Gene amplification as a form of population-level gene expression regulation

Tomanek, Isabella; Grah, Rok; Lagator, Mato; Andersson, Anna M. C.; Bollback, Jonathan P.; Tkačik, Gašper; Guet, Călin C.

doi:10.1038/s41559-020-1132-7

Cited by 33 publications

(58 citation statements)

References 58 publications

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“…It is well known that the expression of a growth promoting gene can be enhanced by the spontaneous acquisition of promoter‐up mutations (Zaprasis et al ., 2014; Rosenberg et al ., 2016; Dormeyer et al ., 2017; Reuß et al ., 2019). Moreover, a growth defect, which is caused by insufficient expression of a specific gene required for rapid growth, is often suppressed by increasing the gene dosage via selective amplification (Elliot et al ., 2013; Dormeyer et al ., 2017; Rosenberg et al ., 2018; Reuß et al ., 2019; Wicke et al ., 2019; Tomanek et al ., 2020). In the present study, we found that several Δ pdxT suppressor mutants had amplified a 15 kb‐long genomic region containing the pdxS gene to overcome PLP limitation (Fig.…”

Section: Discussionmentioning

confidence: 99%

A Bacillus subtilis ΔpdxT mutant suppresses vitamin B6 limitation by acquiring mutations enhancing pdxS gene dosage and ammonium assimilation

Richts

Lentes

Daniel

et al. 2021

Environ Microbiol Rep

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Summary Pyridoxal‐5′‐phosphate (PLP), the biologically active form of vitamin B6, serves as a cofactor for many enzymes. The Gram‐positive model bacterium Bacillus subtilis synthesizes PLP via the PdxST enzyme complex, consisting of the PdxT glutaminase and the PdxS PLP synthase subunits, respectively. PdxT converts glutamine to glutamate and ammonia of which the latter is channelled to PdxS. At high extracellular ammonium concentrations, the PdxS PLP synthase subunit does not depend on PdxT. Here, we assessed the potential of a B. subtilis ΔpdxT mutant to adapt to PLP limitation at the genome level. The majority of ΔpdxT suppressors had amplified a genomic region containing the pdxS gene. We also identified mutants having acquired as yet undescribed mutations in ammonium assimilation genes, indicating that the overproduction of PdxS and the NrgA ammonium transporter partially relieve vitamin B6 limitation in a ΔpdxT mutant when extracellular ammonium is scarce. Furthermore, we found that PdxS positively affects complex colony formation in B. subtilis. The catalytic mechanism of the PdxS PLP synthase subunit could be the reason for the limited evolution of the enzyme and why we could not identify a PdxS variant producing PLP independently of PdxT at low ammonium concentrations.

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Section: Discussionmentioning

confidence: 99%

A Bacillus subtilis ΔpdxT mutant suppresses vitamin B6 limitation by acquiring mutations enhancing pdxS gene dosage and ammonium assimilation

Richts

Lentes

Daniel

et al. 2021

Environ Microbiol Rep

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“…Among the genetic factors that control colicin synthesis, PCN variability has a crucial role, as cells with high PCN are more likely to undergo colicin release 62 . These studies suggest that population heterogeneity in PCN might work as a bethedging [G] strategy: a fraction of the population is best suited to survive an environmental perturbation, but do so at the cost of overexpressing plasmid-encoded genes, which produces a competitive disadvantage when selection for high expression is absent 63 .…”

Section: [H1] Plasmid Copy Number and Evolution [H2] Increased Gene Expressionmentioning

confidence: 99%

Beyond horizontal gene transfer: the role of plasmids in bacterial evolution

et al. 2021

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Plasmids have a key role in bacterial ecology and evolution because they mobilize accessory genes by horizontal gene transfer. However, recent studies have revealed that the evolutionary impact of plasmids goes above and beyond being mere gene delivery platforms. Plasmids are usually kept at multiple copies per cell, producing islands of polyploidy in the bacterial genome. As a consequence, the evolution of plasmid-encoded genes is governed by a different set of rules than those affecting chromosomal genes, and these rules are shaped by unusual concepts in bacterial genetics such as genetic dominance, heteroplasmy or segregational drift. In this Review, we discuss recent advances that underscore the importance of plasmids in bacterial ecology and evolution beyond horizontal gene transfer. We focus on new evidence that suggests that plasmids might accelerate bacterial evolution, mainly by promoting the evolution of plasmid-encoded genes, but also by enhancing the adaptation of their host chromosome. Finally, we integrate the most relevant

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“…In other cases, phenotypic heterogeneity arises without the involvement of environmental cues, and the underlying mechanisms are diverse. Genetic mechanisms include site-specific recombination (Scott and Simon, 1982;Reyes Ruiz et al, 2020), slipped-strand mispairing at tracts of repetitive DNA sequences (Moxon et al, 2006), and amplification of specific genome regions (Belikova et al, 2020;Tomanek et al, 2020). As described below, cell diversification into two or more phenotypic states can also be driven by nongenetic mechanisms, such as propagation of feedback loops (Ferrell, 2002) and formation of DNA methylation patterns .…”

Section: Introductionmentioning

confidence: 99%

Waddington’s Landscapes in the Bacterial World

Sánchez-Romero

Casadesús

2021

Front. Microbiol.

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Conrad Waddington’s epigenetic landscape, a visual metaphor for the development of multicellular organisms, is appropriate to depict the formation of phenotypic variants of bacterial cells. Examples of bacterial differentiation that result in morphological change have been known for decades. In addition, bacterial populations contain phenotypic cell variants that lack morphological change, and the advent of fluorescent protein technology and single-cell analysis has unveiled scores of examples. Cell-specific gene expression patterns can have a random origin or arise as a programmed event. When phenotypic cell-to-cell differences are heritable, bacterial lineages are formed. The mechanisms that transmit epigenetic states to daughter cells can have strikingly different levels of complexity, from the propagation of simple feedback loops to the formation of complex DNA methylation patterns. Game theory predicts that phenotypic heterogeneity can facilitate bacterial adaptation to hostile or unpredictable environments, serving either as a division of labor or as a bet hedging that anticipates future challenges. Experimental observation confirms the existence of both types of strategies in the bacterial world.

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Gene amplification as a form of population-level gene expression regulation

Cited by 33 publications

References 58 publications

A Bacillus subtilis ΔpdxT mutant suppresses vitamin B6 limitation by acquiring mutations enhancing pdxS gene dosage and ammonium assimilation

A Bacillus subtilis ΔpdxT mutant suppresses vitamin B6 limitation by acquiring mutations enhancing pdxS gene dosage and ammonium assimilation

Beyond horizontal gene transfer: the role of plasmids in bacterial evolution

Waddington’s Landscapes in the Bacterial World

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