Evolutionary pathways to antibiotic resistance are dependent upon environmental structure and bacterial lifestyle
- University of Pittsburgh, United States
Abstract
Bacterial populations vary in their stress tolerance and population structure depending upon whether growth occurs in well-mixed or structured environments. We hypothesized that evolution in biofilms would generate greater genetic diversity than well-mixed environments and lead to different pathways of antibiotic resistance. We used experimental evolution and whole genome sequencing to test how the biofilm lifestyle influenced the rate, genetic mechanisms, and pleiotropic effects of resistance to ciprofloxacin in Acinetobacter baumannii populations. Both evolutionary dynamics and the identities of mutations differed between lifestyle. Planktonic populations experienced selective sweeps of mutations including the primary topoisomerase drug targets, whereas biofilm-adapted populations acquired mutations in regulators of efflux pumps. An overall trade-off between fitness and resistance level emerged, wherein biofilm-adapted clones were less resistant than planktonic but more fit in the absence of drug. However, biofilm populations developed collateral sensitivity to cephalosporins, demonstrating the clinical relevance of lifestyle on the evolution of resistance.
Data availability
Sequencing data were deposited to NCBI as Bioproject 485123.R code for filtering and data processing can be found here:https://github.com/sirmicrobe/U01_allele_freq_code.
Article and author information
Author details
Alfonso Santos-Lopez
Funding
National Institutes of Health (U01AI124302-01)
- Vaughn S Cooper
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Karla Kirkegaard, Stanford University School of Medicine, United States
Version history
- Received: April 11, 2019
- Accepted: September 13, 2019
- Accepted Manuscript published: September 13, 2019 (version 1)
- Version of Record published: October 25, 2019 (version 2)
Copyright
© 2019, Santos-Lopez et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Evolutionary pathways to antibiotic resistance are dependent upon environmental structure and bacterial lifestyle
eLife 8:e47612.
https://doi.org/10.7554/eLife.47612
Further reading
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- Evolutionary Biology
- Microbiology and Infectious Disease
The way that bacteria grow – either floating in liquid or attached to a surface – affects their ability to evolve antimicrobial resistance and our ability to treat infections.
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- Developmental Biology
- Evolutionary Biology
Despite rapid evolution across eutherian mammals, the X-linked MIR-506 family miRNAs are located in a region flanked by two highly conserved protein-coding genes (SLITRK2 and FMR1) on the X chromosome. Intriguingly, these miRNAs are predominantly expressed in the testis, suggesting a potential role in spermatogenesis and male fertility. Here, we report that the X-linked MIR-506 family miRNAs were derived from the MER91C DNA transposons. Selective inactivation of individual miRNAs or clusters caused no discernible defects, but simultaneous ablation of five clusters containing 19 members of the MIR-506 family led to reduced male fertility in mice. Despite normal sperm counts, motility, and morphology, the KO sperm were less competitive than wild-type sperm when subjected to a polyandrous mating scheme. Transcriptomic and bioinformatic analyses revealed that these X-linked MIR-506 family miRNAs, in addition to targeting a set of conserved genes, have more targets that are critical for spermatogenesis and embryonic development during evolution. Our data suggest that the MIR-506 family miRNAs function to enhance sperm competitiveness and reproductive fitness of the male by finetuning gene expression during spermatogenesis.
