Promoter-creating mutations in
            <i>Pseudomonas putida</i>
            : A model system for the study of mutation in starving bacteria

Kasak, Lagle; Hõrak, Rita; Kivisaar, Maia

doi:10.1073/pnas.94.7.3134

Cited by 91 publications

(97 citation statements)

References 55 publications

(54 reference statements)

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“…The result of the mechanism(s) responsible for this phenomenon is the production of mutations that arise in nondividing or stationary-phase bacteria when the cells are subjected to nonlethal selective pressure, such as nutrientlimited environments (6,11,15,32,61). While most of the research has involved Escherichia coli model systems, similar observations have been made in other prokaryotes (43) as well as in eukaryotic organisms (69).…”

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confidence: 92%

Adaptive, or Stationary-Phase, Mutagenesis, a Component of Bacterial Differentiation in Bacillus subtilis

2002

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Adaptive (stationary-phase) mutagenesis occurs in the gram-positive bacterium Bacillus subtilis. Furthermore, taking advantage of B. subtilis as a paradigm for the study of prokaryotic differentiation and development, we have shown that this type of mutagenesis is subject to regulation involving at least two of the genes that are involved in the regulation of post-exponential phase prokaryotic differentiation, i.e., comA and comK. On the other hand, a functional RecA protein was not required for this type of mutagenesis. The results seem to suggest that a small subpopulation(s) of the culture is involved in adaptive mutagenesis and that this subpopulation(s) is hypermutable. The existence of such a hypermutable subpopulation(s) raises important considerations with respect to evolution, the development of specific mutations, the nature of bacterial populations, and the level of communication among bacteria in an ecological niche.For over a decade, there has been considerable interest in a phenomenon that has been called adaptive, or stationaryphase, mutagenesis. The result of the mechanism(s) responsible for this phenomenon is the production of mutations that arise in nondividing or stationary-phase bacteria when the cells are subjected to nonlethal selective pressure, such as nutrientlimited environments (6,11,15,32,61). While most of the research has involved Escherichia coli model systems, similar observations have been made in other prokaryotes (43) as well as in eukaryotic organisms (69).In the FЈ lac frameshift reversion assay system in E. coli, stationary-phase mutations that lead to the generation of Lac ϩ cells can be distinguished from normal growth-dependent spontaneous Lac ϩ mutations (21, 59, 63). Specifically, Lac ϩ mutations are generated in stationary-phase cells via a molecular mechanism that requires a functional homologous recombination system (11,21,36,37), FЈ transfer functions (20, 23), and a component(s) of the SOS system (50). Genetic evidence suggests that DNA polymerase III (18, 35) and DNA polymerase IV (51, 52) are responsible for the synthesis of errors that lead to these mutations. Furthermore, for the Lac ϩ mutations, different sequence spectra are generated for the stationaryphase mutations than for the types of mutations generated during growth.For instance, a majority of the Lac ϩ mutations that arise during stationary phase have a Ϫ1 deletion at mononucleotide repeats within the target gene. On the other hand, for the spontaneous mutations that arise during growth, various types of mutations occur in seemingly random locations (19, 62). These characteristics suggested that stationary-phase Lac ϩ reversions occur via a different molecular mechanism(s) than for those reversions of the same lac allele that are generated during growth. However, there is also evidence that demonstrates that the mutations generated by this lac system during stationary phase are the result of gene amplification followed by SOS-induced mutagenesis and selection (39).Although the very observations of ada...

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confidence: 92%

Adaptive, or Stationary-Phase, Mutagenesis, a Component of Bacterial Differentiation in Bacillus subtilis

2002

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“…Both of these classes have been shown to play important roles across a wide range of taxa, from vertebrates (1, 2) to bacteria (3,4), and their relative importance has been the topic of considerable discussion (5)(6)(7)(8)(9)(10)(11)(12). Significantly, many previous studies have addressed these questions by focusing on single instances of functional innovation (13)(14)(15)(16) or selective regimes (17)(18)(19)(20)(21)(22). However, to identify general principles, it is necessary to study evolutionary innovation for a large number of different functions in parallel.…”

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confidence: 99%

The predictability of molecular evolution during functional innovation

Blank

Wolf

Ackermann

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Determining the molecular changes that give rise to functional innovations is a major unresolved problem in biology. The paucity of examples has served as a significant hindrance in furthering our understanding of this process. Here we used experimental evolution with the bacterium Escherichia coli to quantify the molecular changes underlying functional innovation in 68 independent instances ranging over 22 different metabolic functions. Using whole-genome sequencing, we show that the relative contribution of regulatory and structural mutations depends on the cellular context of the metabolic function. In addition, we find that regulatory mutations affect genes that act in pathways relevant to the novel function, whereas structural mutations affect genes that act in unrelated pathways. Finally, we use population genetic modeling to show that the relative contributions of regulatory and structural mutations during functional innovation may be affected by population size. These results provide a predictive framework for the molecular basis of evolutionary innovation, which is essential for anticipating future evolutionary trajectories in the face of rapid environmental change.adaptation | transcription | compensatory mutation | biosynthesis O ne of the most important questions in evolutionary biology concerns the molecular mechanisms that underlie functional innovations. These changes are often polarized into two classes: those that affect protein structure and those that affect protein expression level. Both of these classes have been shown to play important roles across a wide range of taxa, from vertebrates (1, 2) to bacteria (3, 4), and their relative importance has been the topic of considerable discussion (5-12). Significantly, many previous studies have addressed these questions by focusing on single instances of functional innovation (13-16) or selective regimes (17)(18)(19)(20)(21)(22). However, to identify general principles, it is necessary to study evolutionary innovation for a large number of different functions in parallel. Indeed, the fact that only a small number of examples exist has resulted in few hypotheses being put forth that identify general characteristics of the molecular changes underlying functional innovation. One prominent hypothesis states that if the development of a novel trait is spatially or temporally limited, then innovation frequently occurs through changes in regulation (23,24). Whether there are general patterns beyond this is not well-established.Here we used an experimental system that allows the analysis of a large number of independent cases of evolutionary innovation and investigation of the underlying genetic changes. We worked with a collection of 87 strains of Escherichia coli that each had a deletion of one gene encoding a different metabolic function (SI Appendix, Table S1). Each of these deletions resulted in an inability to grow in minimal glucose media. Then, for each of these 87 deleted metabolic functions, we used experimental evolution to select for novel func...

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“…In previous studies on adaptation to utilize phenol using recombinant strains, mutations were found in the promoter region which resulted in constitutively active 0''-dependent promoters (Burchhardt et al, 1997;Kasak et al, 1997;Nurk et al, 1993). The adaptation mechanism of strain T A N 1 was quite different because a mutation was not found in the promoter region.…”

Section: Discussionmentioning

confidence: 99%

“…strain EST1001 (Kivisaar et al, 1989), tbuD from Pseudomonas pickettii PKOl (Kukor & Olson, 1992) or pheA from Bacillus stearothermophilus BR219 (Kim & Oriel, 1995). Recently, mutations that allow P. putida or Escherichia coli to utilize phenol as a carbon source have been reported (Burchhardt et al, 1997;Kasak et al, 1997;Nurk et al, 1993). These studies used recombinant strains transformed with exogenous genes for phenol degradation.…”

Section: Introductionmentioning

confidence: 99%

Adaptation of Cornamonas testosteroni TAM1 to utilize phenol: organization and regulation of the genes involved in phenol degradatio

Arai¹,

Akahira²,

Ohishi³

et al. 1998

Microbiology

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Comamonas testosteroni TAU1 was not able to grow on phenol as a sole carbon and energy source, but it gained the ability to utilize phenol after a 2-3-week incubation in a medium containing phenol. Phenol hydroxylase (PH) and catechol2,3-dioxygenase (C230) were highly induced by phenol in the adapted strain designated as strain P1, suggesting that phenol was degraded via the meta-pathway. Gene clusters for phenol degradation were isolated from both strains TAU1 and P1. The structural genes encoding multicomponent PH and C230 (aphKLMNOPQB), and a regulatory gene of the NtrC family (aphR), were located in a divergent transcriptional organization. The cloned aphKLMNOPQl3 genes from either strain TAU1 or strain P1 produced active PH and C230 enzymes in strain TA441. No difference was found between the strains in the sequences of aphR and the intergenic promoter region of aphK and aphR. However, the transcriptional activities of the aphK and aphR promoters were higher in strain P1 than in strain TA441. The aphK-promoter activity was not observed in aphR mutant strains and these strains could not grow on phenol. The aphR mutant of strain P1 was able to grow on phenol after transformation with a recombinant aphR gene but strain TAM1 was not, suggesting that the expression of the aph genes is silenced by an unidentified repressor in strain TAU1 and that this repressor is modified in strain P1.

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Promoter-creating mutations in Pseudomonas putida : A model system for the study of mutation in starving bacteria

Cited by 91 publications

References 55 publications

Adaptive, or Stationary-Phase, Mutagenesis, a Component of Bacterial Differentiation in Bacillus subtilis

Adaptive, or Stationary-Phase, Mutagenesis, a Component of Bacterial Differentiation in Bacillus subtilis

The predictability of molecular evolution during functional innovation

Adaptation of Cornamonas testosteroni TAM1 to utilize phenol: organization and regulation of the genes involved in phenol degradatio

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