Mutant Selections Linking Physiology, Inhibitors, and Genotypes

TOC

Chapter 139

ROBERT A. LaROSSA

OVERVIEW

Inhibitory conditions result in the selection of genetic variants. Such variants have been useful as selectable markers facilitating studies of rare genetic events such as recombination and mutagenesis (619). Many such selections have also defined the sites of agrichemical and drug action. These inhibitory agents, resultant selections, and mutants have been crucial probes allowing insights into the broad range of biological mechanisms occurring in bacteria. Studies of surface phenomena, transport, central and peripheral metabolic events, transcription, translation, specific and global regulatory mechanisms, protein folding, and replication have been advanced by such analyses. The aim of this chapter is to provide a catalog of such inhibitory agents and their targets. It is my belief that such a catalog provides an important connection between the genome and the physiology of an organism.

SELECTIONS AND SCREENS

Chemical, physical, and biological insults can be applied to Escherichia coli and Salmonella typhimurium (official designation, Salmonella enterica serovar Typhimurium). The response of a bacterial strain, i.e., its phenotype, is a complex function of the organism’s genetic constitution, or genotype, its natural history, and its current environment. Conditions allowing all but a few cells to grow result in selections of genetic variants that overcome the environmental challenges. In other cases, rare mutants unable to grow under conditions in which the vast majority of organisms thrive can be obtained by screening. The analysis of both mutational classes can be most revealing; thorough study often rewards the dedicated researcher with fundamental new insights into biological phenomena.

SOME TOOLS OF THE TRADE

Environment

To devise a selection or a screen, the experimenter customizes the microbial environment. This customization may encompass manipulation of nutritional parameters and physical conditions such as temperature, pressure, and irradiation. Such manipulations by themselves can constitute positive selections or effective screens. These manipulations can also be utilized in conjunction with inhibitory agents to optimize selection or screening protocols.

Mutagenesis

Mutagenesis protocols can influence both the recovery of mutants and the spectrum of mutations obtained. It is thus useful to employ a variety of mutagens with a defined selection. For example, spontaneous hydrogen peroxide-resistant mutants have not been obtained from S. typhimurium despite repeated attempts with a tight and powerful selection; such mutants are recovered readily after chemical mutagenesis (131). Moreover, various protocols can lead to the preponderance of different mutational classes. Many chemical treatments yield point mutations, while spontaneous mutations are often small deletions (460). Transposon mutagenesis most often results in loss of gene function (411). In addition, the high efficiency (=1) of recovering mutations by selection for drug resistance after exposure to transposons such as Tn5, Tn10, and Mud (Ap lac) facilitates selection of mutants resistant to a second agent and makes the screening for hypersensitive loss-of-function mutants manageable (411, 443, 796).

Inhibitory Agents

Energy, chemicals, and living things have the capacity to either inhibit bacterial growth or kill cells. Energy in many forms, including heat, visible light, UV rays, and gamma rays, can compromise cells. Chemical inhibitors may be elements, simple inorganic molecules, complex organic molecules, or natural products produced by an organism for a variety of reasons, including protection of its ecological niche or repelling of predators. A rich collection of antibacterial agents has arisen from the synthetic organic chemical practices of the modern pharmaceutical and agrichemical industries, the natural product isolation and screening of the pharmaceutical industry, and the development of novel compounds for a variety of uses by the chemical industry. Bacterial viruses, mammalian macrophages, and other microbes are also capable of efficient destruction of bacterial populations. These tools have been repeatedly exploited by bacterial geneticists to provide both fundamental and applied knowledge.

Modern Genetic Technologies

A wide variety of genetic methods are applicable to the characterization of selectable phenotypes. A few of general utility are mentioned here. Transposon-mediated insertion mutations that are linked to alleles conferring resistance or sensitivity or that are themselves responsible for the phenotype (411, 443, 796) can be physically isolated by using drug resistance as a selectable marker in in vivo or in vitro molecular cloning experiments (524). Such DNA fragments can be mapped accurately to the E. coli genome by powerful computer-assisted restriction digest matching and hybridization methodologies (414, 661). Multicopy plasmid libraries representative of the E. coli and S. typhimurium genomes are easy to construct. These libraries can be used to isolate resistant or hypersensitive variants that result from the amplification of small regions of the chromosome (see, e.g., reference 250 and 472). Again, such "meromultiploids" can be rapidly and accurately mapped by computer-assisted restriction enzyme digestion analyses or by hybridization to the ordered library of E. coli fragments present in phage lambda vectors (414, 661).

PATHWAY FOR INHIBITOR ACTION

To inhibit the growth of E. coli or S. typhimurium, a generic inhibitor must pass through the aqueous culture medium and one or both of the cellular membranes. Within the cytoplasm, periplasm, or cellular membranes, the inhibitory substance must compromise a vital cellular function. The response to the inhibitory substance may be modulated by altering (i) the efficiency with which it reaches its target, (ii) the target structure, (iii) the target quantity, (iv) the catabolism of the inhibitory substance, (v) the metabolic responses to target inhibition, or (vi) the functional alternatives to the inhibited target. Thus, inhibitor hypersensitivity (Fig. 1) can arise from (i) lessening of permeability barriers or efflux mechanisms (e.g., tolC [536, 653]), (ii) creation of targets with a greater affinity for the inhibitor (hisG [698]), (iii) decreased intracellular levels of targets (e.g., his promoter down-mutations [208]), (iv) increased conversion of a proinhibitor to an inhibitor, (v) destruction of inhibitor detoxification systems (e.g., inactivation of neomycin phosphotransferase) or inactivation of fueling pathways (e.g., pta-ack) that can degrade otherwise toxic products to more benign substances (see, e.g., reference 797), and (vi) destruction of isozymes (see, e.g., reference 442). Conversely, resistance (Fig. 2) can arise by (i) preventing binding or permeation of molecules or organisms (e.g., phage λ [88, 134, 135, 253, 644, 766], colicin E1 [449, 536, 653], and histidine analogs [13, 14, 15]), (ii) creating target structures with lowered affinities for an inhibitor (781; e.g., hisG [540, 698, 699, 824]), (iii) elevating target levels (781; e.g., hisO, hisR, hisS, hisT, hisU, and hisW [23, 98, 126, 148, 657, 658, 660, 705, 706, 784]), (iv) transforming an inhibitor to an inactive form or preventing proinhibitor transformation to a toxic form (e.g., fluoroacetate to fluorocitrate [96, 281, 463, 797] and glycylvaline to valine [1, 178]), (v) obviating deleterious accumulations behind the block imposed by either a mutation or an inhibitor, and (vi) evolving cryptic enzyme activities (e.g., ebg [118] and ilvF [174, 610]).

Fig. 1Some causes of inhibitor-hypersensitive mutants. Consider a cell in which enzyme U catalyzes the conversion of substrated to product e. The relative amounts of d and e are indicated by whether the symbol is an uppercase or lowercase letter (larger and smaller amounts, respectively). The inhibitor of enzyme U can be in the extracellular space (Ke) or internalized within the Cell (Ki). Within the cytoplasm, the inhibitor can bind to its target or be catabolized by a second protein, C, to metabolites m and n. Substrate d may be consumed by either enzyme U, an isozyme V, or another enzyme, R, yielding an alternative product, f. Inhibitor-hyper-sensitive mutants can arise by Ii) mutations that increase entry of the inhibitor into the cell, (ii) structural alterations of target enzyme U that result in increased affinity for the inhibitor, (iii) regulatory mutations that lower the concentration of enzyme U, (iv) alleles that prevent catabolism of inhibitor K by protein C, (v) mutations that cause the accumulation of metabolic intermediates to toxic levels, or (vi) loss-function mutations that inactivate inhibitor-resistant isozymes of enzyme U.

Source:

Fig. 2Some mechanisms underlying inhibitor-resistant mutants. A cell in which enzyme T catalyzes the conversion of substrate a to product b is depicted. The relative amounts of a and b are indicated by whether the symbol is an uppercase or lowercase letter (larger and smaller amounts, respectively). The inhibitor of enzyme T can be in the extracellular space (Ie) or internalized within the cell (I1). Within the cytoplasm, the inhibitor can bind to its target or be catabolized by a second protein, C, to metabolites m and n. Substrate a may be consumed by enzyme T, an isozyme Z, or another enzyme, R, yielding an alternative product, j. Resistance can arise by (i) exclusion of inhibitor I from the cellular compartment containing enzyme T, (ii) structural alterations of enzyme T such that its affinity for inhibitor I is diminished. (iii) regulatory mutations increasing the intracellular concentration of enzyme T, (iv) mutations that cause the catabolism of inhibitor I, (v) alleles that prevent the accumulation of substrate a to toxic levels, and (vi) evolution of cryptic isozymes of enzyme T, the target of inhibitor I, that are unaffected by the inhibitor.

Source:

ALTERING METABOLIC CAPACITY

E. coli and S. typhimurium utilize a large, though limited, number of organic compounds as sole sources of carbon, nitrogen, phosphorus, sulfur, and energy. Positive genetic selections that expand the metabolic repertoire of these organisms have been devised. These include the utilization of d-amino acids for protein synthesis, utilization of a single amino acid as a sole nitrogen or carbon source, utilization of organophosphates as a sole phosphorus source, utilization of djenkoic acid as a sole sulfur source, and utilization of many carbon compounds as energy sources. Although single mutations can expand metabolic capacity, mutation of several genes may be required to satisfy these selections.

An interesting twist on expanding metabolic capacity comes from gene amplification. In this regard, a discussion of the multiple transaminsases is illuminating. These enzymes have overlapping specificities in vitro. Amplification of ilvE, which encodes the branched-chain amino acid transaminase B, allows production of physiologically significant levels of tyrosine, which are not obtained with the haploid ilvE gene. Similarly, amplification of tyrB allows transaminase B to act in alanine synthesis, while overproduction of transaminase A or C is sufficient to meet the metabolic demand for leucine in an ilvE mutant. Thus, function may be modulated by changing enzyme concentrations in vivo via alteration of gene dosage or expression (61).

Loss of metabolic capacity can also be detected. Many positive selections for loss of function are known. Indirect screening methods (replica plating, indicator media) allow identification of interesting phenotypes. One such indirect method, hypersensitivity to a herbicide, has been useful in metabolic studies (443) and has led to the development of a new selection for ilvA alleles (231). Moreover, the indirect method has been extremely powerful in defining the responses of cells to DNA-damaging regimens (810).

LESSONS AND IMPACTS

Resistance-determining alleles have been exploited in several ways. They have served as selectable markers in genetic crosses. This utility is being supplanted by new techniques and use of drug resistance-specifying insertion alleles in strain construction. Nevertheless, a lasting legacy of these selections has been the definition of a very broad range of biological phenomena that have been intensively studied. A few examples illustrating this generality in conjunction with Fig. 2 may be illuminating.

Alleles preventing association of an inhibitory agent with the cell (Fig. 2, part i) have contributed much to our present understanding of surface architecture and membrane transport systems. Mutations that decrease inhibitor-target interactions (Fig. 2, part ii) have advanced our knowledge of antibiotic and agrichemical action, allostery, feedback inhibition, and repression. Mutations that increase the intracellular concentration of a target macromolecule (Fig. 2, part iii) have led directly to the genetic regulatory concepts of attenuation, repression, and activation.

Interference with inhibitor metabolism (Fig. 2, part iv) has led to findings both obvious and surprising. It is understood that fluoroacetate is a poison only if it enters the tricarboxylic acid cycle. Thus, mutations preventing the formation of fluoroacetyl coenzyme A are expected to confer resistance to fluoroacetate; such mutations have been obtained (96, 281, 463, 797). In contrast, if multiple phages are used as the inhibitory agents, bacterial Gro mutants both blocked in phage killing and defective in cellular metabolism are selected (256, 257, 258, 259, 260). It is worth emphasizing that this latter approach has had a profound effect on our understanding of protein folding, the cellular redox state, and transcription.

Preventing substrate accumulation (Fig. 2, part v) has been the basis of selections that have helped demonstrate that accumulations of sugar phosphates and 2-ketoacids are toxic (569, 752, 796, 797). These same selections are being used in the detailed dissection of protein structure-function and fine-structure genetic mapping (231). The recruitment of alternative functions (Fig. 2, part vi) has intriguing evolutionary implications. Selections have uncovered silent, cryptic genes that are activated by mutation (see, e.g., references 118, 174, 361, and 610). Further analyses have indicated that a gene encoding one isozyme may be cryptic in E. coli and expressed in S. typhimurium, while the gene encoding the second isozyme is silent in S. typhimurium and functional in E. coli (782). Moreover, studies of evolved β-galactosidase and transaminases together indicate that a new in vivo function to meet a selection can be accomplished by changes in enzyme structure or changes in enzyme quantity or both (61, 118).

Analyses of hypersensitive and resistant alleles that use a single inhibitory agent can be most informative in the study of a single phenomenon. Analysis of mutations altered in both responses to an amino acid antagonist has defined the multiple components of the yeast general control system (841). Similarly, extensive genetic, physiological, and enzymatic studies of feedback-hypersensitive and feedback-resistant alleles of hisG have been most useful in understanding the role of the hisG gene product (698, 824). Several other such examples are well known.

An interesting contrast is provided by studies of sulfonylurea herbicide resistance and hypersensitivity in S. typhimurium. Resistance mutations precisely define acetolactate synthase as the site of action of these herbicides (441). Numerous transposon-induced, herbicide-hypersensitive mutations have also been collected (796). Studies of these mutations demonstrated that the accumulation of 2-ketobutyrate upon acetolactate synthase inhibition is toxic (443). This observation suggests that such toxic accumulation may be an important factor in herbicide target selection and that schemes can be conceived in which selections and screens may be used to mimic inborn errors of human metabolism (444).

These positive selections have also had direct economic and clinical impact. The sites of action of vital pharmaceutical and agrichemical agents have been and continue to be defined by mutant analyses of E. coli and S. typhimurium. Feedback-insensitive mutations of E. coli, S. typhimurium, and other bacteria play a critical role in pathway engineering designed to produce small biological molecules by schemes involving fermentation or agriculture.

LIMITATIONS OF INHIBITOR AND MUTANT ANALYSES

Mutations often cause an adverse situation in which cellular growth is not optimal. Even under permissive conditions, compensatory secondary mutations may accumulate. Conclusions attributing a phenotype to a mutation may be erroneous if that phenotype is actually a consequence of both the primary mutation and compensatory alterations. Hypotheses drawn from mutants can often be buttressed by analyzing growth disadvantages created by the addition of very specific chemical inhibitors of particular enzymes. In such cases, the time for selection and expression of compensatory mutations is minimized. Analysis of such transient phenocopies is, however, complicated; inhibitor specificity may not be absolute. For example, various oxayl hydroxamates inhibit both isopropyl malate dehydrogenase (the leuB product) and acetohydroxy acid isomeroreductase (the ilvC product [839]). Thus, mutually supportive physiological and genetic data derived from a single inhibitory condition are most desirable.

TABLES

Tables 1 through 3 build upon the splendid effort of Vinopal (803). Table 1 provides a list of selections by which mutations have been obtained. It is apparent that a single selection can often yield mutations in a wide variety of genes. Table 2 (p. 2551), cross-referencing Table 1, lists alphabetically those genes for which resistant alleles have been obtained by positive selections. From this table, one can see that alleles of single genes can often be obtained by a variety of selections. It is often useful to have access to a range of inhibitors interfering with a class of metabolic reactions. To address this need, the genes listed in Tables 1 and 2 are regrouped in Table 3 (p.2571) by metabolic function following the convention of Riley (643). As can be seen, selections for a broad spectrum of metabolic functions have been devised. For genes in the amino acid and cofactor biosynthesis domain, selections based on mechanisms other than false feedback inhibition are relatively few. By providing these three tables, I hope to provide maximal access to the contents of this chapter for geneticists, biochemists, and physiologists. An array of inhibitory agents with different specificities is therefore presented. As in the past, the utility of these tools for scientific investigation is limited only by the imagination of the experimenter.

Table 1-01Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-02Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-03Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-04Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-05Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-06Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-07Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-08Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-09Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-10Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-11Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-12Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-13Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-14Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-15Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-16Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-17Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-18Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 1-19Selections giving rise to mutants of E.coli and S.typhimuriuma

Table 2-01Genes for which selections exist in E.coli and S. typhimurium

Table 2-02Genes for which selections exist in E.coli and S. typhimurium

Table 2-03Genes for which selections exist in E.coli and S. typhimurium

Table 2-04Genes for which selections exist in E.coli and S. typhimurium

Table 2-05Genes for which selections exist in E.coli and S. typhimurium

Table 2-06Genes for which selections exist in E.coli and S. typhimurium

Table 2-07Genes for which selections exist in E.coli and S. typhimurium

Table 2-08Genes for which selections exist in E.coli and S. typhimurium

Table 2-09Genes for which selections exist in E.coli and S. typhimurium

Table 2-10Genes for which selections exist in E.coli and S. typhimurium

Table 2-11Genes for which selections exist in E.coli and S. typhimurium

Table 2-12Genes for which selections exist in E.coli and S. typhimurium

Table 2-13Genes for which selections exist in E.coli and S. typhimurium

Table 2-14Genes for which selections exist in E.coli and S. typhimurium

Table 2-15Genes for which selections exist in E.coli and S. typhimurium

Table 2-16Genes for which selections exist in E.coli and S. typhimurium

Table 2-17Genes for which selections exist in E.coli and S. typhimurium

Table 2-18Genes for which selections exist in E.coli and S. typhimurium

Table 2-19Genes for which selections exist in E.coli and S. typhimurium

Table 2-20Genes for which selections exist in E.coli and S. typhimurium

Table 2-21Genes for which selections exist in E.coli and S. typhimurium

Table 2-22Genes for which selections exist in E.coli and S. typhimurium

Table 3Selectable genes grouped by metabolic functiona

A cautionary note is in order. I hope that the cross-referenced tables emphasize that, unlike the one-to-one correspondence between gene and gene product, the relationship between phenotype and genotype is more complicated. Many different genotypes can give rise to a single phenotype. Similarly, many different selections can alter a single gene.

FUTURE DIRECTIONS

Inhibitory conditions will continue to be important genetic tools with which to probe E. coli and S. typhimurium physiology. The study of mutants hypersensitive to environmental insults, alluded to earlier, is a most fertile area for exploitation. In addition, bacteriophage-resistant mutations have recently been of prime importance in defining pathway-assisted protein folding in the cell (531). Vigorous investigation of several such ill-defined mutants may reveal other new challenges to our orthodoxies. Relatively few natural product inhibitors of essential amino acid and cofactor biosynthetic pathways are identified (Table 1). Searches for such products and molecular biological definition of their modes of action may contribute both to our understanding of the establishment of microbial niches and to the development of a bioagrichemical industry akin to the antibiotic industry. These possibilities, and several others, portend an integrative understanding of biology emanating from the continued detailed study of the selectable phenotypes in E. coli and S. typhimurium.

ACKNOWLEDGMENTS

I thank past and present members of the DuPont Microbial Genetics laboratory for their patience as I labored on this chapter. Dana Smulski of DuPont helped to ensure the accuracy of the references. I am grateful to Carol Perrotto of DuPont for her conduct of computerized literature searches. My training in the laboratories of Phil Hartman, Dieter Söll, Brooks Low, and Dale Kaiser convinced me that judicious genetic analysis of inhibitor action is a field worthy of extended study. R. T. Vinopal’s compilation of selectable phenotypes was an invaluable starting point for this effort.

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