Chemotaxis in bacteria.
12 Aug 1966-Science (American Association for the Advancement of Science)-Vol. 153, Iss: 3737, pp 708-716
TL;DR: These results show that E. coli is chemotactic toward oxygen and energy sources such as galactose, glucose, aspartic acid, threonine, or serine and that chemotaxis allows bacteria to find that environment which provides them with the greatest supply of energy.
Abstract: Motile Escherichia coli placed at one end of a capillary tube containing an energy source and oxygen migrate out into the tube in one or two bands, which are clearly visible to the naked eye and can also be demonstrated by photography, microscopy, and densitometry and by assaying for bacteria throughout the tube. The formation of two bands is not due to heterogeneity among the bacteria, since the bacteria in each band, when reused, will form two more bands. If an anaerobically utilizable energy source such as galactose is present in excess over the oxygen, the first band consumes all the oxygen and a part of the sugar and the second band uses the residual sugar anaerobically. On the other hand, if oxygen is present in excess over the sugar, the first band oxidizes all the sugar and leaves behind unused oxygen, and the second band uses up the residual oxygen to oxidize an endogenous energy source. The essence of the matter is that the bacteria create a gradient of oxygen or of an energy source, and then they move preferentially in the direction of the higher concentration of the chemical. As a consequence, bands of bacteria (or rings of bacteria in the case of agar plates) form and move out. These results show that E. coli is chemotactic toward oxygen and energy sources such as galactose, glucose, aspartic acid, threonine, or serine. The full repertoire of chemotactic responses by E. coli is no doubt greater than this, and a more complete list remains to be compiled. The studies reported here demonstrate that chemotaxis allows bacteria to find that environment which provides them with the greatest supply of energy. It is clearly an advantage for bacteria to be able to carry out chemotaxis, since by this means they can avoid unfavorable conditions and seek optimum surroundings. Finally, it is necessary to acknowledge the pioneering work of Englemann, Pfeffer, and the other late-19thcentury biologists who discovered chemotaxis in bacteria, and to point out that the studies reported here fully confirm the earlier reports of Beijerinck (4) and Sherris and his collaborators (5,6) on a band of bacteria chemotactic toward oxygen. By using a chemically defined medium instead of a complex broth, it has been possible to study this band more closely and to demonstrate in addition the occurrence of a second band of bacteria chemotactic toward an energy source. Beijerinck (4) did, in fact, sometimes observe a second band, but he did not offer an explanation for it.
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TL;DR: Chemotaxis toward amino-acids results from the suppression of directional changes which occur spontaneously in isotropic solutions.
Abstract: Chemotaxis toward amino-acids results from the suppression of directional changes which occur spontaneously in isotropic solutions.
2,069 citations
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TL;DR: The chemotactic response of unicellular microscopic organisms is viewed as analogous to Brownian motion, and a macroscopic flux is derived which is proportional to the chemical gradient.
Abstract: The chemotactic response of unicellular microscopic organisms is viewed as analogous to Brownian motion. Local assessments of chemical concentrations made by individual cells give rise to fluctuations in path. When averaged over many cells, or a long time interval, a macroscopic flux is derived which is proportional to the chemical gradient. By way of illustration, the coefficients appearing in the macroscopic flux equations are calculated for a particular microscopic model.
1,660 citations
Cites background from "Chemotaxis in bacteria."
...For organisms such as flagellated cells which t In the experiments of Adler (1966a), for example, typical concentrations of the critical substrate O2 are of the order of lo-* M....
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...Introduction The chemotactic sensitivity of such one-celled organisms as Escherichia coli (Adler, 1966a,b) and myxamebae (see, e.g. Bonner, 1967) has been well documented, but the ability of an organism of microscopic dimensions to sense and respond to macroscopic chemical gradients has often been…...
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TL;DR: It is demonstrated that E. coli forms biofilms on multiple abiotic surfaces in a nutrient‐dependent fashion and type I pili (harbouring the mannose‐specific adhesin, FimH) are required for initial surface attachment and thatMannose inhibits normal attachment.
Abstract: We have used Escherichia coli as a model system to investigate the initiation of biofilm formation. Here, we demonstrate that E. coli forms biofilms on multiple abiotic surfaces in a nutrient-dependent fashion. In addition, we have isolated insertion mutations that render this organism defective in biofilm formation. One-half of these mutations was found to perturb normal flagellar function. Using defined fli, flh, mot and che alleles, we show that motility, but not chemotaxis, is critical for normal biofilm formation. Microscopic analyses of these mutants suggest that motility is important for both initial interaction with the surface and for movement along the surface. In addition, we present evidence that type I pili (harbouring the mannose-specific adhesin, FimH) are required for initial surface attachment and that mannose inhibits normal attachment. In light of the observations presented here, a working model is discussed that describes the roles of both motility and type I pili in biofilm development.
1,618 citations
Cites methods from "Chemotaxis in bacteria."
...Motility and chemotaxis were analysed using both swarm assays (Adler, 1966; Wolfe and Berg, 1989) and phase-contrast microscopy of living cells. lNK1324 was used for insertion mutagenesis of 2K1056 as previously described (Kleckner et al., 1991)....
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...Motility and chemotaxis were analysed using both swarm assays (Adler, 1966; Wolfe and Berg, 1989) and phase-contrast microscopy of living cells....
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TL;DR: It is argued that the key properties of biochemical networks should be robust in order to ensure their proper functioning, and it is shown that this applies in particular to bacterial chemotaxis.
Abstract: 1 are responsible for many important cellular processes, including cell-cycle regulation and signal transduction. Here we address the issue of the sensitivity of the networks to variations in their biochemical parameters. We propose a mechanism for robust adaptation in simple signal transduction networks. We show that this mechanism applies in particular to bacterial chemotaxis 2-7 . This is demonstrated within a quantitative model which explains, in a unified way, many aspects of chemotaxis, including proper responses to chemical gradients 8-12 . The adaptation property 10,13-16 is a consequence of the network's connectivity and does not require the 'fine-tuning' of parameters. We argue that the key properties of biochemical networks should be robust in order to ensure their proper functioning. Cellular biochemical networks are highly interconnected: a per- turbation in reaction rates or molecular concentrations may affect numerous cellular processes. The complexity of biochemical net- works raises the question of the stability of their functioning. One possibility is that to achieve an appropriate function, the reaction rate constants and the enzymatic concentrations of a network need to be chosen in a very precise manner, and any deviation from the 'fine-tuned' values will ruin the network's performance. Another possibility is that the key properties of biochemical networks are robust; that is, they are relatively insensitive to the precise values of biochemical parameters. Here we explore the issue of robustness of one of the simplest and best-known signal transduction networks: a biochemical network responsible for bacterial chemotaxis. Bacteria such as Escherichia coli are able to sense (temporal) gradients of chemical ligands in their vicinity 2 . The movement of a swimming bacterium is composed of a series of 'smooth runs', interrupted by events of 'tumbling', in which a new direction for the next run is chosen randomly. By modifying the tumbling frequency, a bac- terium is able to direct its motion either towards attractants or away from repellents. A well established feature of chemoxis is its property of adaptation 10,13-16 : the steady-state tumbling frequency in a homogeneous ligand environment is insensitive to the value of ligand concentration. This property allows bacteria to maintain their sensitivity to chemical gradients over a wide range of attractant or repellent concentrations. The different proteins that are involved in chemotactic response have been characterized in great detail, and much is known about the interactions between them (Fig. 1a). In particular, the receptors that sense chemotactic ligands are reversibly methylated. Biochem- ical data indicate that methylation is responsible for the adaptation property: changes in methylation of the receptor can compensate for the effect of ligand on tumbling frequency. Theoretical models proposed in the past assumed that the biochemical parameters are fine-tuned to preserve the same steady-state behaviour at different ligand concentrations 17,18 . We present an alternative picture in which adaptation is a robust property of the chemotaxis network and does not rely on the fine-tuning of parameters. We have analysed a simple two-state model of the chemotaxis network closely related to the one proposed previously 2,19 . The two- state model assumes that the receptor complex has two functional states: active and inactive. The active receptor complex shows a kinase activity: it phosphorylates the response regulator molecules,
1,567 citations
TL;DR: The requirements that define swarming motility in diverse bacterial model systems are reviewed, including an increase in the number of flagella per cell, the secretion of a surfactant to reduce surface tension and allow spreading, and movement in multicellular groups rather than as individuals.
Abstract: How bacteria regulate, assemble and rotate flagella to swim in liquid media is reasonably well understood. Much less is known about how some bacteria use flagella to move over the tops of solid surfaces in a form of movement called swarming. The focus of bacteriology is changing from planktonic to surface environments, and so interest in swarming motility is on the rise. Here, I review the requirements that define swarming motility in diverse bacterial model systems, including an increase in the number of flagella per cell, the secretion of a surfactant to reduce surface tension and allow spreading, and movement in multicellular groups rather than as individuals.
1,159 citations
References
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01 Jan 1940
TL;DR: Professor Szent-Gyorgyi, the Nobel laureate, has played a distinguished part in the development of the present knowledge of cellular oxidation, and his complete grasp of the subject has enabled him to provide in a recent series of lectures a clear and accurate account of the fundamental principles in terms that can be understood by anyone who has even an elementary knowledge of biochemistry.
Abstract: Our knowledge of the enzyme systems which supply energy to the living cell has advanced remarkably during the past few years. Unfortunately the advance has revealed an ever-increasing complexity in these systems, and descriptions of modern ideas on this subject tend to be just as incomprehensible to the non-expert as is a wiring diagram of a modern wireless set to a person ignorant of the laws of electricity. Professor Szent-Gyorgyi, the Nobel laureate, has played a distinguished part in the development of our present knowledge of cellular oxidation, and his complete grasp of the subject has enabled him to provide in a recent series of lectures a clear and accurate account of the fundamental principles in terms that can be understood by anyone who has even an elementary knowledge of biochemistry. He stresses the, fundamental principle that, as regards release of energy, the cell cannot make jumps but has to proceed by small steps. Apparently the sudden release of a large amount of oxidative energy would wreck the cell, and hence oxidation must proceed cautiously. He suggests that the "currency unit" of the cell as regards energy exchange is the liberation of eleven calories per gramme-molecule reacting. This implies a large number of steps in any simple oxidative process. For example, the reaction 2H + 0 = H.O releases sixtyeight calories, and hence the cell has to carry through this change in about six separate steps. The need to maintain control of the rate of energy liberation also implies that the cell can only tise reactions that do not occur spontaneously and are brought about by the special mechanisms possessed by the cell. In addition to these complications the evidence suggests that primitive life was anaerobic and that aerobic mechanisms have been added to more primitive systems. These fundamental conceptions make intelligible the complexity of the cellular enzyme systems, which at first sight appear so irrational. The general conception of the oxidation of a carbohydrate such as glucose is that the chain is split and then the fragments are gradually stripped of hydrogen atoms by a series of dehydrogenases; finally oxidation is carried out by a series of cytochrome oxidases. In the course of these lectures the author gives an interesting account of how he came to discover ascorbic acid. He began with a study of the adrenal cortex, and this led to a consideration of the disorders of pigmentation in Addison's disease. Next the discoloration of the injured tissues of fruits and vegetables was studied and a powerful but unknown inhibitor of this reaction was found to occur in the juice of certain plants. Scientific curiosity caused the author to devote some years of work to this unknown substance, which turned out in the end to be ascorbic acid or vitamin C: "In this way I became a father without wishing it-the father of a vitamin. Such accidents seem to happen even in science." It is of interest to reflect that this accident happened because the author was free to follow his fancy, and would not have occurred if he had been boulnd by the ties of a carefully planned scheme of research. CANCER IN CHILDHOOD
669 citations
TL;DR: A chemically defined growth medium capable of producing motile bacteria was devised and it was found that the presence of glucose or growth above 37° prevented synthesis of flagella.
Abstract: SUMMARY: A simple chemically defined medium for examining the motility of Escherichia coli K12 was designed. The essential components were: (1) a chelating agent to protect the motility against inhibition by traces of heavy metal ions; (2) a buffer to keep the pH value at the optimum between pH 6·0 and 7·5; (3) an energy source to stimulate the motility above that allowed by an endogenous energy source. Oxygen was required unless an energy source was provided which yielded energy anaerobically. A temperature optimum was determined.
A chemically defined growth medium capable of producing motile bacteria was devised. It was found that the presence of glucose or growth above 37° prevented synthesis of flagella.
399 citations
TL;DR: The results are interpreted to mean that E. coli shows chemotaxis toward oxygen and serine, and the only amino acid that this strain can use either aerobically or anaerobically when grown under the conditions used here, gives rise to two bands.
Abstract: Adler, Julius (University of Wisconsin, Madison). Effect of amino acids and oxygen on chemotaxis in Escherichia coli. J. Bacteriol. 92:121-129. 1966.-Motile cells of Escherichia coli placed at one end of a capillary tube containing a mixture of the 20 amino acids commonly found in proteins migrate out into the tube in two bands. The bands are clearly visible to the naked eye, and they can also be demonstrated by microscopy, photography, and densitometry, and by assaying for bacteria throughout the tube. The occurrence of more than one band is not due to heterogeneity among the bacteria, since each band can be used over to give rise to two again. The first band uses all the oxygen to oxidize portions of one or more of the amino acids, including serine, and the second band consumes the residual serine anaerobically. The results are interpreted to mean that E. coli shows chemotaxis toward oxygen and serine. When no energy source is added to the medium, a band of bacteria still appears. It consumes all the oxygen to oxidize an endogenous energy source. The addition of any one of 10 oxidizable amino acids stimulates the rate of travel of this band. Alanine, an example that was studied in detail, supports such a band that consumes all the oxygen to oxidize a portion of the alanine. Serine, the only amino acid that this strain can use either aerobically or anaerobically when grown under the conditions used here, gives rise to two bands.
110 citations
TL;DR: The central concept of this paper is that of a line (adj. linear or unilinear) which signifies a single, unbranched, finite or infinite chain of descent
Abstract: mutation or segregation may intervene, but further descendants will again follow this rule of clonal heredity, which is the corollary of equal division. But other rules of inheritance are known-for example, the entailment of estates in land and the traditional law of primogeniture in titles of nobility-whereby a legacy must pass undivided through a single line of descent through the generations. This paper will have to do with biological analogies of linear inheritance which have appeared in experiments on the transduction of motility-genes in Salmonella. Transduction is a mechanism of genetic recombination which is notable for the transfer of hereditary fragments from one cell to another (SYMPOSIUM 1955, LEDERBERG 1956a). In these experiments, a temperate bacteriophage serves as vector for the fragments, which are furnished by the disruption of the chromosomes of a bacterial host as it supports the growth of the phage. When this crop of phage is applied to cells of a suitably marked recipient strain, some (1W6) of these cells yield a transformed clone which carries a given marker from the donor. In previous studies, the transformed clones have exhibited the same genotypic stability as did the parents. However, the selective methods which were used to isolate the rare recombinants would overlook transductional effects that did not yield substantial clones of the new types. These studies included auxotrophic, fermentative, resistance, serological and motility markers, and each one for which a suitable selective technique was available was subject to transduction in much the same fashion. The following experiments are a follow-up of observations on “motility trails” (see paragraph 1. 1) initiated by DR. BRUCE STOCKER during a research visit to this laboratory (STOCKER, ZINDER and LEDERBERG 1953). After his return to England, DR. STOCKER began microscopic studies on these trails; the immediate concern here was the problem of segregation and crossing over in transductional clones. However, the two studies proved to be operationally inseparable. I am indebted to DR. STOCKER for an unreserved exchange of materials, information and manuscript drafts throughout these studies. In the main, the terminology also follows his suggestions. A concordance of my results and interpretations with his (STOCKER 1956b) is given a t the close of this paper. Glossary and symbols. The central concept of this paper is that of a line (adj. linear or unilinear) which signifies a single, unbranched, finite or infinite chain of descent
81 citations
67 citations