Long-Term Diversity and Genome Adaptation of Acinetobacter baylyi in a Minimal-Medium Chemostat

Jezequel, Nadia; Lagomarsino, Marco Cosentino; Heslot, F.; Thomen, Philippe

doi:10.1093/gbe/evs120

Cited by 10 publications

(17 citation statements)

References 40 publications

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“…Of the nine SNPs (numbers of SNPs in line with a recent experimental evolution report in A. baylyi (Jezequel et al, 2013)) described in Table 2, one SNP in the znuA-atp1 intergenetic region occurred in both sequenced strains. The znuA and atp1 encode a putative transporter and ATPase, respectively.…”

Section: Parallel Evolutionmentioning

confidence: 54%

Growth phase-specific evolutionary benefits of natural transformation in Acinetobacter baylyi

et al. 2015

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Natural transformation in bacteria facilitates the uptake and genomic integration of exogenous DNA. This allows horizontal exchange of adaptive traits not easily achieved by point mutations, and has a major role in the acquisition of adaptive traits exemplified by antibiotic resistance determinants and vaccination escape. Mechanisms of DNA uptake and genomic integration are well described for several naturally transformable bacterial species; however, the selective forces responsible for its evolution and maintenance are still controversial. In this study we evolved transformation-proficient and -deficient Acinetobacter baylyi for 175 days in serial transfer cultures where stress was included. We found that natural transformation-proficient populations adapted better to active growth and early stationary phase. This advantage was offset by the reduced performance in the late stationary/death phase. We demonstrate fitness trade-offs between adaptation to active growth and survival in stationary/death phase caused by antagonistic pleiotropy. The presented data suggest that the widely held assumption that recombination speeds up adaptation by rapid accumulation of multiple adaptive mutations in the same genetic background is not sufficient to fully account for the maintenance of natural transformation in bacteria.

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Section: Parallel Evolutionmentioning

confidence: 54%

Growth phase-specific evolutionary benefits of natural transformation in Acinetobacter baylyi

et al. 2015

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“…IS1236 also has been implicated in facilitating gene amplifications, including 86% of the amplification events observed in a region located close to Tn5613 (39). Sequencing of a chemostat population evolved under nitrogen-limiting conditions for ϳ2,800 generations found five IS1236 insertions and several large deletions and genomic rearrangements among 22 total mutations profiled (40), none of which affected the genes commonly mutated in our AE experiment. The abundance of both new copies of IS1236 and deletions and other chromosomal rearrangements mediated by this mobile genetic element demonstrates its central role in changing strain function and genome structure.…”

Section: Discussionmentioning

confidence: 66%

Genome Instability Mediates the Loss of Key Traits by Acinetobacter baylyi ADP1 during Laboratory Evolution

et al. 2015

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Acinetobacter baylyi ADP1 has the potential to be a versatile bacterial host for synthetic biology because it is naturally transformable. To examine the genetic reliability of this desirable trait and to understand the potential stability of other engineered capabilities, we propagated ADP1 for 1,000 generations of growth in rich nutrient broth and analyzed the genetic changes that evolved by whole-genome sequencing. Substantially reduced transformability and increased cellular aggregation evolved during the experiment. New insertions of IS1236 transposable elements and IS1236-mediated deletions led to these phenotypes in most cases and were common overall among the selected mutations. We also observed a 49-kb deletion of a prophage region that removed an integration site, which has been used for genome engineering, from every evolved genome. The comparatively low rates of these three classes of mutations in lineages that were propagated with reduced selection for 7,500 generations indicate that they increase ADP1 fitness under common laboratory growth conditions. Our results suggest that eliminating transposable elements and other genetic failure modes that affect key organismal traits is essential for improving the reliability of metabolic engineering and genome editing in undomesticated microbial hosts, such as Acinetobacter baylyi ADP1.T he large-scale engineering of genome sequences is a growing area of synthetic biology and bioengineering with many applications (1, 2). Projects such as the development of reduced bacterial genomes (3), modifying the genetic code (4), and optimizing metabolic pathways (5) require whole-scale genetic rewriting of genomes in order to accommodate progressively more ambitious goals. The process of making such modifications is a resourceintensive undertaking with significant technical, human-resource, and time costs. Acinetobacter baylyi ADP1 has been proposed as a model organism for metabolic engineering, synthetic biology, and genome evolution studies because it is naturally transformable (6-8). During normal growth in the laboratory, ADP1 expresses competence machinery that enables it to efficiently import extracellular DNA without any sequence constraints (9, 10). By designing DNA constructs with homology to the ADP1 genome, targeted deletions or insertions of new genes can be made with high efficiency without the need for artificial transformation techniques or the expression of heterologous genes, as is typically required when engineering the Escherichia coli genome (5, 11). Thus, ADP1 could be a useful chassis organism for studies that require large-scale or combinatorial genome modifications.One known challenge associated with ADP1, however, is that the competence phenotype is unstable when it is cultured in the laboratory (12). In general, genetic reliability is a key trait sought after in chassis organisms; one does not want to design a DNA sequence only to see it be rapidly deleted or mutated when placed in a living organism. In this vein, efforts to engineer E. coli v...

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“…Many microbial evolution experiments employ a constant, simple environment that imposes a seemingly straightforward and moderate selection pressure on the organism, which is often the limiting presence of a single essential nutrient (33) like carbon, nitrogen (34)(35)(36)(37), phosphorus (38)(39)(40), or sulfur (38,41). Keeping all other parameters (temperature, aeration, culture volume, and other nutrients, etc.)…”

Section: Designs and Parameters Of Experimental Evolution General Conmentioning

confidence: 99%

Experimental Design, Population Dynamics, and Diversity in Microbial Experimental Evolution

Bergh

Swings

Fauvart

et al. 2018

Microbiol Mol Biol Rev

163

164

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In experimental evolution, laboratory-controlled conditions select for the adaptation of species, which can be monitored in real time. Despite the current popularity of such experiments, nature's most pervasive biological force was long believed to be observable only on time scales that transcend a researcher's life-span, and studying evolution by natural selection was therefore carried out solely by comparative means. Eventually, microorganisms' propensity for fast evolutionary changes proved us wrong, displaying strong evolutionary adaptations over a limited time, nowadays massively exploited in laboratory evolution experiments. Here, we formulate a guide to experimental evolution with microorganisms, explaining experimental design and discussing evolutionary dynamics and outcomes and how it is used to assess ecoevolutionary theories, improve industrially important traits, and untangle complex phenotypes. Specifically, we give a comprehensive overview of the setups used in experimental evolution. Additionally, we address population dynamics and genetic or phenotypic diversity during evolution experiments and expand upon contributing factors, such as epistasis and the consequences of (a)sexual reproduction. Dynamics and outcomes of evolution are most profoundly affected by the spatiotemporal nature of the selective environment, where changing environments might lead to generalists and structured environments could foster diversity, aided by, for example, clonal interference and negative frequency-dependent selection. We conclude with future perspectives, with an emphasis on possibilities offered by fast-paced technological progress. This work is meant to serve as an introduction to those new to the field of experimental evolution, as a guide to the budding experimentalist, and as a reference work to the seasoned expert.

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Long-Term Diversity and Genome Adaptation of Acinetobacter baylyi in a Minimal-Medium Chemostat

Cited by 10 publications

References 40 publications

Growth phase-specific evolutionary benefits of natural transformation in Acinetobacter baylyi

Growth phase-specific evolutionary benefits of natural transformation in Acinetobacter baylyi

Genome Instability Mediates the Loss of Key Traits by Acinetobacter baylyi ADP1 during Laboratory Evolution

Experimental Design, Population Dynamics, and Diversity in Microbial Experimental Evolution

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