643 and complement 3400450 to 3403872
789359141097012 CAR31646.1 SEN0712STM0767dcoA-221046C/Tsynonymousna-pseudogene in STM; biotin requiring enzyme; forms oxaloacetate from pyruvate and CO2; repeated at 63302-66643 and complement 3400450 to 3403873
789362141097014 CAR31646.1 SEN0712STM0767dcoA-221046T/Csynonymousna-pseudogene in STM; biotin requiring enzyme; forms oxaloacetate from pyruvate and CO2; repeated at 63302-66643 and complement 3400450 to 3403874
789389141100748 CAR31646.1 SEN0712STM0767dcoA-221027T/Csynonymousna-pseudogene in STM; biotin requiring enzyme; forms oxaloacetate from pyruvate and CO2; repeated at 63302-66643 and complement 3400450 to 3403874
789488141100750 CAR31646.1 SEN0712STM0767dcoA-221027G/Csynonymousna-pseudogene in STM; biotin requiring enzyme; forms oxaloacetate from pyruvate and CO2; repeated at 63302-66643 and complement 3400450 to 3403875
789503141100752 CAR31646.1 SEN0712STM0767dcoA-221027C/Gsynonymousna-pseudogene in STM; biotin requiring enzyme; forms oxaloacetate from pyruvate and CO2; repeated at 63302-66643 and complement 3400450 to 3403876
789512141101249 CAR31646.1 SEN0712STM0767dcoA-221027A/Gsynonymousna-pseudogene in STM; biotin requiring enzyme; forms oxaloacetate from pyruvate and CO2; repeated at 63302-66643 and complement 3400450 to 3403877
799987153929121CAR32307.1SEN0721STM0776galE21027T/AAA lys to asn 253bp to np00052, 00520UDP-glucose 4-epimerase; galactose and nucleotide sugars metabolism
818905153929776CAR32324.1SEN0738STM0793bioA21046C/TAA asp to asn 110ap to np00780biotin metabolism
831768153929123CAR32336.1SEN0751STM0805moaD21027C/AAA phe to leu 9nn to nn-biosynthesis of the molybdenum cofactor
833026153929778 CAR32338.1 SEN0753STM0807ybhL21046T/CAA phe to leu 178nn to nn-poorly characterized
883330153929780CAR32381.1SEN0798STM0852yliG21046C/AAA arg to leu 139bp+ to nn-2-methylthioadenine synthetase: RNA binding; catalytic activity; iron-sulfur cluster binding
900607141097015CAR32397.1SEN0814STM0868deoR21046G/Asynonymousna-putative transport protein/regulator
909178141101251 CAR32407.1 SEN0824STM0878potG21027G/Tsynonymousnaputrescine transport ATP-binding protein
937016141101253CAR32433.1SEN0850STM0942yjbZ21027C/Tsynonymousna-macrolide export
1019733153929125CAR32501.1SEN0917STM1053none21027T/GAA glu to ala 109ap to nn-poorly characterized
1035179153929127CAR32513.1SEN0930STM1065ymbA21027C/TAA ala to val 169nn to nn-poorly characterized
1095448153929129CAR32573.1SEN0989STM1128putP21027G/TAA TER at cys 120np to TER-Na+/proline symporter
1099079153929131CAR32576.1SEN0992STM1131kdgM21027Del A/-DEL 1 bpDel-oligogalacturonate-specific porin protein; pectin secretion?
1163256153929133CAR32650.1SEN1067STM1938yecA21027T/GAA trp to gly 182nn to nn-metal-binding protein
1164068141097017CAR32651.1SEN1068STM1937tyrP21046G/Asynonymousna-Tryptophan/tyrosine permase family
1175680141101255CAR32664.1SEN1081STM1922motB21027G/Asynonymousna02030, 02040couples rotation with proton/sodium motive force
1189967141097020CAR32676.1SEN1093STM1910ftsI21046C/Tsynonymousna-penicillin-binding protein
1216457153929135CAR32701.1SEN1118STM1885edd21027A/GAA lys to arg 503bp to bp+00030Pentose phosphate pathway
1248118153929137CAR32743.1SEN1162STM1869none21027T/AAA val to asp 52nn to ap-phage-tail assembly-like protein
1249431153929782CAR32745.1SEN1164STM1868.1Nnone21046A/GAA asp to gly 68ap to nn-TER codon of STM is changed; alternative ORF is longer in SE
1276695141101257CAR32775.1SEN1194STM1843none21027G/Tsynonymousna-multidrug efflux system protein domain PRK10504
1279901153929139CAR32780.1SEN1199STM1838yobF21027A/GAA lys to arg 12bp to bp+-cytoplasmic
1281189141101259CAR32782.1SEN1201STM1836ftsI21027C/Tsynonymousna-penicillin-binding protein; peptidoglycan synthetase
1284118153929784CAR32785.1SEN1204STM1833none21046C/TAA arg to gln 129bp+ to np-membrane
1287804153929141CAR32789.1SEN1209STM1828yoaE21027G/AAA val to ile 29nn to nn-terC, tellurium resistance
1289642153929786CAR32790.1SEN1210STM1827none21046C/TAA gly to ser 421nn to np-diguanylate cyclase/ phosphodiesterase
1317293141101261CAR32818.1SEN1238STM1799emtA21027C/Asynonymousna-lysM/invasin domains; lytic transglycosylase; Goose Egg White Lysozyme (GEWL) domain.
1319180153929143CAR32821.1SEN1241STM1796treA21027T/CAA thr to ala 512np to nn00500hydrolysis of trehalose to glucose
1328395141097021CAR32829.1SEN1250STM1787none21046C/Tsynonymousna-Ni,Fe-hydrogenase I large subunit; fermentative growth
1416687141101263AAL20623.1 SEN1327-1328STM1705osmB21027G/Asynonymousna-osmotically inducible lipoprotein; may aid stationary-phase survival
1445558153929145CAR32932.1SEN1355STM1678none21027C/TAA asp to asn 49ap to np-2'-hydroxyisoflavone reductase
1474943141101265CAR32965.1SEN1386nanone21027T/Csynonymousna-degenerate lysogenic bacteriophage in Enteritidis, E. coli and Typhi CT18;
1503343141097024CAR32996.1SEN1418STM1635none21046C/Tsynonymousna02010ABC-type polar amino acid transport system
1533003153929147CAR33025.1SEN1446STM1610ydcK21027A/GAA val to ala 250nn to nn-UDP-3-O-[3-hydroxymyristoyl]: LPS
1554930153929149CAR33043.1SEN1464STM1591ydcZ21027Del1554930-935AA leu to phe 10 (DEL event) nn to nn -unknown function
1554930153929149CAR33043.1SEN1464STM1591ydcZ21027Del1554930-935DEL 6bpDel11&12-unknown function
1579797153929788CAR33063.1SEN1484STM1571yddG21046C/TAA cys to tyr 78np to nn-unknown function
1610591141097025CAR33088.1SEN1509STM1543none21046C/Asynonymousna-sugar metabolism/transportprotein
1638463153929790CAR33118.1SEN1539STM1512dcp21046T/CAA asp to gly 386ap to nn-dipeptidyl carboxypeptidase II; amino acid transport
1656696153929151CAR33135.1SEN1555bfynfI21027T/GAA asp to glu 93ap to ap-TorD; cytoplasmic chaperone TorD
1659052153929792CAR33138.1SEN1558STM1491none21046T/GAA leu to arg 22nn to bp+02010proline/glycine betaine transport system
1681327153929153CAR33157.1SEN1576STM1472ytcJ-like21027G/AAA TER at trp 409nn to TER-metal-dependent hydrolase with the TIM-barrel fold
1697323153929155CAR33172.1SEN1590STM1457rnfC21027G/A AA glu to asp 591ap to ap-NADH ubiquinone dehydrogenase; RnfC; electron transport to nitrogen
1715322153929157CAR33193.1SEN1611STM1436nemA21027C/TAA pro to ser 38nn to np-Old yellow enzyme (OYE)-like FMN; N-ethylmaleimide reductase;
1723077153929794CAR33201.1SEN1619STM1428ydhC21046G/AAA gly to ser 241nn to np-Major facilitator superfamily
1738692141097027CAR33218.1SEN1636STM1409ssaJ21046C/Tsynonymousna03070Type III secretion, lipoprotein EscJ
1764145153929159CAR33245.1SEN1663STM1382orf 40821027C/AAA his to asn 327bp- to np-ribokinase; DeoR family
1775109141097030CAR33257.1SEN1675STM1370sufB21046G/Asynonymousna-activates cysteine desulfurase SufS with SufCD
1785781141101267CAR33265.1SEN1683STM1361ydiM21027C/Asynonymousna-Major facilitator superfamily
1800374141097032CAR33277.1SEN1695STM1349pps21046T/Csynonymousna00620, 00720forms phosphoenolpyruvate from pyruvate
1801472141101269CAR33277.1SEN1695STM1349pps21027A/Gsynonymousna00620, 00720forms phosphoenolpyruvate from pyruvate
1806066141097033CAR33282.1SEN1700STM1344ydiV21046G/Tsynonymousna-putative diguanylate cyclase/phosphodiesterase
1828544153929161CAR33304.1SEN1723STM1320ydjN21027G/AAA TER at trp 225np- to TER-Predicted Na+/dicarboxylate symporter
1843306153929796CAR33318.1SEN1737STM1306astB21046G/AAA arg to cys 39bp to np-00330Succinylarginine dihydrolase
1860952153929798CAR33334.1SEN1753SeD_A2056ydjG21046G/TAA arg to ser 245bp to np-Hypothetical oxidoreductase
1901744141101271CAR33379.1SEN1799STM1252none21027G/Asynonymousna-predicted neuraminidase (sialidase)
1934221141097035CAR33411.1SEN1831STM1218lolD21046G/Asynonymousna-ABC-type antimicrobial peptide transport; lipoprotein transport
1987706153929800CAR33463.1SEN1883STM1165grxB21046A/GAA ile to val 5nn to nn-Glutaredoxin 2 [Posttranslational modification, protein turnover, chaperones]
2008553141097037CAR33486.1SEN1906STM1142csgD21046T/Csynonymousna-DNA-binding transcriptional regulator; activates csg operons involved in biofilm formation
2062613141101273CAR33553.1 SEN1970SeD_A2305none21027G/Asynonymousna-DNA breaking rejoining enzyme superfamily. Phage integrase domain.
2084629153929802CAR33577.1SEN1995SeD_A2331none21046T/CAA arg to gly 149bp to nn--
2131226153929163CAR33630.1SEN2050STM2052pduQ21027A/CAA asp to ala 64ap to nn00053, 00120, 00650, 00051, 00052, 00260, 00310, 00520, 00625propanol dehydrogenase
2142697141101275CAR33643.1SEN2063STM2065phsA21027T/Csynonymousna-thiosulfate reductase precursor
2144992141101277CAR33644.1SEN2065STM2066sopA21027A/Gsynonymousna-secreted effector protein
2158117141101279CAR33654.1SEN2075STM2076hisA21027C/Tsynonymousna00340amino acid transport and metabolism
2172706153929165CAR33666.1SEN2085BSeD_A2427rfbX21027T/CAA arg to gly 300bp+ to nn-O-antigen transporter: in SG & STY, not in STM
2182397153929167CAR33676.1SEN2093STM2097rfbB21027A/TAA cys to ser 274np to np00520, 00523, 00521dTDP-glucose 4,6-dehydratase
2182436153929804CAR33676.1SEN2093STM2097rfbB21046G/TAA his to asn 261bp- to np00520, 00523, 00521dTDP-glucose 4,6-dehydratase
2200415141101281CAR33691.1bfSTM2112wcaD21027G/Asynonymousna-putative colanic acid polymerase
2203153141097039CAR33694.1SEN2111STM2115wcaA21046G/Asynonymousna-colanic acid:glycosyl transferase
2231955153929169CAR33712.1SEN2129STM2134none21027G/AAA gly to glu 207nn to ap-inner membrane
2256571141101283CAR33735.1SEN2150STM2156Anone21027T/Csynonymousna-putative protein of unknown function; possible lipoprotein
2293090153929171CAR33770.1SEN2185STM2192yeiB21027G/AAA pro to ser 290nn to np-inner membrane
2307838153929806CAR33782.1SEN2197STM2204fruA21046C/TAA ala to thr 321nn to np00051, 02060fructose-specific metabolism/transportprotein
2468813141101285CAR33928.1SEN2344STM2362purF21027G/Asynonymousna00251, 00230nucleotide:amidophosphoribosyltransferase
2526004153929808CAR33982.1SEN2396STM2410yfeA21046A/GAA his to tyr 600bp- to nn-diguanylate cyclase/phosphodiesterase
2557022141097041CAR34012.1SEN2427STM2446none21046G/Tsynonymousna-iron-dependent peroxidase
2566232141101287CAR34023.1SEN2438STM2458eutB21027G/Tsynonymousna00564adenosylcobalamin:ethanolamine ammonia-lyase
2573093153929173CAR34029.1SEN2444STM2464eutN21027G/AAA his to tyr 71bp- to nn-ethanolamine utilization
2642024141097044naSEN2494STM2514ratB21046G/Asynonymousna-pseudogene; unknown function; putative OMP; many repeats (DUF824)
2664521141097045CAR34093.1SEN2510STM2530none21046G/Asynonymousna-anaerobic DMSO reductase
2677674153929810CAR34099.1SEN2516STM2536pepB21046G/AAA pro to ser 187nn to np-Cytosol aminopeptidase family
2686717153929812CAR34110.1SEN2527STM2547none21046C/TAA thr to met 191np to nn-lipid:hydrolase
2690699153929814CAR34114.1SEN2531STM2551nicO21046C/AAA phe to leu 128nn to nn-High-affinity nickel protein (see STM2552)
2736265141101289CAR34152.1SEN2570STM2644srmB21027C/Tsynonymousna-transcription: LysR
2751287142460370naSEN_r005STM2657rrlG 21027AA/GGrrnna0301023S rrn subunit
2751875142460371naSEN_r005STM2657rrlG 21027T/C rrnna0301023S rrn subunit
2786647153929175CAR34191.1SEN2609STM2689bapA21027G/TAA trp to cys 2319nn to np-proline/threonine-rich protein
2788796153929177CAR34191.1SEN2609STM2689bapA21027A/CAA ile to leu 3036nn to nn-proline/threonine-rich protein
2829865141097047CAR34218.1SEN2638STM2794ygaE21046G/Asynonymousna-regulator of gab gene expression; DNA-binding trnascriptional regulator CsiR; GntR family
2851388153929816CAR34242.1SEN2662STM2817luxS21046C/T AA ala to thr 109nn to np00271produces autoinducer; AI II quorum sensing
2869327153929179CAR34259.1SEN2680STM2839ygaA21027C/TAA gly to arg 72nn to bp+-Required for the expression of anaerobic nitric oxide (NO) reductase; acts as a transcriptional activator for the norVW operon
2908407153929181CAR34299.1SEN2721STM2879sicP21027G/AAA ser to leu 112np to nn-chaperone related to virulence
2939833153929183CAR34330.1SEN2751STM2912pgk21027Del2939833-844DEL 12bpDel167-170-lysR; transcriptional regulator
2957802153929185CAR34352.1SEN2773STM2934cysN21027C/AAA TER at glu 447ap to TER00230, 00450, 00920sulfate adenylyltransferase subunit 1
3014949141097049CAR34397.1SEN2819STM2974fucA21046C/Tsynonymousna00051Ribulose-5-phosphate 4-epimerase and related epimerases and aldolases
3032200153929187CAR34413.1SEN2834STM2992argA21027C/GAA leu to val 225nn to nn00220N-acetylglutamate synthase
3046877141101291CAR34422.1SEN2843STM3001thyA21027G/Asynonymousna00670, 00240catalyzes formation of dTMP and 7,8-dihydrofolate from 5,10-methylenetetrahydrofolate and dUMP
3073028141097051CAR34445.1SEN2867STM3024rcnA21046C/Gsynonymousna-nickel/cobalt efflux protein RcnA ; membrane protein conferring nickel and cobalt resistance
3081698153929818CAR34452.1SEN2874STM3030none21046C/TAA met to ile 6nn to nn-putative periplasmic protein
3081785153929189CAR34453.1SEN2875STM3031none21027G/AAA leu to phe 12nn to nn-Ail/OmpX-like protein; possible surface antigen
3135538141097054CAR34505.1SEN2928STM3084.sfadR21046G/Asynonymousna-similar to Escherichia coli regulator for uxu operon (AAC77280.1); GntR family
3148475153929820CAR34519.1SEN2942STM3099yggR21046C/TAA ala to thr 138nn to np03090twitching motility protein; pilu retraction
3153640153929822CAR34526.1SEN2949STM3106ansB21046G/AAA gly to asp 237nn to ap00252, 00460, 00910catalyzes the formation of aspartate from asparagine CRP regulated and induced by anaerobiosis
3153778153929824CAR34526.1SEN2949STM3106ansB21046C/TAA ala to val 283nn to nn00252, 00460, 00910catalyzes the formation of aspartate from asparagine CRP regulated and induced by anaerobiosis
3195186153929191CAR34562.1SEN2986STM3143hybG21027C/AAA arg to leu 74bp+ to nn-hydrogenase 2 accessory protein HypG; may effect maturation of large subunit of hydrogenase-2
3206865153929193CAR34576.1SEN3000STM3157yghA21027C/AAA ser to arg 110np to bp+-oxidoreductase
3218705153929195CAR34587.1SEN3011STM3168ygiR21027A/CAA leu to arg 121nn to bp+-Fe-S oxidoreductase family 2
3225510141097055CAR34593.1SEN3017STM3174par C21046G/Asynonymousna-decatenates newly replicated chromosomal DNA and relaxes positive and negative DNA supercoiling
3296285153929826CAR34526.1SEN3082STM3241tdcE21046T/CAA asp to gly 135np to nn00650, 00640, 00620Pyruvate formate lyasea:anaerobic glycolysis
3363009141097057CAR34724.1SEN3148STM3315yrbH21046G/Asynonymousna-D-arabinose 5-phosphate isomerase:polysialic acid capsule expression protein
3377504141101293CAR34739.1SEN3163STM3330gltB21027G/Asynonymousna-catalyzes the formation of glutamate from glutamine and alpha-ketoglutarate
3407874153929828CAR34767.1SEN3191STM3358none21046C/GAA val to leu 140nn to nn-gntR transcriptional regulator
3432239141097060CAR34788.1SEN3213STM3379accB21046G/Asynonymousna-acetylCoA carboxylase, BCCP subunit:biotin
3441850153929197CAR34798.1SEN3223STM3389envR21027A/GAA val to ala 194nn to nn-regulator for envCD; acrEF; TetR/AcrR family
3446987153929830CAR34800.1SEN3225STM3391acrF21046G/AAA arg to his 992bp+ to bp--multidrug transport;acriflavin resistance
3455766153929832CAR34805.1SEN3230STM3402yrdC21046C/GAA gly to ala 171nn to nn-RimN; YrdC; required for maturation of 16s RNA; binds preferentially double stranded RNA
3507751153929834CAR34877.1SEN3302STM3475nirD21046G/AAA val to ile 28nn to nn-nitrite reductase
3572250153929199CAR34928.1SEN3353STM3528pseudo21027C/TAA gly to glu 241nn to np-pseudogene in reference; ABC-type phosphate transport system
3576418141101295CAR34931.1SEN3355STM3531none21027G/Asynonymousna-dihydroxyacid dehydratase
3584158153929201CAR34936.1SEN3360STM3536glgC21027C/AAA glu to asp 174ap to np-ADP-glucose pyrophosphorylase
3586071141097062CAR34937.1SEN3361STM3537glgX21046C/Asynonymousna-glycogen debranching enzyme
3594297141101297CAR34943.1 SEN3367STM3544yhhW21027G/Asynonymousna-Cupin domain
3613736153929836CAR34963.1SEN3387STM3564livK21046C/AAA ala to ser 207nn to np-branched chain amino acid binding
3658575153929203CAR35003.1SEN3427STM3604none21027C/TAA gly to glu 369nn to np-inner membrane
3673351153929205CAR35014.1SEN3438STM3615yhjK21027G/AAA arg to cys 398bp+ to np-putative phosphodiesterase; may inhibit biofilm formation; may facilitate invasion of epithelial cells; see HmsP of Yersinia pestis
3683137141101299CAR35018.1SEN3442STM3619bcsA21027C/Asynonymousna-polymerizes uridine 5'-diphosphate glucose to cellulose; acts with BcsB, BcsZ and BcsC in cellulose biosynthesis
3734249153929838CAR35066.1SEN3487STM3665avtA21046G/AAA ser to asn 60np to np-valine--pyruvate transaminase
3744227153929207CAR35076.1SEN3497STM3675sgbH21027G/TAA gly to trp 145nn to nn-3-hexulose-6-phosphate isomerase
3744397141101301CAR35076.1SEN3497STM3675sgbH21027G/Tsynonymousna-3-hexulose-6-phosphate isomerase
3788343153929840CAR35112.1SEN3533STM3711rfaF21046C/GAA thr to arg 331np to bp+01031, 00540LPS heptosyltransferase II
3792668153929209CAR35116.1SEN3537STM3715rfaZ21027G/TAA ala to glu 17nn to ap-LPS core biosynthetic protein
3793026141097063CAR35117.1SEN3538STM3716rfaY21046T/Csynonymousna01031, 00540LPS: modification of heptose region of core
3795869141101303CAR35120.1SEN3541STM3719rfaB21027C/Asynonymousna01031, 00540LPS: 1,6-D-galactosyltransferase
3867458153929211CAR35184.1SEN3608STM3792none21027G/AAA arg to cys 254bp+ to np-putative L-fucose permease
3880104153929213CAR35195.1SEN3619STM3802dsdA21027Del3880104-0113DEL 10bp Del00260D-serine deaminase; dehydratase
3970231142459123naSEN3703-r011STM3888-3889yieP-rrsC21027T/A intergenicna--
3972440142460372naSEN_r012STM3891rrlC21027A/G rrnna0301023S rrn subunit
3973593159695620naSEN_r012STM3891rrlC21046C/Trrnna0301023S rrn subunit
3973601159695621naSEN_r012STM3892rrlC21046GCCT/TGTCrrnna0301023S rrn subunit; bp 3973601appears to discriminate between Sanger ref PT4 (g) and CA template PT4 (c); does not alter restriction site used in PFGE
3973611159695622naSEN_r012STM3891rrlC21046GT/CArrnna0301023S rrn subunit; alters PFGE restriction site
4018775141097067CAR35315.1SEN3740STM3939cyaA21046C/Tsynonymousna00230adenylate cyclase
4018861153929215CAR35315.1SEN3740STM3939cyaA21027A/G AA asn to ser 702np to np00230adenylate cyclase
4027489141101307CAR35325.1SEN3749STM3952corA21027C/Tsynonymousna-magnesium/nickel/cobalt transporter
4068166159695624naSEN_r015STM3991rrlA21046C/Trrnna0301023S rrn subunit; sequence is reverse complement to what is in cyaA manuscript
4068174159695625naSEN_r015STM3991rrlA21046GCCT/TGTCrrnna0301023S rrn subunit; sequence is reverse complement to what is in cyaA manuscript
4068184159695626naSEN_r015STM3991rrlA21046GT/CArrnna0301023S rrn subunit; sequence is reverse complement to what is in cyaA manuscript
4133134141101309naSEN3843STM4052pseudo21027T/Gsynonymousna-pseudogene in Enteritidis; missing 5' 28 aa of Typhimurium gene.
4146218153929842CAR35430.1SEN3857STM4067none21046A/GAA thr to ala 42np to nn-putative ADP-ribosylglycohydrolase
4152430141101311CAR35437.1SEN3864STM4074ego21027A/Gsynonymousna02010ABC-type sugar transport system
4189388153929844CAR35472.1SEN3898SeD_A4510mocR subfamily21046Del4189388-9479DEL 92bpDel-transcription: gntR: flanked by an 11bp repeat GCGGCAAAATG
4223137142459104naSEN3925-3926STM4131-4132murI-SEN_r01721046G/A intergenicna--
4269421142460373nabfSTM4179rrlE21027TT/CCrrnna0301023S rrn subunit
4274880153929846CAR35534.1SEN3965STM4183aceB21046G/CAA val to leu 345nn to nn00630, 00620malate synthase A
4296365141097070CAR35553.1SEN3986STM4220lysC21046T/Csynonymousna00260, 00300lysine sensitive aspartokinase III
4331502141097072CAR35587.1SEN4023STM4254uvrA21046C/Tsynonymousna-DNA excision repair enzyme
4351538141101313CAR35593.1SEN4030STM4261siiE21027T/Csynonymousna-Fusion protein; sulfite oxidase (SO); molybdopterin binding
4365146141097074CAR35601.1SEN4039STM4269yjcE21046C/Tsynonymousna-Sodium/hydrogen exchanger:pH maintenance
4368126153929217CAR35604.1SEN4042STM4272lrgB21027Del4368126-8137DEL 12bp (in-frame)Del-LrgB-like:murein:penicillin:seritonin
4402066153929219CAR35632.1SEN4071STM4299melB21027G/AAA gly to asp 331nn to ap-GPH family melibiose permease II
4418467141101315CAR35646.1SEN4086STM4315hilD21027C/Tsynonymousna-arabinose operon control protein:DNA binding
4418965153929221CAR35647.1SEN4087STM4316none21027C/AAA val to phe 34nn to nn-cytoplasmic protein
4420944141101317CAR35650.1SEN4090STM4319phoN21027A/G synonymousna00740, 02020, 00361non-specific acid phosphatase
4472579153929223CAR35699.1 CAR35700.1SEN4139 & SEN4140STM4373 and STM4374yjfK and yjfL21027Del4472579-2589DEL 11bp (fusion)Del-TER codon and sequence 3' of yjfK removed; ORF reads through to end of yjfL
4517227153929225CAR35746.1SEN4187STM4438pmbA21027C/TAA thr to met 103np to nn-protease involved in proteolytic processing of the antibiotic Microcin B17 and in sensitivity to the DNA gyrase inhibitor LetD
4532612153929848CAR35763.1SEN4204ASeD_A4835treB21046A/GAA leu to pro 235nn to nn-trehalose-specific IIBC part of PTS (pseudogene in Typhimurium, read through in Enteritidis)
4558130153929227CAR35786.1SEN4232STM4479yjgP21027T/CAA phe to leu 227nn to nn-permease
4565438153929229CAR35793.1SEN4239STM4486yjgB21027C/TAA gly to ser 154nn to np-alcohol dehydrogenase
4574262153929231CAR35805.1SEN4250SeD_A4882*sefD21027Del A/-DEL 1bpDel-*S. Enteritidis fimbrial protein (pseudogene in most Salmonella serotypes, with the exception of Dublin, but it is not a named protein in Dublin; sefD of Dublin contains SeC_A4882)
4579004141097075naSEN4256SeD_A4893pseudo21046C/TAA TER at gln 25np to TER-Dublin transposase family gene ORF included within SEN4256, but this ORF is a pseudogene already in SE.
4592540153929233CAR35824.1SEN4271STM4510none21027C/TAA thr to ile 215np to nn-aspartate racemase
4622524153929235CAR35850.1SEN4298STM4533tsr21027A/GAA met to val 82nn to nn02030, 02020serine sensor receptor
4642252153929850CAR35868.1SEN4316STM4551none21046Del4642252-2466DEL 215 bp (5' 135 bp & 1st 80 bp)Del-turnover of cyclic diguanosine monophosphate
4666711153929237CAR35890.1SEN4337STM4581yjjK21027T/CAA asn to ser 99np to ap-ABC transporter; see chvD (Agrobacterium tumefaciens)

a Shading indicates SNPs that differentiate PT13a 21027, which is positive for biofilm formation but negative for egg contamination (BF-EC+), from the reference PT4 genome (BF+EC+) and PT13a 21046 (BF-EC+). Conversely, SNPs that differentiate PT13a from the reference strain PT4 strain and PT13a 21027 are unshaded.

bThe genomic database for the reference strain Salmonella enterica subsp. enterica serovar str. P125109 is available at http://www.sanger.ac.uk/Projects/Salmonella/ and has been submitted under EMBL Accession Number AM933172 and is present in NCBI RefSeq Accession Number NC_011294.

cDates of analysis span Jan 2006 - July 2009. Location of SNPs may change pending confirmatory sequencing and corrections to the deposited sequence.

dSNP ID are NCBI's Entrez dbSNP unique identifiers.

eAbbreviations and symbols: STM, S. Typhimurium LT2; PSLT, large virulence plasmid of S. Typhimurium LT2; STY, S. Typhi CT18; t, S. Typhi Ty2; SEN, S. Enteritidis PT4; SeD, S. Dublin; SeAg, S. Agona; del, deletion; tbd, to be determined; TER, terminating codon; nn, neutral non-polar; np, neutral polar; ap, acidic polar; bp, basic polar; np-, neutral slightly polar.