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Microbiology and Molecular Biology Reviews, September 1998, p. 814-984, Vol. 62, No. 3
1092-2172/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Linkage Map of Escherichia coli K-12, Edition 10: The Traditional Map

Mary K. B. Berlyn*

Department of Biology and School of Forestry and Environmental Studies, Yale University, New Haven, Connecticut 06520-8104

SUMMARY
INTRODUCTION
MAP UNITS
NOMENCLATURE
    Gene Symbol Convention
    The Issue of Stability
ACKNOWLEDGMENTS
REFERENCES

SUMMARY
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This map is an update of the edition 9 map by Berlyn et al. (M. K. B. Berlyn, K. B. Low, and K. E. Rudd, p. 1715-1902, in F. C. Neidhardt et al., ed., Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed., vol. 2, 1996). It uses coordinates established by the completed sequence, expressed as 100 minutes for the entire circular map, and adds new genes discovered and established since 1996 and eliminates those shown to correspond to other known genes. The latter are included as synonyms. An alphabetical list of genes showing map location, synonyms, the protein or RNA product of the gene, phenotypes of mutants, and reference citations is provided. In addition to genes known to correspond to gene sequences, other genes, often older, that are described by phenotype and older mapping techniques and that have not been correlated with sequences are included.

INTRODUCTION
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Previously, Berlyn et al. (323) presented the traditional map, the EcoMap physical map, and a map by Singer and Low showing the distribution of the Gross-Singer transposon set around the chromosome. The map in this paper is a revision of that traditional map of Escherichia coli K-12, the linkage map of known genes and other functional sites (Fig. 1), and the physical map, EcoMap 10, of Kenneth Rudd is presented in the companion article (3763a).


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  		FIG. 1.   Linear drawing of circular linkage map of E. coli K-12. Symbols are defined in Table 1. Arrows show the direction of transcription. Where T-bars are used to display groups of genes, the length of the T shows the approximate length and position of the group in terms of the map coordinates, allowing visual ordering of closely packed groups.

The linkage map in this presentation includes genes located primarily by restriction, sequence, and cotransduction data reported in the literature and databases. It uses coordinates based on the complete sequence released by the Blattner laboratory. Obviously, the sequence is now the major resource for placing genes on the map. In some regions the placement represents a shift from the edition 9 map, which was based on coordinates of Rudd's EcoMap 7 composite of sequenced genes and regions (27, 33, 395, 568, 569, 926, 3308, 3465, 4127, 4128), placed on the physical map of Escherichia coli (2291, 3763b) by restriction and sequence comparisons. Those map positions were based on the results in the literature and on EcoMap and GenBank database entries. EcoMap 10 coordinates are of course also based on the completed sequence, and cross-consulting this summary map and the EcoMap that follows should be straightforward.

The linkage map of Fig. 1 includes 2,220 genes and about 40 other chromosomal markers, such as phage attachment sites, defective-phage elements, replication origins and termini, and other features traditionally included on the published linkage map. It does not include open reading frames (ORFs) lacking evidence for expression, with unknown functions or putative functions inferred by sequence homologies only. A few exceptions occur for Salmonella genes where the inference is strong that they are also expressed in E. coli. The ORFs not included in this map can be found on EcoMap 10. The Fig. 1 map places the genes that can be found in sequence annotation and EcoMap 10 on the right side of the line. On the left side are genes not present on physical maps or the sequence, and in most cases these are not connected to a specific point on the axis to indicate that the localization is only approximate. As in previous editions of the E. coli linkage map (187, 188, 189, 190, 190a, 323, 4368, 4369, 4370, 4371), an asterisk indicates that the gene is not precisely located with respect to near neighbors and parentheses indicate that the location is even more uncertain and that the gene is located only within that general region. I have been very conservative about removing these from the map; even though the usefulness of some of these may be quite limited, there will probably be cases where the old, sometimes poorly characterized phenotype may be helpful in ascribing functions and phenotypic effects to ORFs. Also shown on the left side in boldface followed by colons are operon names that are distinct from any gene name within the operon and termination and attachment sites. The arrows indicate the direction of transcription and span genes included within a transcription unit.

Updates of map information are available in electronic form from several sites. These include the E. coli Genetic Stock Center's (CGSC's) World Wide Web server at URL http://cgsc.biology.yale.edu, which provides an interface for querying the database and retrieving formatted reports about genes, map regions, strains, and mutations, etc. (323a); the National Center for Biotechnology Information ftp site for EcoSeq and EcoMap, ncbi.nlm.nih.gov/repository/Eco/EcoMap7; the Colibri map at http://www.pasteur.fr/Bio/Colibri.html, the ECDC map at http://susi.bio.unigiessen.de/ecdc.html, the site for the sequencing project at the University of Wisconsin, http://www.genetics.wisc.edu, a gene-protein database, http://www.mbl.edu/html/ecoli.html, Genome Information Broker at http://mol.genes.nig.ac.jp/ecoli, and others. See also Rudd (3673). The references attempt to document map information, the basic definition of the gene's function, and expression information and do not include information relating to detailed physical structure, active site in vitro mutagenesis, or enzyme mechanism. Earlier map papers contain additional references for some of the loci (188-190a, 323).

MAP UNITS
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Since the 1976 recalibration of the linkage map in terms of minutes required for time of entry of markers in interrupted conjugation experiments, the standard representation of the map has used the basic units of minutes and a total length of 100 minutes (190a). This has been a convenient and accepted coordinate system for the map, and although the current map units are based on restriction and sequence data rather than time of entry, we retain the term minute for 1/100 of the length of the chromosome. Both the CGSC database and EcoMap use as "left endpoints" the counterclockwise boundary of the coding region, and genes in Fig. 1 are placed approximately at these coordinates, with the higher-resolution map of Rudd (3763a) providing more exact placement, showing nucleotide and minute coordinates for the physically mapped genes.

NOMENCLATURE
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Gene Symbol Convention

The standard genetic nomenclature for E. coli is that of Demerec et al. (1016), as subsequently amended through use, and as described in Instructions to Authors for the Journal of Bacteriology (see also reference 3821). This map, like those preceding it, follows those nomenclatural conventions. Accordingly, we have adhered to a three-letter lowercase mnemonic symbol, with an uppercase letter added when there are two or more genes in that mnemonic category. If authors have added an uppercase letter for a gene in a single-instance category, we have used that published four-letter symbol. For attachment sites and noncoding features of the chromosome, etc., the same standard has not been used, and we have continued to use the variable-length symbols historically applied to these sites. We have continued the convention proposed for sites of termination of replication and repetitive sequences, by using italicized symbols with the first letter uppercase.

The Issue of Stability

Many names have been changed by investigators since the 1990 map was published. When those changes were part of a systematic revision of nomenclature (often aimed at clarifying usage and resolving conflicts) for a group of related genes and were in compliance with the current E. coli gene nomenclature system, or were changed for compelling mnemonic reasons or for resolution of redundancy or conflict, also in conformance with the standard system, we have adopted those changes. We have not adopted and we wish to discourage changes of valid preexisting names proposed by authors simply because they believe that theirs is a symbol signifying a more apt or accurate mnemonic. For example, a previously published name based on the pathway or phenotype is valid and should not, simply as a matter of course, be replaced by an alternate mnemonic based on the name of the enzyme that the gene codes for once that functional information has been determined. In general, the stability of a name has more value than improved nuances. In a few cases, we have been compelled to use a new name, despite the apparent validity of the original name, simply because the new name has been widely adopted in the literature. In a number of cases, a new gene has been assigned a symbol which has already been used or which is simultaneously proposed for another gene, with the two mnemonics having entirely different meanings. These names have had to be resolved, usually by changing the newer assignment. In a few cases, a uniquely named gene has been shown later to belong to a category for which a symbol already exists, and the latter symbol has been used instead of the earlier assignment. There is one case in this paper where use of a symbol already assigned to a different gene was strongly preferred by authors, and I was very reluctant to suggest a new symbol for the earlier, published gene name to the earlier authors, since that symbol has been used in a number of publications; for the interim I have broken convention to assign the newer genes temporary symbols with asterisks (gsp*), in order to show them on the map and in the hope of resolving that naming with the usual precedence custom in the near future. Some synonymy is unavoidable, since a gene under study may be named and described in print before its identity to a known gene is discovered. However, a common practice in the recent literature seems to allow publication of an author's preliminary name for a gene even if its identity to a known gene has been discovered before publication, and that practice creates unnecessary synonymy. Alternate gene symbols are listed in Table 1, and Table 2 provides an alphabetized list of such symbols with cross-references to the symbols used in Table 1.

                              
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  		TABLE 1.   E. coli genes and replication- or phage-related sitesa

                              
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  		TABLE 2.   Alternate gene symbols

There is a standing tradition of coordinating gene symbols between the CGSC and the Salmonella Genetic Stock Center to avoid the assignment of the same symbol to different genes in the two organisms and the assignment of different symbols to homologous genes, insofar as this coordination is feasible. We have not, however, changed names of E. coli genes in order to extend this tradition to other bacteria or other organisms. The desirability and feasibility of uniform nomenclature conventions for all bacteria or other microbial groupings are currently only topics of discussion and conjecture, and changes to enhance similarities in an ad hoc, piecemeal fashion seem counterproductive at the present time. Readers are reminded that symbol changes create discontinuity with previous literature concerning genes, with even more serious ramifications for allele designations, since unique allele numbers are assigned on the basis of the three letter mnemonic and changes in a symbol may necessitate renumbering of alleles as well.

ACKNOWLEDGMENTS
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This work was supported by the National Science Foundation grants BIR9315421 and BIR9010005.

I thank Stanley Letovsky and Peter Kalamarides for their work in implementation and system administration for the database, which allowed direct retrieval of all the various Table 1 data and the drawing of map segments directly from the CGSC database. Even so, extensive layout work was required for the final figure, and I am indebted to Elise Low for her skill and patience in doing that during all the revisions that went into this version of the map. A number of people have worked tirelessly to get this paper together. Special thanks again go to Elise Low for editing graphics files and for unending proofreading and cross-checks on the tables and references in addition to the layout work. Completion of this task owes much to her skill and her dedication to accuracy and timeliness and to Peter Kalamarides for writing and executing scripts that brought the tables together at every critical juncture. Special thanks also go to Linda Mattice and Narinder Whitehead for valuable help with proofreading and tracking down publications for both versions and for keeping the stock center on course during this work. I'm especially grateful to all of the above for their unstinting efforts at deadline-approaching time. I thank Graeme Berlyn for sharing and helping with use of his computer setup during the printing operation, and also James Bryan for table formatting help in the earlier edition. Brooks Low and Kenn Rudd coauthored the 1996 edition of the map and therefore were major contributors to this map as well; I thank them for that collaboration and their continued help and support. Kenn Rudd and I have attempted to keep this map and the physical map compatible in terms of names and annotations; Kenn has been crucial in keeping me updated with regard to his new information, displaying his characteristic dedication and generosity with regard to his sequence-to-gene detection and expertise. Special thanks this year go to Edward Adelberg for supplying the database with bibliographic updates based on his scanning and annotation of Medline references in the context of his own bibliographic database of current papers in E. coli genetics developed and kept up to date over the past 2 1/2 years. They have been enormously helpful in our attempts to keep the CGSC database current with respect to literature on E. coli genes. These maps continue the tradition of E. coli K-12 linkage map editions so capably constructed by Barbara J. Bachmann over the past 20 years and that of her predecessors for E. coli maps dating back to 1958. Our debt to these previous maps is obvious. The accuracy of the great majority of gene positions on the map is completely indebted to the American and Japanese sequencing projects, and for this particular version of the map, especially to GenBank access to the complete sequence submitted by Fred Blattner and his colleagues as part of the Genome Sequencing project in Wisconsin. And of course we are indebted to numerous scientists who have provided helpful map-related information in the form of discussion, corrections of database inaccuracies, preprints, and personal communications.

FOOTNOTES

* Mailing address: 355 Osborn Memorial Laboratories, 165 Prospect St., Box 208104, Yale University, New Haven, CT 06520-8104. Phone: (203) 432-9997. Fax: (203) 432-3854. E-mail: mary.berlyn{at}yale.edu.

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