The Genetic Map of Salmonella typhimurium, Edition VIII

TOC

Chapter 110

KENNETH E. SANDERSON, ANDREW HESSEL, SHU-LIN LIU, and KENNETH E. RUDD

INTRODUCTION

We present a somewhat modified version of edition VIII of the genetic map of Salmonella typhimurium (official designation, Salmonella enterica serovar Typhimurium) strain LT2, which was published in 1995 (1717). We list a total of 1,160 genes; 1,081 of these have been located on the circular chromosome, and 29 of these are on pSLT, the 90-kb plasmid which is almost invariably found in LT2 lines; the remaining 50 genes are not yet mapped. The first edition of the map in 1965 contained 133 genes; later editions were published in 1967, 1970, 1972, 1978, and 1983, and edition VII, in 1988, listed a total of 750 genes (1721). A slightly modified version of edition VI of the map, presented originally in 1983, was published in the first edition of the present volumes (1718).

Strain LT2 is one of 25 different S. typhimurium isolates established by Lilleengen (1205) and designated LT1 to LT25; these strains represent 25 different phage sensitivity phenotypes. Many of these LT strains were used by Zinder and Lederberg for a study of genetic exchange, leading to the discovery of phage-mediated transduction (2236). M. Demerec obtained the LT strains from Zinder and began an exhaustive series of studies in the mid-1950s. The most important materials used were mutant strains derived from strain LT2, though a few were derived from strain LT7. Since the 1950s, strain LT2 has been the major focus of genetic and biochemical analysis, and thus the map we present here is derived primarily from work with LT2. However, more recently other strains have been used for specific reasons: e.g., some strains of S. typhimurium have been studied because they have higher levels of virulence than strain LT2; strain LT2 does not utilize histidine as sole carbon source, so other wild-type strains which do so have been used to study the hut operon.

All genes presently known to us are listed in Table 1 (p. 1907), with formerly used or alternative symbols in Table 2 (p. 1939). The references which describe these genes include a selection of the references from the first six editions which were presented in the first version of the present volumes (1718), those which were in edition VII published in 1988 (1721), and those which have been published since 1988 and which were included in the edition VIII published earlier (1717).

Table 1-01Genes of S. typhimurium.

Table 1-02Genes of S. typhimurium.

Table 1-03Genes of S. typhimurium.

Table 1-04Genes of S. typhimurium.

Table 1-05Genes of S. typhimurium.

Table 1-06Genes of S. typhimurium.

Table 1-07Genes of S. typhimurium.

Table 1-08Genes of S. typhimurium.

Table 1-09Genes of S. typhimurium.

Table 1-10Genes of S. typhimurium.

Table 1-11Genes of S. typhimurium.

Table 1-12Genes of S. typhimurium.

Table 1-13Genes of S. typhimurium.

Table 1-14Genes of S. typhimurium.

Table 1-15Genes of S. typhimurium.

Table 1-16Genes of S. typhimurium.

Table 1-17Genes of S. typhimurium.

Table 1-18Genes of S. typhimurium.

Table 1-19Genes of S. typhimurium.

Table 1-20Genes of S. typhimurium.

Table 1-21Genes of S. typhimurium.

Table 1-22Genes of S. typhimurium.

Table 1-23Genes of S. typhimurium.

Table 1-24Genes of S. typhimurium.

Table 1-25Genes of S. typhimurium.

Table 1-26Genes of S. typhimurium.

Table 1-27Genes of S. typhimurium.

Table 1-28Genes of S. typhimurium.

Table 2Alternative gene symbolsa

THE GENETIC MAP

The coordinate system used in the first four editions of the linkage map of S. typhimurium was determined by F-mediated conjugation; Hfr strains were used in interrupted conjugation experiments to place individual genes and P22-transduction linkage groups on a 138-min time-of-entry linkage map. In edition V, the map was changed to 100 units to correspond to the 100-min linkage map of Escherichia coli K-12. This was done to emphasize the similarity of the two genera and to facilitate comparisons. This 100-unit system was also used in editions VI and VII. In those editions, the 100 units of the map were based on "phage lengths" of the transducing phage P22 (1721). P22 can normally encapsulate about 45 kb of DNA; this is approximately 1% of the Salmonella chromosome. The map described here is the first edition in which we present a physical map of the chromosome with the interval between genes based directly on the length of the DNA. We report these gene intervals as centisomes (Cs), each one of which represents 1% of the length of DNA in the chromosome, and we also present the DNA segments in kilobase pairs (kb).

This physical map of the chromosome is based on a low-resolution genomic cleavage map determined by digestion with rare-cutting endonucleases and separation of the resulting fragments with pulsed-field gel electrophoresis (PFGE). Preliminary cleavage maps used the enzymes XbaI (1224), BlnI (1739, 2163), and I-CeuI (hereafter called CeuI) (1223). The overall structure of the chromosome shown in Fig. 1 (p. 1957) is based on a summary of work with these three enzymes (1222), plus some additional unpublished work.

Fig. 1Genetic map of S .typhimurium LT2. The gene designations used here are described in Table 1. The map is shown as 20 linear segments, representing the circular chromosome, and one linear segment representing the circular plasmid pSLT. The chromosome is composed of 100 centisomes (Cs); a scale covering 5 Cs is shown to the left of each segment. The scale is also designated in kilobases (Kb); the entire chromosome is designated as 4,808 kb (1222). In the middle of each segment are vertical lines which show the restriction maps for the endonucleases XbaI, CeuI, and BlnI, indicated by X, C, and B, respectively; a horizontal line indicates a restriction site. These sites were determined from PFGE (1222, 1224, 2162, 2163). The position of many genes around the chromosome were anchored using PFGE, through the XbaI map, and BlnI sites in Tn10 transposons which had transposed into these genes (1224, 1224, 2162). Genes which have been mapped in this way are indicated by a short horizontal bar to the left of the XbaI map, and the gene named is flagged with a superscript ?; e.g., the carAB genes at 1.6 Cs, the leu genes at 2.8 Cs, and the pan genes at 4.5 Cs have been mapped through analysis of Tn10 insertions in these genest (1222). Other genes are anchored through a specific restriction site which falls into a known gene; e.g., CeuI sites are found only in the rrn genes; thus, at 6.2 Cs the CeuI site indicates the location of the rrnH operon, at 58.1 Cs it indicates the location of the rrnG operon, and so on. In these cases, too we show a short horizontal bar to the left of the XbaI map. The locations of the genes between these fixed points are based on several types of data (see the text). In many cases, the location is based on phage-mediated transduction; the distance between genes was determined by assuming that the lengths of P22 and P1 transducing fragments are 1 and 2 Cs, respectively, and applying the formula developed by Wu (2170) to convert the percentage of joint transduction to map distance in centisomes, with modifications as described in Fig. 2 of Sanderson and Roth (1721). Parentheses around a gene symbol indicate that the location of the gene is known only approximately, usually from conjugation studies or sequence comparison with E. coli. An asterisk indicates that the gene has been mapped more precisely, usually by phage-mediated transduction, but that its position with respect to adjacent markers in not known. Arrows to the extreme right of the genes and operons indicate the direction or mRNA transcription at these loci. The endpoints of the region of the chromosome inverted with respect to E. coli are indicated by the word "inversion: and by arrows. The region of the chromsome for which high-resolution restirction mapping data have been published (2166) is delimited by the letters HR.

Source:

The genomic cleavage map shows the positions of 24 XbaI fragments, 12 BlnI fragments, and 7 CeuI fragments on a circular molecule of 4,808 kb of DNA (1222). The positions of genes on this cleavage map were determined by three methods. (i) Strains with insertions of the transposon Tn10 into known genes were analyzed. The presence of XbaI and BlnI sites in Tn10 permitted the location of these insertions, and thus of the gene into which Tn10 is inserted, through digestion of the DNA of the strain by the enzyme, followed by separation of the fragments by PFGE. A total of 109 independent strains with Tn10 insertions were reported, but some of these were not in genes of known function (1222); together with unpublished work done recently, a total of 75 genes have been located on the physical map solely through analysis of Tn10-containing strains. (ii) A total of 12 genes could be placed on the map because their DNA sequence included a site for the endonucleases XbaI, BlnI, or CeuI. (iii) In some situations, restriction mapping data or data from nucleotide sequences were used to correct or refine the locations of genes on the map. For example, a high-resolution restriction map for a 240-kb region spanning the 91 to 96 Cs region of the map located the positions of several genes (2166); these data were used to modify the locations of some genes in this interval.

The physically mapped Tn10 insertions and genes (discussed above) were used to align genes whose positions were known only by linkage data, and also were used as "anchors" for DNA sequence (described in detail below).

The chromosome is a closed circle of DNA, and early editions of the linkage map were shown in this way. In editions from V to VII the linkage map was displayed not as a circle but as 10 linear 10-min intervals. The present edition is similar, but because the number of known genes has increased, it is shown as 20 linear 5-Cs intervals (Fig. 1). This figure integrates gene location information discovered by genetic linkage and by physical analyses. The position of any gene shown was determined using the data available in the following preference order: first, by the order of genes found in sequenced DNA segments; second, by Tn10 or other physical anchors; third, by genetic linkage data; and, last, by extrapolation based on data from E. coli K-12 (see below). For display purposes, when gene orientation conflicts arose between physical and genetic data, preference was given to gene linkage information.

Most of the elements shown on the map are structural genes for proteins or, in a smaller number of cases, for rRNA or tRNA. We have not shown control elements for operons such as promoters, mRNA leaders, and terminators, nor have we shown the position of unnamed or poorly characterized chromosomal genes. We have not shown chromosomal elements such as repetitive extragenic palindromic (REP) sequences (771, 1423), but an exception is that we have indicated the positions of the six IS200 sequences which are mapped on the chromosome of LT2 (1134, 1136, 1724).

NOMENCLATURE

We use the system of nomenclature for genes which was established by Demerec et al. (437). This system uses a three-letter designation for the gene or operon, e.g., his for mutations in the genes for histidine synthesis, followed by a capital letter, also in italics, designating the specific gene in that operon, e.g., hisD for a mutation in the gene for histidinol dehydrogenase. This system has become the de facto standard for bacterial genetics. Authors considering a three-letter designation for a new gene in S. typhimurium should check the published maps of S. typhimurium and E. coli to see whether the proposed name has been used previously; they are also encouraged to contact the Salmonella Genetic Stock Center (SGSC) to see whether a proposed name has been used previously but not published. Allele number assignments should also be obtained from the SGSC. It is important to clear such numbers with the SGSC so that each mutation is identified by a unique allele number. A mutation is defined by its three-letter designation plus the allele number, i.e., the mutation his-1 might be initially thought to be hisD1, based on its perceived enzyme defect, but is later changed to hisE1. Thus, there should be only one his-1 mutation. Using assigned numbers is especially important for transposon insertions named by the "z– –" sytem proposed by Hong and Ames (824). In this case, the allele number may be the only identifier for a mutation, since all mutations mapped with "z– –" have a single series of allele numbers. As mapping is refined, a mutation’s "z– –" designation may change, but it retains its original allele number. It is therefore important that assigned allele numbers be used to avoid confusion of different laboratories using the same number for different insertions. It is also vital that strains be identified by a unique strain designation, which includes two or three capital letters (assigned for Salmonella strains by the SGSC to the laboratory, or by the E. coli Genetic Stock Center [CGSC] for E. coli strains) plus a number. The expanding use of the computer to keep records demands the use of correct strain designations; suffixes and phenotype designations after the strain designation, to refer to derivatives of a parent strain, are often not accepted by programs used for cataloging strains.

When possible, the same name should be used for homologous genes in related species such as E. coli and Salmonella spp. Many changes have been made in naming genes in these organisms to bring them into correspondence, and each edition of the maps has seen such changes. For example, a system of naming the genes for flagellar synthesis and function was proposed which recognizes the homology of these genera (891) and this system, now widely accepted, is used here. We encourage the trend to the use of these standardized names for E. coli and S. typhimurium for genes in other bacterial species as well when functional data and amino acid sequence data indicate that the genes are homologous.

PLASMID pSLT IN S. TYPHIMURIUM LT2

Because the plasmid content of strains of a species of bacteria is often extremely variable, the plasmids are not normally considered part of the genome; therefore, neither the F-factor in some lines of E. coli K-12 nor several types of plasmids frequently found in some wild-type Salmonella strains are treated as components of the normal genome. However, the original line of S. typhimurium LT2 contains a specific plasmid which we consider part of the genome. This plasmid has been called the virulence plasmid, the 90-kb plasmid, the 60-MDa plasmid, the cryptic plasmid, and pSLT (standing for salmonella LT); we use the last designation.

For two reasons, we consider this plasmid to be part of the normal genome of S. typhimurium LT2. The first is that the plasmid is an almost invariable part of the genome of LT2 lines. It is carried by all the lines of LT2 which we have tested, except for those few from which it has been intentionally eliminated. This is true even though LT2 has been in culture for many years and has been subjected to innumerable single-colony isolations. Genes on the plasmid which regulate replication, incompatibility, and partitioning (164, 242, 296) enable the plasmid to be maintained stably at low copy number. In addition, pSLT or a closely related plasmid is commonly found in independent S. typhimurium isolates from nature.

The second reason for considering pSLT to be part of the genome is that genes on the plasmid influence the phenotype in several ways, and thus mutations of genes on the plasmid may be mistaken for mutations of chromosomal genes. This influence of pSLT on the phenotype was first noted by Smith et al. (1837), who noted that it encoded Fin⁺ (fertility inhibition) properties, reducing the fertility of Hfr strains of S. typhimurium; special measures have been developed which restore fertility up to the level found in E. coli K-12 (1720). Many other genes have been detected due to their effect on phenotype. For example, mutations in the traT gene of pSLT cause an increase in outer membrane permeability, leading to an antibiotic-supersensitivity phenotype; this gene is listed in Table 1 (p. 1907). Other genes on pSLT, many of which influence the virulence of the strain, are also listed in Table 1 and are shown on a restriction map of pSLT in Fig. 1 (p. 1957).

SEQUENCED GENES OF S. TYPHIMURIUM

Gene identification can be largely based on open reading frames, codon usage distributions, and sequence-based evidence of homology (198, 1661). A significant amount of genomic DNA sequence has become available for S. typhimurium. By the end of 1994, we could assemble StySeq1, a nonredundant DNA sequence database modeled after the EcoSeq collection of E. coli genomic DNA sequences (1690). In fact, the extensive genomic sequence data available for E. coli (see, e.g., references 181 and 1853) cover close to two-thirds of the genome. Therefore, many S. typhimurium genes were identified at the sequence level as partial, but convincing, matches to one of the E. coli protein sequences in the EcoGene subset of SWISS-PROT (101).

StySeq1 has 197 contiguous sequence blocks (contigs) that do not overlap. Together, the nonredundant chromosomal genomic S. typhimurium StySeq1 DNA sequence collection is 548,508 bp in length. This represents 11.4% of the Salmonella chromosome, estimated to be 4,808 kb in length (1222). Eight contigs are greater than 10,000 bp in length. The longest contig, hisGstyM (Table 3 [p. 1940]), is 33,958 bp in length.

Table 3-01Sequenced genes of S. typhimuriuma

Table 3-02Sequenced genes of S. typhimuriuma

Table 3-03Sequenced genes of S. typhimuriuma

Table 3-04Sequenced genes of S. typhimuriuma

Table 3-05Sequenced genes of S. typhimuriuma

Table 3-06Sequenced genes of S. typhimuriuma

Table 3-07Sequenced genes of S. typhimuriuma

Table 3-08Sequenced genes of S. typhimuriuma

Table 3-09Sequenced genes of S. typhimuriuma

Table 3-10Sequenced genes of S. typhimuriuma

Table 3-11Sequenced genes of S. typhimuriuma

Table 3-12Sequenced genes of S. typhimuriuma

Table 3-13Sequenced genes of S. typhimuriuma

Table 3-14Sequenced genes of S. typhimuriuma

Table 3-15Sequenced genes of S. typhimuriuma

Table 3-16Sequenced genes of S. typhimuriuma

Of the 197 DNA sequences in this collection (Table 3), 191 are ordered and oriented as they might be on the S. typhimurium chromosome. This was accomplished in several ways: physical anchor, genetic pin, and extrapolation.

i) In the physical anchor method, if a Tn10 insertion, rare restriction site, or other direct physical link could be associated with one of the genes from StySeq, it was anchored and the positions of the other nearby genes were calculated based on a single base-pair anchor point per contig. Gene positions thus have high local precision (1-bp resolution) and coarse genomic map position accuracy, based on analysis by PFGE (ranging from 1,000 bp in some situations to over 10,000 bp, depending on the locations of restriction sites for the enzymes used). Unsequenced genes could also be anchored, and this information was taken into account in mapping the unsequenced genes depicted in Fig. 1. Sixty-two StySeq1 contigs were positioned in this way. (ii) In the genetic pin method, gene positions were assigned to a number of sequenced and unsequenced genes on the basis of linkage data. The positions of the anchors were used to realign conjugation and transduction mapping distances, allowing the integration of physical and genetic maps presented in Fig. 1. In turn, those genetic map positions were used to pin more sequences to the integrated genomic map. An additional 93 contigs in Table 3 were positioned by this approach. (iii) The extrapolation method was used to position a final 36 contigs by using map position information from E. coli-Salmonella gene pairs to extrapolate a position.

The aligned DNA sequences are ordered to coincide with the orientations of homologous sequences in the EcoSeq7 collection of aligned and oriented E. coli genes. Although some local inversions are likely to have occurred, most comparisons indicate a close correlation of the orientations and map positions of genes between E. coli and S. typhimurium, with one major exception. There is a large inversion of a chromosomal segment relative to the corresponding E. coli region with endpoints near 26 and 36 min on the genetic map (1721). We could localize this region on the physical map (Fig. 1), and this allowed us to set the orientation of genes in this region of S. typhimurium as being opposite to that of the E. coli homologs in this inverted segment.

Alignment of all but six of the StySeq1 contigs, at least as a best approximation subject to constant refinement, allowed the genes encoded in the DNA sequences to also be aligned. In this way, 523 protein-coding genes and 15 structural RNA genes were given genomic map positions based locally on DNA sequence information and globally on a combination of physical anchor points, genetic cross data, and extrapolation from the E. coli map. Fifty-one unnamed genes (described as orf or similar in GenBank entries) were given provisional names beginning with the letter "y" (1690); these genes were excluded from Table 1 but are listed in Table 3.

Until a larger proportion of the S. typhimurium genome is sequenced, the genetic linkage data will remain useful as the basis for the map. E. coli has a high-resolution genomic restriction map for the entire chromosome, whereas the high-resolution map of S. typhimurium is being assembled as parts (2166). Nonetheless, several genes were physically positioned by DNA sequence and high-resolution restriction map data in the 91 to 96 Cs region of the S. typhimurium LT2 chromosome (2166) by using a single anchor.

Having access to both E. coli and S. typhimurium DNA sequence over the same region provides an opportunity to predict frameshift corrections and helps ensure the highest level of accuracy. Other organisms help identify probable new genes in S. typhimurium with homologs as well, but the comparison to E. coli involves enough preference for third-position changes to establish the correct frame for most protein-coding genes.

MAP REFINEMENT

If errors are detected in this work, we hope that this information will be transmitted to us to allow corrections. To assist in the preparation of future map editions or updates, we would appreciate receiving any information regarding the position and function of new genes, or refinements to the positions or roles of the genes described here. Electronic mail should be addressed to kesander@acs.ucalgary.ca and rudd@ncbi.nlm.nih.gov. StySeq1 and associated files can be retrieved in electronic form from the anonymous ftp site ncbi.nlm.nih.gov in the /repository/Eco/Sty directory. Diskettes will be mailed on request to those without Internet access.

ACKNOWLEDGMENTS

The assistance of numerous investigators in providing strains used for Tn10 mapping and in furnishing unpublished information is gratefully acknowledged. We are especially grateful to John R. Roth for providing invaluable information and discussions as well as editorial comments. We also acknowledge the excellent editorial comments provided by Charles G. Miller. We thank K. K. Wong and Michael McClelland for their significant contribution to the genomic mapping of S. typhimurium. We also thank Lauryl M. J. Nutter for assistance with the final preparation of this manuscript. K.E.R. gives special thanks to Amos Bairoch for providing SWISS-PROT Salmonella sequences and many helpful discussions, to Jinghui Zhang for alignment of sequences to EcoSeq, and to Webb Miller for many valuable conversations and algorithm development. During the preparation of this report, K.E.S. was supported by an operating grant and an infrastructure grant from the Natural Sciences and Engineering Research Council, and by grant RO1 AI34829 from the National Institute of Allergy and Infectious Diseases.

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