Bacterial Osmoregulation: A Paradigm for the Study of Cellular Homeostasis

Wood, Janet M.

doi:10.1146/annurev-micro-090110-102815

Cited by 260 publications

(344 citation statements)

References 129 publications

(247 reference statements)

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“…These results reveal differences in how past events can modulate the behavior of individuals and groups of bacteria. medium, to counteract the loss of water (18,19). Sodium chloride has been used in other studies to characterize specific stress responses of C. crescentus (20)(21)(22).…”

Section: Significancementioning

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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Section: Significancementioning

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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“…Glycine betaine (GB) is an important osmoprotectant for many species in all domains of life (17,18,20). The widespread use of GB has been explained, in part, by the superior osmoprotection offered by GB as a compatible solute for many organisms (21).…”

Section: Distribution and Biological Roles Of Choline And Gbmentioning

confidence: 99%

“…While these transporters are transcriptionally induced by osmostress (reviewed in reference 44), the rapid initial uptake is not dependent on de novo transcription. This section of the review focuses only on transport regulation by the osmolytes themselves, which occurs after the initial osmostress response and under nonstress conditions, and I refrain from review of sensing osmolarity and cell envelope stress, which has been well reviewed elsewhere (18,49,50). Choline and GB transporters in P. aeruginosa can be regulated at the transcriptional level (48).…”

Section: Choline and Gb Import Versus De Novo Synthesismentioning

confidence: 99%

“…To protect cell function and turgor under conditions that include any of these osmotic insults, osmoprotectants (also called compatible solutes) are imported or synthesized and accumulate in the cytosol (reviewed in references 17 and 18). Their import, export, and synthesis are tightly regulated, and most environmental bacteria can make use of diverse compatible solutes, including glycine betaine (GB), carnitine, choline-O-sulfate, dimethylsulfoniopropionate (DMSP), proline, stachydrine, taurine, ectoine, mannitol, trehalose, and N-acetylglutaminylglutamine amide (NAGGN) (18). The ability of bacteria to accumulate or synthesize these osmoprotectants is likely important for their survival and competition in any environment where the external osmolarity is not constant and relatively isotonic.…”

mentioning

confidence: 99%

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Homeostasis and Catabolism of Choline and Glycine Betaine: Lessons from Pseudomonas aeruginosa

Wargo

2013

Appl Environ Microbiol

155

121

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Most sequenced bacteria possess mechanisms to import choline and glycine betaine (GB) into the cytoplasm. The primary role of choline in bacteria appears to be as the precursor to GB, and GB is thought to primarily act as a potent osmoprotectant. Choline and GB may play accessory roles in shaping microbial communities, based on their limited availability and ability to enhance survival under stress conditions. Choline and GB enrichment near eukaryotes suggests a role in the chemical relationships between these two kingdoms, and some of these interactions have been experimentally demonstrated. While many bacteria can convert choline to GB for osmoprotection, a variety of soil-and water-dwelling bacteria have catabolic pathways for the multistep conversion of choline, via GB, to glycine and can thereby use choline and GB as sole sources of carbon and nitrogen. In these choline catabolizers, the GB intermediate represents a metabolic decision point to determine whether GB is catabolized or stored as an osmo-and stress protectant. This minireview focuses on this decision point in Pseudomonas aeruginosa, which aerobically catabolizes choline and can use GB as an osmoprotectant and a nutrient source. P. aeruginosa is an experimentally tractable and ecologically relevant model to study the regulatory pathways controlling choline and GB homeostasis in choline-catabolizing bacteria. The study of P. aeruginosa associations with eukaryotes and other bacteria also makes this a powerful model to study the impact of choline and GB, and their associated regulatory and catabolic pathways, on host-microbe and microbe-microbe relationships.

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“…The regulation of intracellular osmolality by transport or biosynthesis of compatible solutes is believed to be the principal osmoprotection response in the gram-negative bacterium Escherichia coli 6 that can be mediated by several molecular mechanisms. First, E. coli controls in-and outflux of water and other small molecules by activation of aquaporins as an immediate response to sudden changes in osmotic pressure 7 .…”

Section: Introductionmentioning

confidence: 99%

Ubiquinone accumulation improves osmotic-stress tolerance in Escherichia coli

2014

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Bacteria are thought to cope with fluctuating environmental solute concentrations primarily by adjusting the osmolality of their cytoplasm. To obtain insights into underlying metabolic adaptions, we analyzed the global metabolic response of Escherichia coli to sustained hyperosmotic stress using non-targeted mass spectrometry. We observed that 52% of 1,071 detected metabolites, including known osmoprotectants, changed abundance with increasing salt challenge. Unexpectedly, unsupervised data analysis revealed a substantial increase of most intermediates in the ubiquinone-8 (Q8) biosynthesis pathway and a 110-fold accumulation of Q8 itself, as confirmed by quantitative lipidomics. We then demonstrate that Q8 is necessary for acute and sustained osmotic stress tolerance using Q8 mutants and tolerance rescue through feeding non-respiratory Q8 analogues. Finally, in vitro experiments with artificial liposomes reveal mechanical membrane stabilization as a principal mechanism of Q8-mediated osmoprotection. Thus, we find that besides regulating intracellular osmolality, E. coli enhances its cytoplasmic membrane stability to withstand osmotic stress. AbstractBacteria are thought to cope with fluctuating environmental solute concentrations primarily by adjusting the osmolality of their cytoplasm. To obtain insights into underlying metabolic adaptions, we analyzed the global metabolic response of Escherichia coli to sustained hyperosmotic stress using non-targeted mass spectrometry. We observed that 52% of 1,071 detected metabolites, including known osmoprotectants, changed abundance with increasing salt challenge. Unexpectedly, unsupervised data analysis revealed a substantial increase of most intermediates in the ubiquinone-8 (Q8) biosynthesis pathway and a 110-fold accumulation of Q8 itself, as confirmed by quantitative lipidomics. We then demonstrate that Q8 is necessary for acute and sustained osmotic stress tolerance using Q8 mutants and tolerance rescue through feeding non-respiratory Q8 analogues.Finally, in vitro experiments with artificial liposomes reveal mechanical membrane stabilization as a principal mechanism of Q8-mediated osmoprotection. Thus, we find that besides regulating intracellular osmolality, E. coli enhances its cytoplasmic membrane stability to withstand osmotic stress.

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Bacterial Osmoregulation: A Paradigm for the Study of Cellular Homeostasis

Cited by 260 publications

References 129 publications

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

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

Homeostasis and Catabolism of Choline and Glycine Betaine: Lessons from Pseudomonas aeruginosa

Ubiquinone accumulation improves osmotic-stress tolerance in Escherichia coli

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