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Evolutionary potential, cross-stress behavior and the genetic basis of acquired stress resistance in Escherichia coli.

ABSTRACT: Bacterial populations have a remarkable capacity to cope with extreme environmental fluctuations in their natural environments. In certain cases, adaptation to one stressful environment provides a fitness advantage when cells are exposed to a second stressor, a phenomenon that has been coined as cross-stress protection. A tantalizing question in bacterial physiology is how the cross-stress behavior emerges during evolutionary adaptation and what the genetic basis of acquired stress resistance is. To address these questions, we evolved Escherichia coli cells over 500 generations in five environments that include four abiotic stressors. Through growth profiling and competition assays, we identified several cases of positive and negative cross-stress behavior that span all strain-stress combinations. Resequencing the genomes of the evolved strains resulted in the identification of several mutations and gene amplifications, whose fitness effect was further assessed by mutation reversal and competition assays. Transcriptional profiling of all strains under a specific stress, NaCl-induced osmotic stress, and integration with resequencing data further elucidated the regulatory responses and genes that are involved in this phenomenon. Our results suggest that cross-stress dependencies are ubiquitous, highly interconnected, and can emerge within short timeframes. The high adaptive potential that we observed argues that bacterial populations occupy a genotypic space that enables a high phenotypic plasticity during adaptation in fluctuating environments.

SUBMITTER: Dragosits M

PROVIDER: S-EPMC3588905 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Evolutionary potential, cross-stress behavior and the genetic basis of acquired stress resistance in Escherichia coli.

Dragosits Martin M Mozhayskiy Vadim V Quinones-Soto Semarhy S Park Jiyeon J Tagkopoulos Ilias I

Molecular systems biology 20130101

Bacterial populations have a remarkable capacity to cope with extreme environmental fluctuations in their natural environments. In certain cases, adaptation to one stressful environment provides a fitness advantage when cells are exposed to a second stressor, a phenomenon that has been coined as cross-stress protection. A tantalizing question in bacterial physiology is how the cross-stress behavior emerges during evolutionary adaptation and what the genetic basis of acquired stress resistance is ...[more]

PMID: 23385483

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Project description:Escherichia coli isolates from inflammatory bowel disease (IBD) patients are often multidrug resistant, including to streptomycin. Streptomycin resistance (StrR) mutations can alter bacterial behavior, which may influence intestinal disease. We generated a spontaneous StrR strain of the intestinal adherent-invasive E. coli (AIEC) strain NC101. Whole-genome sequencing revealed a single missense mutation in rpsL that commonly confers StrR, rpsL-K43N. StrR NC101 exhibited a striking loss of aggregation and significantly increased motility, behaviors that can impact host-microbe interactions. Behavioral changes were associated with reduced transcription of csgA, encoding the biofilm component curli, and increased transcription of fliC, encoding flagellin. Scanning electron microscopy (SEM) detailed morphologic changes consistent with the observed alterations in multicellular behavior. Because intestinal E. coli isolates exhibit remarkable strain-specific differences, we generated spontaneous StrR mutants of 10 clinical E. coli phylotype B2 strains from patients with IBD, colorectal cancer, and urinary tract infection. Out of these 10 StrR clinical strains, two had altered colony morphology on Congo red agar (suggesting changes in extracellular products), and three had significant changes in motility. These changes were not associated with a particular rpsL mutation nor with the presence of virulence genes encoding the inflammation-associated E. coli metabolites yersiniabactin or colibactin. We conclude that common mutations in rpsL, which confer StrR, can differentially alter disease-associated phenotypes across intestinal E. coli strains. These findings highlight the heterogeneity among seemingly similar intestinal E. coli strains and reveal the need to carefully study the strain-specific effects of antibiotic resistance mutations, particularly when using these mutations during strain selection studies. IMPORTANCE We demonstrate that StrR, commonly acquired through a single point mutation in rpsL (a gene encoding part of the 30S bacterial ribosome), strikingly alters the morphology and behavior of a key intestinal AIEC strain, NC101. These changes include remarkably diminished aggregation and significantly increased motility, traits that are linked to AIEC-defining features and disease development. Phenotypic changes were heterogeneous among other StrR clinical E. coli strains, underscoring the need to evaluate the strain-specific effects of commonly acquired antibiotic resistance mutations. This is important, as the results of studies using mutant StrR Enterobacteriaceae strains (e.g., for cloning or in vivo selection) may be confounded beyond our demonstrated effects. Long term, these findings can help researchers better distinguish the contribution of specific E. coli traits to functional changes in the microbiota. Evaluating these strain-level differences could provide insight into the diversity of IBD symptoms and lead to improved therapies for microbiota-driven intestinal disorders.

Dataset Information

Evolutionary potential, cross-stress behavior and the genetic basis of acquired stress resistance in Escherichia coli.

Publications

Evolutionary potential, cross-stress behavior and the genetic basis of acquired stress resistance in Escherichia coli.

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