Is Escherichia coli growing in glucose-limited chemostat culture able to utilize other sugars without lag?

Lendenmann, Urs; Egli, Thomas

doi:10.1099/00221287-141-1-71

Cited by 63 publications

(48 citation statements)

References 28 publications

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“…Experimentally, this can be realised in chemostats where glucose concentrations can be kept fixed. Sufficiently low concentrations of glucose then allow co-utilisation of glucose and lactose (Lendenmann et al, 1996;Lendenmann and Egli, 1995), consistent with the prediction of our model.…”

Section: Limitations To the Modelsupporting

confidence: 75%

Limited by sensing - A minimal stochastic model of the lag-phase during diauxic growth

Chu

2017

Journal of Theoretical Biology

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Many microbes when grown on a mixture of two carbon sources utilise first and exclusively the preferred sugar, before switching to the less preferred carbon source. This results in two distinct exponential growth phases, often interrupted by a lag-phase of reduced growth termed the lag-phase. While the lag-phase appears to be an evolved feature, it is not clear what drives its evolution, as it comes with a substantial up-front fitness penalty due to lost growth. In this article a minimal mathematical model based on a master-equation approach is proposed. This model can explain many empirically observed phenomena. It suggests that the lag-phase can be understood as a manifestation of the trade-off between switching speed and switching efficiency. Moreover, the model predicts heterogeneity of the population during the lag-phase. Finally, it is shown that the switch from one carbon source to another one is a sensing problem and the lag-phase is a manifestation of known fundamental limitations of biological sensors.

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Section: Limitations To the Modelsupporting

confidence: 75%

Limited by sensing - A minimal stochastic model of the lag-phase during diauxic growth

Chu

2017

Journal of Theoretical Biology

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“…Thus the mammalian intestine can be thought of as a chemostat in which several hundred species of bacteria are in equilibrium, competing for resources from a mixture of limiting nutrients (6,39). The chemostat allows for simultaneous utilization of several limiting nutrients by an individual species (40). It remains to be established whether this observation extends to in vivo nutrient utilization by E. coli.…”

Section: Discussionmentioning

confidence: 99%

Carbon nutrition of Escherichia coli in the mouse intestine

Chang

Smalley

Tucker

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

469

452

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Whole-genome expression profiling revealed Escherichia coli MG1655 genes induced by growth on mucus, conditions designed to mimic nutrient availability in the mammalian intestine. Most were nutritional genes corresponding to catabolic pathways for nutrients found in mucus. We knocked out several pathways and tested the relative fitness of the mutants for colonization of the mouse intestine in competition with their wild-type parent. We found that only mutations in sugar pathways affected colonization, not phospholipid and amino acid catabolism, not gluconeogenesis, not the tricarboxylic acid cycle, and not the pentose phosphate pathway. Gluconate appeared to be a major carbon source used by E. coli MG1655 to colonize, having an impact on both the initiation and maintenance stages. N-acetylglucosamine and N-acetylneuraminic acid appeared to be involved in initiation, but not maintenance. Glucuronate, mannose, fucose, and ribose appeared to be involved in maintenance, but not initiation. The in vitro order of preference for these seven sugars paralleled the relative impact of the corresponding metabolic lesions on colonization: gluconate > N-acetylglucosamine > N-acetylneuraminic acid ‫؍‬ glucuronate > mannose > fucose > ribose. The results of this systematic analysis of nutrients used by E. coli MG1655 to colonize the mouse intestine are intriguing in light of the nutrientniche hypothesis, which states that the ecological niches within the intestine are defined by nutrient availability. Because humans are presumably colonized with different commensal strains, differences in nutrient availability may provide an open niche for infecting E. coli pathogens in some individuals and a barrier to infection in others.

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“…Other methods, such as growth in batch culture or in chemostats containing defined mixtures of reduced carbon compounds, do not approximate spermosphere nutritional conditions (8,(11)(12)(13)16). We used the sterile sand system to demonstrate that the mutation in pfkA decreases the growth rate of E. cloacae during colonization of the spermospheres of certain seeds.…”

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confidence: 99%

Importance of pfkA for Rapid Growth of Enterobacter cloacae during Colonization of Crop Seeds

Roberts

Déry

Yucel

et al. 2000

Appl Environ Microbiol

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Enterobacter cloacae A-11 is a prototrophic, glycolytic mutant of strain 501R3 with a single transposon insertion in pfkA. The populations of strain A-11 on cucumber and radish seeds were smaller than the populations of strain 501R3 in natural soil, but the populations of these two strains on pea, soybean, sunflower, and sweet corn seeds were similar (D. P. Roberts, P. D. Dery, I. Yucel, J. Buyer, M. A. Holtman, and D. Y. Kobayashi, Appl. Environ. Microbiol. 65:2513-2519, 1999). The net effect of the mutation in pfkA in vitro was a shift from rapid growth on certain carbohydrates detected in seed exudates to much slower growth on other carbohydrates, amino acids, and organic acids. The impact of the mutation in pfkA was greatest on the growth rate of E. cloacae on the seeds that released the smallest quantities of fructose, other carbohydrates, and amino acids. Corn, pea, soybean, and sunflower seeds released total amounts of carbohydrates and amino acids at rates that were approximately 10-to 100-fold greater than the rates observed with cucumber and radish seeds for the first 24 h after inhibition began. The growth rate of strain A-11 was significantly less (50% less) than the growth rate of strain 501R3 on radish seeds, and the growth rate of strain A-11 was too low to estimate on cucumber seeds in sterile sand for the first 24 h after inhibition began. The growth rate of strain A-11 was also significantly lower on soybean seeds, but it was only 17% lower than the growth rate of strain 501R3. The growth rates of strains 501R3 and A-11 were similar on pea, sunflower, and corn seeds in sterile sand for the first 30 h after imbibition began. Large reductions in the growth rates of strain A-11 on seeds were correlated with subsequent decreased levels of colonization of seeds compared to the levels of colonization of strain 501R3. The strain A-11 populations were significantly smaller than the strain 501R3 populations only on radish and cucumber seeds. The mutation in pfkA appears to decrease the level of colonization by E. cloacae for seeds that release small quantities of reduced carbon compounds by decreasing the size of the pool of compounds that support rapid growth by this bacterium.Colonization of the subterranean portions of plants by bacteria can be an essential process when these organisms are used for beneficial purposes, such as plant growth promotion, plant disease control, and bioremediation (2, 3, 5). Several traits, including motility, chemotaxis, salt tolerance, binding to roots, and the production of the O-antigenic side chain of lipopolysaccharide, have been correlated with the colonization of plant surfaces (1,6,7,9,10,21). It has also been established that microbial growth is an essential process for colonization (20, 22-26, 28, 29). The complex mixtures of carbohydrates, amino acids, organic acids, and other nutrients (4) released from seeds and roots are thought to support the growth of beneficial bacteria in the spermosphere and rhizosphere. We have used a mutational approach to study the r...

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Is Escherichia coli growing in glucose-limited chemostat culture able to utilize other sugars without lag?

Cited by 63 publications

References 28 publications

Limited by sensing - A minimal stochastic model of the lag-phase during diauxic growth

Limited by sensing - A minimal stochastic model of the lag-phase during diauxic growth

Carbon nutrition of Escherichia coli in the mouse intestine

Importance of pfkA for Rapid Growth of Enterobacter cloacae during Colonization of Crop Seeds

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