scholarly journals Escherichia coli populations adapt to complex, unpredictable fluctuations by minimizing trade-offs across environments

2016 ◽  
Author(s):  
Shraddha Madhav Karve ◽  
Devika Bhave ◽  
Dhanashri Nevgi ◽  
Sutirth Dey

In nature, organisms are simultaneously exposed to multiple stresses (i.e. complex environments) that often fluctuate unpredictably. While both these factors have been studied in isolation, the interaction of the two remains poorly explored. To address this issue, we selected laboratory populations of Escherichia coli under complex (i.e. stressful combinations of pH, H2O2 and NaCl) unpredictably fluctuating environments for ~900 generations. We compared the growth rates and the corresponding trade-off patterns of these populations to those that were selected under constant values of the component stresses (i.e. pH, H2O2 and NaCl) for the same duration. The fluctuation-selected populations had greater mean growth rate and lower variation for growth rate over all the selection environments experienced. However, while the populations selected under constant stresses experienced trade-offs in the environments other than those in which they were selected, the fluctuation-selected populations could by-pass the across-environment trade-offs almost entirely. Interestingly, trade-offs were found between growth rates and carrying capacities. The results suggest that complexity and fluctuations can strongly affect the underlying trade-off structure in evolving populations.

2016 ◽  
Author(s):  
Shraddha Karve ◽  
Devika Bhave ◽  
Dhanashri Nevgi ◽  
Sutirth Dey

AbstractIn nature, organisms are simultaneously exposed to multiple stresses (i.e. complex environments) that often fluctuate unpredictably. While both these factors have been studied in isolation, the interaction of the two remains poorly explored. To address this issue, we selected laboratory populations ofEscherichia coliunder complex (i.e. stressful combinations of pH, H2O2and NaCl) unpredictably fluctuating environments for ~900 generations. We compared the growth rates and the corresponding trade-off patterns of these populations to those that were selected under constant values of the component stresses (i.e. pH, H2O2and NaCl) for the same duration. The fluctuation-selected populations had greater mean growth rate and lower variation for growth rate over all the selection environments experienced. However, while the populations selected under constant stresses experienced severe tradeoffs in many of the environments other than those in which they were selected, the fluctuation-selected populations could by-pass the across-environment trade-offs completely. Interestingly, trade-offs were found between growth rates and carrying capacities. The results suggest that complexity and fluctuations can strongly affect the underlying trade-off structure in evolving populations.


2017 ◽  
Author(s):  
Meike T. Wortel ◽  
Elad Noor ◽  
Michael Ferris ◽  
Frank J. Bruggeman ◽  
Wolfram Liebermeister

AbstractMicrobes may maximize the number of daughter cells per time or per amount of nutrients consumed. These two strategies correspond, respectively, to the use of enzyme-efficient or substrate-efficient metabolic pathways. In reality, fast growth is often associated with wasteful, yield-inefficient metabolism, and a general thermodynamic trade-off between growth rate and biomass yield has been proposed to explain this. We studied growth rate/yield trade-offs by using a novel modeling framework, Enzyme-Flux Cost Minimization (EFCM) and by assuming that the growth rate depends directly on the enzyme investment per rate of biomass production. In a comprehensive mathematical model of core metabolism inE. coli, we screened all elementary flux modes leading to cell synthesis, characterized them by the growth rates and yields they provide, and studied the shape of the resulting rate/yield Pareto front. By varying the model parameters, we found that the rate/yield trade-off is not universal, but depends on metabolic kinetics and environmental conditions. A prominent trade-off emerges under oxygen-limited growth, where yield-inefficient pathways support a 2-to-3 times higher growth rate than yield-efficient pathways. EFCM can be widely used to predict optimal metabolic states and growth rates under varying nutrient levels, perturbations of enzyme parameters, and single or multiple gene knockouts.Author SummaryWhen cells compete for nutrients, those that grow faster and produce more offspring per time are favored by natural selection. In contrast, when cells need to maximize the cell number at a limited nutrient supply, fast growth does not matter and an efficient use of nutrients (i.e. high biomass yield) is essential. This raises a basic question about metabolism: can cells achieve high growth rates and yields simultaneously, or is there a conflict between the two goals? Using a new modeling method called Enzymatic Flux Cost Minimization (EFCM), we predict cellular growth rates and find that growth rate/yield trade-offs and the ensuing preference for enzyme-efficient or substrate-efficient metabolic pathways are not universal, but depend on growth conditions such as external glucose and oxygen concentrations.


The Condor ◽  
2006 ◽  
Vol 108 (3) ◽  
pp. 601-611 ◽  
Author(s):  
Daniel R. Ardia

AbstractNestlings can exhibit considerable variation in developmental patterns both within and among locations due to differences in environmental conditions and parental investment. I investigated trade-offs between nestling growth rate and residual body mass (body condition) at three locations across the range of the Tree Swallow (Tachycineta bicolor). Nestlings at the northern extreme of the range in Alaska had slower growth rates, lower body mass, and higher residual body mass than nestlings in New York and Tennessee. High insect availability was correlated with increased growth rates of nestlings in New York and Tennessee, but not in Alaska. Conversely, nestlings in Alaska showed increased residual body mass with high insect availability, but nestlings in New York and Tennessee did not. The trade-off between growth rate and residual body mass varied among sites, with fast-growing nestlings in Tennessee maintaining a higher residual body mass than those in Alaska. These results suggest that factors affecting offspring growth and condition vary among sites, leading to geographical differences in offspring development trajectories.


2015 ◽  
Author(s):  
Marjon GJ de Vos ◽  
Alexandre Dawid ◽  
Vanda Sunderlikova ◽  
Sander J Tans

Epistatic interactions can frustrate and shape evolutionary change. Indeed, phenotypes may fail to evolve because essential mutations can only be selected positively if fixed simultaneously. How environmental variability affects such constraints is poorly understood. Here we studied genetic constraints in fixed and fluctuating environments, using theEscherichia coli lacoperon as a model system for genotype-environment interactions. The data indicated an apparent paradox: in different fixed environments, mutational trajectories became trapped at sub-optima where no further improvements were possible, while repeated switching between these same environments allowed unconstrained adaptation by continuous improvements. Pervasive cross-environmental trade-offs transformed peaks into valleys upon environmental change, thus enabling escape from entrapment. This study shows that environmental variability can lift genetic constraint, and that trade-offs not only impede but can also facilitate adaptive evolution.


2017 ◽  
Author(s):  
Adam Paul Arkin ◽  
Guillaume Cambray

ABSTRACTControl of protein biosynthesis is at the heart of resource allocation and cell adaptation to fluctuating environments. One gene’s translation often occurs at the expense of another’s, resulting in global energetic and fitness trade-offs during differential expression of various functions. Patterns of ribosome utilization—as controlled by initiation, elongation and release rates—are central to this balance. To disentangle their respective determinants and physiological impacts, we complemented measurements of protein production with highly parallelized quantifications of transcripts’ abundance and decay, ribosome loading and cellular growth rate for 244,000 precisely designed sequence variants of an otherwise standard reporter. We find highly constrained, non-monotonic relationships between measured phenotypes. We show that fitness defects derive either from protein overproduction, with efficient translation initiation and heavy ribosome flows; or from unproductive ribosome sequestration by highly structured, slowly initiated and overly stabilized transcripts. These observations demonstrate physiological impacts of key sequence features in natural and designed transcripts.


mBio ◽  
2018 ◽  
Vol 9 (2) ◽  
Author(s):  
Valerie S. Forsyth ◽  
Chelsie E. Armbruster ◽  
Sara N. Smith ◽  
Ali Pirani ◽  
A. Cody Springman ◽  
...  

ABSTRACTUropathogenicEscherichia coli(UPEC) strains cause most uncomplicated urinary tract infections (UTIs). These strains are a subgroup of extraintestinal pathogenicE. coli(ExPEC) strains that infect extraintestinal sites, including urinary tract, meninges, bloodstream, lungs, and surgical sites. Here, we hypothesize that UPEC isolates adapt to and grow more rapidly within the urinary tract than otherE. coliisolates and survive in that niche. To date, there has not been a reliable method available to measure their growth ratein vivo. Here we used two methods: segregation of nonreplicating plasmid pGTR902, and peak-to-trough ratio (PTR), a sequencing-based method that enumerates bacterial chromosomal replication forks present during cell division. In the murine model of UTI, UPEC strain growth was robustin vivo, matching or exceedingin vitrogrowth rates and only slowing after reaching high CFU counts at 24 and 30 h postinoculation (hpi). In contrast, asymptomatic bacteriuria (ABU) strains tended to maintain high growth ratesin vivoat 6, 24, and 30 hpi, and population densities did not increase, suggesting that host responses or elimination limited population growth. Fecal strains displayed moderate growth rates at 6 hpi but did not survive to later times. By PTR,E. coliin urine of human patients with UTIs displayed extraordinarily rapid growth during active infection, with a mean doubling time of 22.4 min. Thus, in addition to traditional virulence determinants, including adhesins, toxins, iron acquisition, and motility, very high growth ratesin vivoand resistance to the innate immune response appear to be critical phenotypes of UPEC strains.IMPORTANCEUropathogenicEscherichia coli(UPEC) strains cause most urinary tract infections in otherwise healthy women. While we understand numerous virulence factors are utilized byE. colito colonize and persist within the urinary tract, these properties are inconsequential unless bacteria can divide rapidly and survive the host immune response. To determine the contribution of growth rate to successful colonization and persistence, we employed two methods: one involving the segregation of a nonreplicating plasmid in bacteria as they divide and the peak-to-trough ratio, a sequencing-based method that enumerates chromosomal replication forks present during cell division. We found that UPEC strains divide extraordinarily rapidly during human UTIs. These techniques will be broadly applicable to measurein vivogrowth rates of other bacterial pathogens during host colonization.


1998 ◽  
Vol 180 (7) ◽  
pp. 1970-1972 ◽  
Author(s):  
Bradley S. Stevenson ◽  
Thomas M. Schmidt

ABSTRACT Inadequate regulation of the expression of additional plasmid-borne rRNA operons in Escherichia coli was exaggerated at slow growth rates, resulting in increases of approximately 100% for RNA concentration and 33% for doubling time. These observations are consistent with the hypothesis that multiple rRNA operons constitute a metabolic burden at slow growth rates.


2014 ◽  
Vol 62 (1) ◽  
pp. 48 ◽  
Author(s):  
C. H. Lusk ◽  
K. M. Sendall ◽  
P. J. Clarke

A trade-off between shade tolerance and growth in open conditions is widely believed to underlie the dynamics of humid forests. Little is known about how the growth versus shade tolerance trade-off interacts with other major trade-offs associated with differential adaptation to major environmental factors besides light. We asked whether the growth versus shade tolerance trade-off differed between subtropical rainforest tree assemblages native to basaltic (fertile) and rhyolitic (infertile) soils in northern New South Wales, because of the allocational costs of adaptation to low nutrient availability. Seedling relative growth rates of six basalt specialists and five rhyolite specialists were measured in a glasshouse and the minimum light requirements of each species were quantified in the field by determining the 10th percentile of juvenile tree distributions in relation to understorey light availability. A similar range of light requirements was observed in the two assemblages, and although the two fastest growing species were basalt specialists, seedling growth rates did not differ significantly between the two substrates. The overall relationship between light requirements and growth rate was weak, and there was no compelling evidence that the slope or elevation of this relationship differed between the two assemblages. Growth rates were significantly correlated, overall, with specific leaf area, and marginally with leaf area ratio. The apparent similarity of the growth versus shade tolerance trade-off in the two suites of species could reflect effects of leaf nutrient content on respiration rates; basalt specialists tended to have a smaller root mass fraction, but this may have been offset by the effects of leaf nitrogen status on respiration rates, with higher respiration rates expected on fertile basaltic soils. However, the results might also partly reflect impairment of the field performance of two basalt specialists that were heavily attacked by natural enemies.


1997 ◽  
Vol 75 (2) ◽  
pp. 335-337 ◽  
Author(s):  
Anthony P. Farrell ◽  
William Bennett ◽  
Robert H. Devlin

We examined the consequence of remarkably fast growth rates in transgenic fish, using swimming performance as a physiological fitness variable. Substantially faster growth rates were achieved by the insertion of an "all-salmon" growth hormone gene construct in transgenic coho salmon (Oncorhynchus kisutch). On an absolute speed basis, transgenic fish swam no faster at their critical swimming speed than smaller non-transgenic controls, and much slower than older non-transgenic controls of the same size. Thus, we find a marked trade-off between growth rate and swimming performance, and these results suggest that transgenic fish may be an excellent model to evaluate existing ideas regarding physiological design.


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