Escherichia coli Gene Products: Physiological Functions and Common Ancestries

TOC

Chapter 116

MONICA RILEY and BERNARD LABEDAN

Determination of the complete sequence of E. coli K-12 strains MG1655 and W3110 and analysis of the biological import of the sequences have proceeded rapidly since publication of several of the Escherichia coli and Salmonella 2nd Edition chapters. As an interim measure until new chapters are written, one link to the Internet lists will provide you with many links to individual Web sites, each accentuating different aspects of genomic analysis of E. coli. The link is: http://www.grs.nig.ac.jp/WGR/link/link_E.coli_e.html

INTRODUCTION

Knowledge about Escherichia coli genes, their gene products, and their roles in cell physiology has reached a point that invites a look at the horizon. We can look at what we know today and see it in a context of some kind of totality of knowledge about E. coli genes and their gene products that will be reached in time. Assembled here is a table of E. coli K-12 genes whose gene products are known, organized by principal physiological function, with literature references through most of 1994. We have summarized the distribution of gene products among physiological and functional categories. Also assembled is information on the amino acid sequence relatedness of E. coli proteins and classification of the functional relatedness of sequence-related pairs. These results are interpreted in the context of evolution, with the objective of understanding more about how genes evolve and ultimately of identifying the relatively small numbers of unique ancestral sequences that probably have generated the families of sequences we observe in E. coli today. We also present a compilation of multiple enzymes present in E. coli that carry out the same biochemical reaction. Some multiple enzymes are related by sequence and thus are likely to have descended from a common ancestor, but others have no apparent sequence relationship and may have derived from different ancestral sequences independently by convergent evolution, or they may have been acquired from another source by lateral transmission. We discuss the capacity for these multiple enzymes to serve as a rich resource that contributes significantly to the adaptive capability of E. coli.

FUNCTIONAL CATEGORIES

Table 1 presents a scheme of categories of cellular functions. Any such classification is arbitrary in that there are many ways to organize the complex function of a cell, and it is artificial in that it seems to create hard boundaries between functional categories when of course cellular functions and processes are complexly intertwined. Also, some categories refer to metabolic pathways, others such as "transport" refer to processes, and still others such as "membranes" refer to cellular structure, categories that are not comparable in kind or mutually exclusive. Thus, one gene product can belong to more than one category. Nevertheless, this classification scheme allows a gross assignment of a major cellular role to each gene and gene product. This allows us to view as a whole the activities and division of labor of the genes and gene products of E. coli that have been characterized to date.

Table 1Categories of cellular functions

Table 2 lists 1,827 characterized gene products of E. coli K-12. Since not all known E. coli genes have characterized gene products, the list of genes that have been sequenced and mapped (see chapter 109) is longer than the list of genes for which the function of the gene product is known. We followed certain rules in choosing genes and gene products for listing. Most open reading frames with hypothetically translated gene products were excluded, except for a few with strong sequence similarities to other well-characterized gene products whose functions are known. These are noted as "putative" or "possible" functions in the table. Genes were excluded whose presence was simply deduced from the phenotype of a mutant, when the effect of the mutation was not described in enough detail to allow assignment of the gene product to a physiological category. However, genes were included whose effect has been characterized as to the physiological role in the cell even though the nature of the actual gene product (enzyme, regulator, permease, etc.) is not yet clear. Such genes were included in the list, assigned a physiological category, but classified as having only a phenotype known rather than having the type of gene product specified. All of the genes in the compilation by Barbara Bachmann in the first edition of this work (88) have been retained, even though some genes are are known only by phenotype (228 of them). One hesitates to delete information of any kind, but it is possible that "old" genes that were known only by mutant phenotype and have not been subjects of study for, say, 20 years should be removed from any subsequent listing of gene products of E. coli.

Table 2-01E.coli genes grouped by function of gene product

Table 2-02E.coli genes grouped by function of gene product

Table 2-03E.coli genes grouped by function of gene product

Table 2-04E.coli genes grouped by function of gene product

Table 2-05E.coli genes grouped by function of gene product

Table 2-06E.coli genes grouped by function of gene product

Table 2-07E.coli genes grouped by function of gene product

Table 2-08E.coli genes grouped by function of gene product

Table 2-09E.coli genes grouped by function of gene product

Table 2-10E.coli genes grouped by function of gene product

Table 2-11E.coli genes grouped by function of gene product

Table 2-12E.coli genes grouped by function of gene product

Table 2-13E.coli genes grouped by function of gene product

Table 2-14E.coli genes grouped by function of gene product

Table 2-15E.coli genes grouped by function of gene product

Table 2-16E.coli genes grouped by function of gene product

Table 2-17E.coli genes grouped by function of gene product

Table 2-18E.coli genes grouped by function of gene product

Table 2-19E.coli genes grouped by function of gene product

Table 2-20E.coli genes grouped by function of gene product

Table 2-21E.coli genes grouped by function of gene product

Table 2-22E.coli genes grouped by function of gene product

Table 2-23E.coli genes grouped by function of gene product

Table 2-24E.coli genes grouped by function of gene product

Table 2-25E.coli genes grouped by function of gene product

Table 2-26E.coli genes grouped by function of gene product

Table 2-27E.coli genes grouped by function of gene product

Table 2-28E.coli genes grouped by function of gene product

Table 2-29E.coli genes grouped by function of gene product

Table 2-30E.coli genes grouped by function of gene product

Table 2-31E.coli genes grouped by function of gene product

Table 2-32E.coli genes grouped by function of gene product

References of genes that were listed in an earlier compilation of gene products (1652) are updated in Table 2 when possible. The choice of references in Table 2 has some arbitrary features. In the previous compilation of gene products of E. coli (1652), early papers on a gene product were cited as well as more recent references. In Table 2 in this chapter, the accent is on more recent work on each gene product. Citations were limited arbitrarily to three per entry. It was not possible in any reasonable time frame to become well enough informed to cite the most meritorious work for each entry; instead, citation to some of the more recent papers on each entry is used. Earlier literature should be accessible by tracing back citations. Genes and gene products that have not received attention in recent years still carry their original citations. The citations in Table 2 are intended to help the reader enter the literature, not to make any judgment on the priority or scientific value of any paper cited or omitted.

Table 2 shows only one assignment to a category of function for each gene product, even though some gene products play multiple roles in the cell. For instance, in metabolism, the acetyl kinase enzyme functions in aerobic catabolism of acetate as a carbon source, but it also is an important enzyme of anaerobic fermentation. A protein kinase or an adenylylation enzyme can be classified either as an enzyme that modifies proteins or as a regulator. Likewise, a porin can be classified either as a transport entity or as a part of a membrane component of the cell structure. A phosphotransferase enzyme can be classified either as a transport entity or as an enzyme of phosphorus metabolism. In each such case, multiple assignments of functional categories have been made and all are provided in the electronic version of the table. However, in the printed version of Table 2 here, one physiological category has been chosen for each gene product and the entries are ordered by that one category of cellular function. The electronic version of the data will be useful to reveal other functions and also will permit views of many other aspects of the data. To this end, the tabulation of the data in electronic format is sortable for instance alphabetically by gene, alphabetically by gene type, numerically by EC number, and so forth. The data is in a database for PC computers called GenProtEc, available by anonymous ftp from mbl.edu as /pub/ecoli.zip or by mail on an MS-DOS disk from M. Riley on request.

Besides providing a list of the presently known gene products of E. coli and entries to the literature for each gene product, Table 2 contains information on how many currently known gene products carry out each kind of functions. Some of this information is shown in Table 1 and is summarized in Tables 3 and 4. The number of gene products assigned to each physiological category is shown in Table 1. These are grouped and summarized in Table 3. Small-molecule metabolism involves 435 genes or 22.9% of the presently known whole. Large-molecule metabolism involves an even larger fraction: 643 genes or 33.9% of the whole. Of the 370 genes assigned to cell processes, transport involves 253 genes, by far the largest component. Transport functions alone make up 13.3% of the whole. Some of the miscellaneous group are genes concerned with phages and plasmids; others, such as the many heat shock proteins or drug resistance factors, are poorly characterized gene products that will be better delineated with further study.

Table 3Distribution of E. coli gene products among physiological categories

Table 4Distribution types of gene products among classifiable E. coli genesa

The number of E. coli gene products that fall in each major category of type of gene product is shown in Table 4. In this view, gene products are classified as either an enzyme, a regulator, a transporter, a protein factor, a membrane component, or an RNA molecule. Assignment of the type of gene product could be made for only 1,616 of the 1,897 genes. The rest are too vaguely defined at present to know what the gene product is. Of the 1,616 gene products, enzymes of metabolism constitute the major fraction. The enzymes and proteins of transport functions and regulatory function constitute two other large categories. The number of gene products in the category of structural elements of the cell is relatively small compared with metabolic functions. This is caused partly by the fact that many membrane components have roles in cellular processes such as transport or cell division and thus were not listed primarily as structural elements and partly by the fact that the enzymes of synthesis of macromolecular components of the cell structure such as peptidoglycans or phospholipids are not classified as structural elements but rather as metabolic functions. Also, we recognize that we still have much to learn about the genetic basis of the structure of the cell and the process of assembly of structural components.

As the remainder of the E. coli genes are sequenced and function is assigned to the gene products, the proportions of cellular roles will probably change. More functions of cell structure and its assembly probably will be added. Possibly, more global regulatory mechanisms will surface. There is room for many more aspects of the life process in the unsequenced portion of the E. coli genome. Even in the parts already sequenced, the Blattner group has found many non-open reading frames, that is, sequences that do not constitute transcribable genes as we presently understand them. These sequences have no known shape or function and have been dubbed grey holes (395). After we have unlocked all their secrets, the distribution of functions of all E. coli gene products may change from what we are seeing today.

RELATIONSHIPS AMONG GENES, ENZYMES, AND REACTIONS

In its time, the historic one gene-one enzyme hypothesis illuminated the relationship of genes to cellular function (114). Later, the word "cistron" was introduced to define the genetic element coding for a gene product that is not subdividable by the trans complementation test (134). The cistron emphasized the basic genetic element as the coding entity for a polypeptide chain rather than the genetic unit underlying a functional entity such as an enzyme. Today, with many genes, enzymes, and reactions characterized in E. coli, we appreciate the many types of relationships that exist in reality between genes and enzymes and the reactions they catalyze.

In many cases, one gene encodes one polypeptide, which catalyzes one biochemical reaction. However, these relationships are not always one to one to one. Figure 1 diagrams some of the other types of relationships found for reactions, enzymes, and genes in E. coli. In the case of isozymes such as fumarase, more than one gene and polypeptide are capable of carrying out one reaction. In a different kind of case, a single polypeptide carries out more than one reaction. Illustrating this is the FadB polypeptide, which catalyzes four separate reactions. Another kind of case is TrpD. The N-terminal part of the TrpD polypeptide associates with the TrpE polypeptide to catalyze one reaction, and the C-terminal part of TrpD catalyzes another reaction. One gene can make two polypeptides when, as in the case of the speD gene, the initial gene product is further processed into two nonidentical subunits. Sometimes there is confusion about the relationships of enzymes, reactions, and EC numbers. (An EC number, designated by the Enzyme Commission of the Internatiuonal Union of Biochemistry and Molecular Biology, represents a biochemical reaction and thus is associated with each component of a multimeric enzyme [1518].) Therefore, in the case of a multisubunit enzyme, like succinate dehydrogenase, more than one gene and one polypeptide are required to carry out the one reaction described by one EC number, in this case 1.3.99.1. Finally, levels of organization can be more complex than multimeric enzymes. Multienzyme complexes like pyruvate dehydrogenase contain more than one multimeric enzyme that work together in catalyzing a concerted set of reactions.

Fig. 1Types of gene-enzyme-reaction relationships in E. coli. Nodes labelled R, E, and G represent the number of unique reactions, enzymes, and genes, respectively, present in E. coli K-12 for each example. A boxed node for an enzyme signifies a dimer.

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Because of the variable relationships between polypeptides and reactions, there are many possible relationships of genes to metabolic reactions. Analysis of mutant phenotypes and genetic complementation tests can be complicated by the variety of possible gene-enzyme-reaction relationships.

MULTIPLE ENZYMES

As is the case for isozymes, some metabolic reactions are carried out in E. coli by more than one enzyme. Table 5 lists examples of "multiple" proteins that catalyze the same reaction or very similar reactions. Only enzymes of metabolism of small molecules are shown. Multiple genes and enzymes also exist for metabolism of large molecules such as DNA polymerases, sigma factors, and nucleases, but these are not included in Table 5.

Why does E. coli contain more than one enzyme for so many reactions? Are they redundant? Do the multiple enzymes serve in the cell as backup systems in case of loss of one enzyme for a vital function? In fact, one may ask how we were able to isolate mutants lacking one enzyme if another enzyme for that reaction existed in the cell. One answer is that quite a few mutants are leaky and that leakiness in many cases is known now to be a consequence of multiple enzymes. Another answer is that the conditions under which many of the pairs of genes are expressed can differ and also the conditions under which the two enzymes are catalytically active can differ. A list of ways that multiple enzymes for the same reaction differ from each other is given in Table 6.

Table 6Ways in which multiple enzymes differ from each other

This phenomenon of enzyme repetition and specialization must have the effect of extending the metabolic capabilities of E. coli. With genes producing a given enzyme under more than one set of conditions and with multiple enzymes being active under different conditions, the bacteria are able to address successfully a wide range of environmental conditions that require enzymes with appropriate properties to become available. For instance, the speA gene produces the biosynthetic arginine decarboxylase; gene expression is induced by growth in minimal media and is repressed by putrescine and spermidine. The enzyme is located in the periplasm and is inhibited by cyclic AMP (1339). The adi gene, on the other hand, produces the degradative arginine decarboxylase, and gene expression is induced under acid conditions and anaerobiosis. The degradative enzyme is located in the cytoplasm (1905). Another example involves the sodA and sodB genes. The sodA gene is induced by oxidative stress under aerobic conditions to produce a manganese-activated superoxide dismutase, whereas the sodB gene is expressed under both aerobic and anaerobic conditions, constitutively producing an iron-activated superoxide dismutase (786).

In terms of evolution, one can ask if multiple enzymes descended from common ancestors. If so, one might expect to see residual similarities in amino acid sequence. Comparison of sequences of the 75 pairs of isozymes for which the sequence is known for both proteins showed that 44 of 75 pairs are related by sequence, some very closely related, some less so. The other 31 pairs were not demonstrably related by sequence (Table 7). Therefore, somewhat over half of the pairs of the currently known multiple enzymes involved in small-molecule metabolism seem to be related by a common ancestor. The other half either do not share ancestry or have diverged to a point that the relationship is no longer detectable. It is possible that the pairs that are not related by sequence are examples of convergent evolution, that is, descendants of separate ancestral sequences evolving to the same function; alternatively, the gene for one of a pair of isozymes might have been acquired in the past by lateral transfer from another organism.

Table 7Sequence relationships between pairs of multiple enzymes

PROTEIN SEQUENCE RELATIONSHIPS AS A TOOL TO STUDY THE ORIGIN OF E. COLI GENES

In the context of evolution, we believe that many of the genes of present-day E. coli originated by a process of duplication of ancestral genes followed by divergence, then by further duplication of these genes, followed by more divergence, and so on (1125, 1454). The very early genes and their proteins are visualized as having broad specificity of action, which then narrowed successively in the descendants formed by duplication and divergence (896, 2234). If all descendants of all ancestral sequences still retain detectable vestiges of sequence similarity, we could expect to be able to identify all ancestral relationships and build a set of trees of evolutionary descent of all organisms that extend back to a set of unique ancestral sequences that were parents of all the genes and gene products extant today.

By examining the relationships among protein sequences within one organism, one is identifying pairs of proteins which display significant level of similarity. This is generally interpreted as a demonstration that these proteins are products of paralogous genes, i.e., homologous genes that descended from a common ancestor by duplication and divergence, according to the definitions proposed by Fitch (544), who opposed paralogy (homology in which divergence occurs after gene duplication in the same species) and orthology (divergence of homologous genes through speciation). Moreover, groups of proteins whose sequences are related could also be detected, meaning it is possible to identify present-day genes descending from shared ancestral genes (familial relationships within a genome).

We have engaged in such a study, identifying pairs and groups of E. coli proteins whose sequence similarities could indicate shared ancestry. Indeed, a higher percentage of all its protein sequences are available for E. coli than for any other organism, providing the opportunity to test for compatibility of the sequence relationships among E. coli proteins with accepted ideas of mechanisms of molecular evolution. E. coli is also the organism for which the greatest proportion of chromosomal genes sequenced to date correspond to genes previously well characterized in terms of function of gene product and regulation. No other organism provides a better opportunity to determine how many ancestral relationships can be detected and how important the mechanism of duplication and divergence has been during the evolution of a genome and its encoded proteins than the massively sequenced E. coli genome does.

Our main goal being to identify descendants of past whole-gene duplications, we undertook to detect any significant similarity extending along either the whole sequence or at least long stretches of each amino acid sequence. We call this kind of similarity "extended sequence similarity," as opposed to "local similarity," i.e., similarity localized to domains or motifs. To do that, we analyzed all the E. coli K-12 chromosomal sequences longer than 100 residues present in the SwissProt database by using two different algorithms designed for extended sequence homology searches. In one study, we first used the well-known FASTA program (1518) and retained any pair displaying alignment of segments at least 100 amino acids long and with at least 20% identity. Then, from the obtained FASTA alignments, we excluded those of questionable biological significance by imposing a high threshold on the number of gaps (corresponding to a NAS [Normalized Alignment Score] of at least 180, calculated according to the method of Doolittle et al. [465]). In a subsequent study, the ALLALLDB program (Darwin package available at the CRBG server at the ETH, Zurich, Switzerland) was used to detect any match corresponding to an alignment of at least 100 amino acid residues and separated no more than 250 PAM (percent accepted mutations) units (644). These two approaches gave us very similar results (1060, 1061), which can be summarized as follows.

The 1,862 protein sequences derived from the sequences of E. coli chromosomal genes present in SwissProt database (version 28) (1,339 known genes and 523 open reading frames) were compared in all pairwise combinations. This operation gave us 2,329 matches separated by no more than 250 PAM units. The distribution of the PAM values was found to be Gaussian only when confined to the matches displaying identity values greater than 20% (Fig. 2). The large majority of the excess pairs with identity values less than 20% but PAM values less than 250 corresponded to the more distantly related members of large families (as defined below).

Fig. 2Distribution of PAM values among 2,329 pairs of protein sequences. In black is shown the number of pairs for all 2,329 matches. In grey is shown the number of pairs that have amino acid identity values greater than 20%.

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The 2,329 pairs corresponded to a large set of 971 sequences (52.15% of the total) displaying similarities to at least one other sequence of this set. An alphabetical list of these 971 proteins (using the SwissProt mnemonics) that have at least one paralogous partner is given in Table 8; 786 of these sequences code for proteins the function of which is known, amounting to 58.7% of all known and sequenced genes. The rest correspond to 185 open reading frames (34.58% of all open reading frames). Thus, a significant number of the genes already sequenced—more than half—appear to be coding for paralogous proteins, and this proportion is even higher when considering only the genes known to have a functional gene product. Interestingly, when we used only the latter, i.e., genes known to be functional, for the ALLALLDB search, we lost only 44 of them, corresponding to those found to match exclusively with an open reading frame. The high proportion, over half of sequences in alignments, is without doubt a minimum figure, since our arbitrary cutoff criteria exclude some well-known examples of proteins believed to share evolutionary ancestry but corresponding to an alignment of less than 100 amino acids. Indeed, there seem to be biologically significant relationships at even lower levels of similarity, comparable to those we detected between far remote members of the same large family. However, such putative supplementary paralogous genes will be added only when we obtain better phylogenetic arguments (see below).

Table 8List of the 971 sequences displaying similarities to at least one other E. coli K-12 chromosomal sequence

This set of 971 paralogous proteins was further analyzed in two complementary ways. (i) We looked at the functional relatedness of the paired proteins, designating each pair as being related, different, or unknown (as in the case of open reading frames or proteins whose cellular function has not been characterized well enough to judge the level of similarity of function). Of the paired 971 proteins, 587 could be related by function to its (best) partner, only 12 were paired with another protein displaying an apparently totally different function, and 336 could not be assessed for lack of information on at least one partner of the pair. The extremely high percentage of similarity of functional relationship among paralogous gene pairs (60.45% of 971, and 98% of the 599 assessable proteins) shows that the sequence relationships between pairs are not accidental but have biological significance. We also used other ways of assessing functional relationships. These are summarized in Table 9. The assignment of the members of the 2,329 pairs to the functional categories reported here in Tables 2 and 3 was examined. Not all members of all pairs had assignments that characterized function, but for those pairs in which both members had been characterized, a large fraction registered as having similar functions (Table 9). Thus, these results strongly suggest that the genes coding for these proteins are paralogous, descendants of duplicate copies of ancestral genes residing in the same genome.

Table 9Functional relationships among sequence-related proteins

(ii) Many of the proteins were found to be related to more than one other E. coli protein and thus are members of groups of interrelated proteins. Besides the 112 pairs (224 sequences), we could distinguish 38 triplets (113 sequences), 41 small groups (281 sequences), and 13 large families (353 sequences). These combinations are listed in Table 10. If each cluster and family were descended from one ancestral gene by duplication and divergence, one could begin to count the numbers of ancestral genes necessary to generate the E. coli genome. This leads to a dramatically small number of putative ancestral sequences. Indeed, the 747 sequences belonging to groups larger than pairs could originate from as few as 92 putative ancestral sequences. This number will undoubtedly fall further as additional genes are sequenced, providing partners for some of the single sequences and amalgamating some of the pairs into families. When the full sequence of the E. coli chromosome is known, we will be able to count the number of unique ancestral sequences required to generate E. coli.

Table 10Families of paralogous genes

To go a step farther in this analysis, we are reconstructing phylogenetic trees for each of the sequence-related groups and then using the putative ancestral sequences to extract other related sequences from databases of sequences. As long as the sequence relationhips among distantly related proteins can be detected, one can continue to move earlier in the tree of descent, relating ancestral sequences for a given species to even earlier ancestral genes that fed many species, thereby progressively reducing the total number of ancestral sequences as one moves in the direction of the begining of the tree. Ultimately, we will be able to approach the identification of a relatively small number of unique primitive ancestral sequences that gave rise to all contemporary genes. E. coli gene sequences will be very useful in this evolutionary context.

MAP RELATIONSHIPS AMONG FUNCTIONALLY RELATED E. COLI GENES

Some 20 years ago, a proposal was put forward that evolution of the E. coli genome might have occurred by successive duplications of the entire genome and that as a consequence, functionally and ancestrally related genes might be located either 90° or 180° from each other on the genetic map (2278, 2279). With many more genes now mapped than were at the time, one can test whether there is a tendency for genes related either by cellular function or by type of protein to cluster at 90° and 180° positions.

When the map positions of genes underlying each functional category as defined in Table 1 were examined, they did not lie at regular positions on the circular map. When map positions of genes for enzymes that catalyze similar reactions were examined, again no pattern of gene location was seen. For instance, phosphotransferase enzymes with an alcohol group as acceptor are enzymes with EC numbers beginning with 2.7.1. They were not clustered at 90° or 180° positions, nor were oxidoreductases acting on the CH-OH group of donors with NAD⁺ or NADP⁺ as the acceptor (EC numbers beginning 1.1.1.). Therefore, the idea of whole genome doubling (745, 1344, 1869, 2278, 2279) does not find support in current E. coli genetic data.

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