Genes Induced Late in Infection Increase Fitness of Vibrio cholerae after Release into the Environment

Schild, Stefan; Tamayo, Rita; Nelson, Eric J.; Qadri, Firdausi; Calderwood, Stephen B.; Camilli, Andrew

doi:10.1016/j.chom.2007.09.004

Cited by 168 publications

(228 citation statements)

References 46 publications

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“…Moreover, focusing on the digestive tract reveals a habitat that is characterized by a sequential exposure to various stimuli. Indeed, previous studies have uncovered examples of a CR strategy both in E. coli (9, 10) and V. cholerae (11).…”

Section: Resultsmentioning

confidence: 99%

“…S1. Now let us consider stress preparation (10)(11)(12)(13)(14)(15)(16)(17). Such environments are characterized by the potential high benefit of preparation (e.g., a 50-fold protection was measured recently in cell survival) (10).…”

Section: Resultsmentioning

confidence: 99%

“…Vibrio cholerae, another species that transits through the digestive tract, was also observed to exhibit an anticipatory response. Specifically, these bacteria were shown to induce genes important for the subsequent life stage outside the host during the late stages of host infection (11).…”

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confidence: 99%

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A mathematical model for adaptive prediction of environmental changes by microorganisms

Mitchell

Pilpel²

2011

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

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Survival in natural habitats selects for microorganisms that are well-adapted to a wide range of conditions. Recent studies revealed that cells evolved innovative response strategies that extend beyond merely sensing a given stimulus and responding to it on encounter. A diversity of microorganisms, including Escherichia coli, Vibrio cholerae, and several yeast species, were shown to use a predictive regulation strategy that uses the appearance of one stimulus as a cue for the likely arrival of a subsequent one. A better understanding of such a predictive strategy requires elucidating the interplay between key biological and environmental forces. Here, we describe a mathematical framework to address this challenge. We base this framework on experimental systems featuring early preparation to either a stress or an exposure to improvement in the growth medium. Our model calculates the fitness advantage originating under each regulation strategy in a given habitat. We conclude that, although a predictive response strategy might by advantageous under some ecologies, its costs might exceed the benefit in others. The combined theoreticalexperimental treatment presented here helps assess the potential of natural ecologies to support a predictive behavior.adaptation | conditioning | evolution M icroorganisms are constantly faced with environmental stimuli and stresses. Over the years, cellular response to such challenges has been intensively studied in several model organisms (1-5). Prevalent response strategies follow a sense and respond logic: cells continuously monitor their environment and induce a cellular response to cope with a stimulus on encounter with it. Although evolution selects for improved sensing and response mechanisms, adaptation can also extend and result in the emergence of more sophisticated response strategies. For example, under stochastic switching, cells randomly alternate between potential cellular states. In a fluctuating environment that is hard to monitor, such a response strategy might ensure that a portion of the population is always prepared for unpredicted challenge (6-8).Here, we focus on environments that are characterized by a stereotypical temporal order of stimuli. Previous theoretical work has suggested that such ecologies may select for organisms that use information about the natural sequence of events (8). Recent studies have revealed examples of such adaptations in model microorganisms. Tagkopoulos et al. (9) investigated the response of Escherichia coli to temperature elevation that is followed shortly after by a drop in oxygen availability on entry of bacteria to the host digestive tract and observed an associative anticipatory regulation pattern-each signal by itself can invoke response to both stimuli. In another study, we have shown that E. coli has adapted to the sequential order of exposure to different sugars along the mammalian digestive tract. Additionally, we have shown that this conditioned response entails the bacteria with fitness advantages when cells are exposed...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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A mathematical model for adaptive prediction of environmental changes by microorganisms

Mitchell

Pilpel²

2011

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

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“…We asked whether weak stress events provide individual cells with increased tolerance against future stress. Memory effects usually have been studied on the basis of population measurements (4,(9)(10)(11)(12). Using population measurements, it is difficult to determine whether history dependence is a consequence of the behavioral changes in individuals or of a shift in the composition of the population as a result of past events.…”

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confidence: 99%

Response of single bacterial cells to stress gives rise to complex history dependence at the population level

Mathis

Ackermann

2016

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

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Most bacteria live in ever-changing environments where periods of stress are common. One fundamental question is whether individual bacterial cells have an increased tolerance to stress if they recently have been exposed to lower levels of the same stressor. To address this question, we worked with the bacterium Caulobacter crescentus and asked whether exposure to a moderate concentration of sodium chloride would affect survival during later exposure to a higher concentration. We found that the effects measured at the population level depended in a surprising and complex way on the time interval between the two exposure events: The effect of the first exposure on survival of the second exposure was positive for some time intervals but negative for others. We hypothesized that the complex pattern of history dependence at the population level was a consequence of the responses of individual cells to sodium chloride that we observed: (i) exposure to moderate concentrations of sodium chloride caused delays in cell division and led to cell-cycle synchronization, and (ii) whether a bacterium would survive subsequent exposure to higher concentrations was dependent on the cell-cycle state. Using computational modeling, we demonstrated that indeed the combination of these two effects could explain the complex patterns of history dependence observed at the population level. Our insight into how the behavior of single cells scales up to processes at the population level provides a perspective on how organisms operate in dynamic environments with fluctuating stress exposure.bacterial memory | single cell | cell cycle | priming | synchronization B acteria are constantly challenged by their environment (1). Are bacterial cells able to respond better to environmental changes if they have experienced similar conditions in the recent past? It has been demonstrated that bacterial populations respond faster to a change of nutrient source when the forthcoming nutrient source has been presented in the recent past (2, 3). Similarly, bacterial populations that were exposed to sublethal stress levels showed increased survival of a higher stress level of the same type (4-6). Theoretical and experimental studies indicate that basing cellular decisions on environmental cues perceived in the past can be advantageous in dynamic environments (3,7,8), suggesting that such history-dependent behavior can be the result of adaptive evolution in dynamic environments.In this study we addressed the question of memory on a singlecell level. We asked whether weak stress events provide individual cells with increased tolerance against future stress. Memory effects usually have been studied on the basis of population measurements (4, 9-12). Using population measurements, it is difficult to determine whether history dependence is a consequence of the behavioral changes in individuals or of a shift in the composition of the population as a result of past events. By using single-cell analysis, we investigated how the behavior of individuals scaled up to hi...

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“…ToxT, the master regulator of virulence, controls population heterogeneity, which results in a small subpopulation of bacteria expressing virulence genes that provide an adaptive benefit if the next environment is a new mammalian host. Concurrently, the majority virulence-off subpopulation is proposed to better adapt to biofilm formation and long-term persistence in the aquatic environment (15,16).…”

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confidence: 99%

Ready or Not: Microbial Adaptive Responses in Dynamic Symbiosis Environments

Cao

Goodrich‐Blair

2017

J Bacteriol

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In mutually beneficial and pathogenic symbiotic associations, microbes must adapt to the host environment for optimal fitness. Both within an individual host and during transmission between hosts, microbes are exposed to temporal and spatial variation in environmental conditions. The phenomenon of phenotypic variation, in which different subpopulations of cells express distinctive and potentially adaptive characteristics, can contribute to microbial adaptation to a lifestyle that includes rapidly changing environments. The environments experienced by a symbiotic microbe during its life history can be erratic or predictable, and each can impact the evolution of adaptive responses. In particular, the predictability of a rhythmic or cyclical series of environments may promote the evolution of signal transduction cascades that allow preadaptive responses to environments that are likely to be encountered in the future, a phenomenon known as adaptive prediction. In this review, we summarize environmental variations known to occur in some well-studied models of symbiosis and how these may contribute to the evolution of microbial population heterogeneity and anticipatory behavior. We provide details about the symbiosis between Xenorhabdus bacteria and Steinernema nematodes as a model to investigate the concept of environmental adaptation and adaptive prediction in a microbial symbiosis.

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Genes Induced Late in Infection Increase Fitness of Vibrio cholerae after Release into the Environment

Cited by 168 publications

References 46 publications

A mathematical model for adaptive prediction of environmental changes by microorganisms

A mathematical model for adaptive prediction of environmental changes by microorganisms

Response of single bacterial cells to stress gives rise to complex history dependence at the population level

Ready or Not: Microbial Adaptive Responses in Dynamic Symbiosis Environments

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