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Article ; Online: The Role of the Environment in Horizontal Gene Transfer.

Acar Kirit, Hande / Bollback, Jonathan P / Lagator, Mato

2022 Volume 39, Issue 11

Abstract: Gene-by-environment interactions play a crucial role in horizontal gene transfer by affecting how the transferred genes alter host fitness. However, how the environment modulates the fitness effect of transferred genes has not been tested systematically ... ...

Abstract	Gene-by-environment interactions play a crucial role in horizontal gene transfer by affecting how the transferred genes alter host fitness. However, how the environment modulates the fitness effect of transferred genes has not been tested systematically in an experimental study. We adapted a high-throughput technique for obtaining very precise estimates of bacterial fitness, in order to measure the fitness effects of 44 orthologs transferred from Salmonella Typhimurium to Escherichia coli in six physiologically relevant environments. We found that the fitness effects of individual genes were highly dependent on the environment, while the distributions of fitness effects across genes were not, with all tested environments resulting in distributions of same shape and spread. Furthermore, the extent to which the fitness effects of a gene varied between environments depended on the average fitness effect of that gene across all environments, with nearly neutral and nearly lethal genes having more consistent fitness effects across all environments compared to deleterious genes. Put together, our results reveal the unpredictable nature of how environmental conditions impact the fitness effects of each individual gene. At the same time, distributions of fitness effects across environments exhibit consistent features, pointing to the generalizability of factors that shape horizontal gene transfer of orthologous genes.
MeSH term(s)	Gene Transfer, Horizontal ; Escherichia coli/genetics ; Salmonella typhimurium/genetics ; Bacteria/genetics ; Environment
Language	English
Publishing date	2022-10-13
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	998579-7
ISSN	1537-1719 ; 0737-4038
ISSN (online)	1537-1719
ISSN	0737-4038
DOI	10.1093/molbev/msac220
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Article ; Online: Pervasive genotype-by-environment interactions shape the fitness effects of antibiotic resistance mutations.

Soley, Jake K / Jago, Matthew / Walsh, Calum J / Khomarbaghi, Zahra / Howden, Benjamin P / Lagator, Mato

Proceedings. Biological sciences

2023 Volume 290, Issue 2005, Page(s) 20231030

Abstract: The fitness effects of antibiotic resistance mutations are a major driver of resistance evolution. While the nutrient environment affects bacterial fitness, experimental studies of resistance typically measure fitness of mutants in a single environment ... ...

Abstract	The fitness effects of antibiotic resistance mutations are a major driver of resistance evolution. While the nutrient environment affects bacterial fitness, experimental studies of resistance typically measure fitness of mutants in a single environment only. We explored how the nutrient environment affected the fitness effects of rifampicin-resistant
MeSH term(s)	Gene-Environment Interaction ; Drug Resistance, Bacterial/genetics ; Anti-Bacterial Agents/pharmacology ; Mutation ; Genotype ; Escherichia coli/genetics ; Genetic Fitness
Chemical Substances	Anti-Bacterial Agents
Language	English
Publishing date	2023-08-16
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	209242-6
ISSN	1471-2954 ; 0080-4649 ; 0962-8452 ; 0950-1193
ISSN (online)	1471-2954
ISSN	0080-4649 ; 0962-8452 ; 0950-1193
DOI	10.1098/rspb.2023.1030
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Article ; Online: Adaptation at different points along antibiotic concentration gradients.

Lagator, Mato / Uecker, Hildegard / Neve, Paul

Biology letters

2021 Volume 17, Issue 5, Page(s) 20200913

Abstract: Antibiotic concentrations vary dramatically in the body and the environment. Hence, understanding the dynamics of resistance evolution along antibiotic concentration gradients is critical for predicting and slowing the emergence and spread of resistance. ...

Abstract	Antibiotic concentrations vary dramatically in the body and the environment. Hence, understanding the dynamics of resistance evolution along antibiotic concentration gradients is critical for predicting and slowing the emergence and spread of resistance. While it has been shown that increasing the concentration of an antibiotic slows resistance evolution, how adaptation to one antibiotic concentration correlates with fitness at other points along the gradient has not received much attention. Here, we selected populations of
MeSH term(s)	Adaptation, Physiological ; Anti-Bacterial Agents/pharmacology ; Drug Resistance, Bacterial ; Escherichia coli ; Mutation
Chemical Substances	Anti-Bacterial Agents
Language	English
Publishing date	2021-05-12
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2135022-X
ISSN	1744-957X ; 1744-9561
ISSN (online)	1744-957X
ISSN	1744-9561
DOI	10.1098/rsbl.2020.0913
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Zs.A 1364 -Letters-: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (1.OG) ab Jg. 2022: Lesesaal (EG)
Zs.A 6024: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 2021: Bestellungen von Artikeln über das Online-Bestellformular ab Jg. 2022: Lesesaal (EG)

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Article ; Online: Experimental determination of evolutionary barriers to horizontal gene transfer.

Acar Kirit, Hande / Lagator, Mato / Bollback, Jonathan P

BMC microbiology

2020 Volume 20, Issue 1, Page(s) 326

Abstract: Background: Horizontal gene transfer, the acquisition of genes across species boundaries, is a major source of novel phenotypes that enables microbes to rapidly adapt to new environments. How the transferred gene alters the growth - fitness - of the new ...

Abstract	Background: Horizontal gene transfer, the acquisition of genes across species boundaries, is a major source of novel phenotypes that enables microbes to rapidly adapt to new environments. How the transferred gene alters the growth - fitness - of the new host affects the success of the horizontal gene transfer event and how rapidly the gene spreads in the population. Several selective barriers - factors that impact the fitness effect of the transferred gene - have been suggested to impede the likelihood of horizontal transmission, however experimental evidence is scarce. The objective of this study was to determine the fitness effects of orthologous genes transferred from Salmonella enterica serovar Typhimurium to Escherichia coli to identify the selective barriers using highly precise experimental measurements. Results: We found that most gene transfers result in strong fitness costs. Previously identified evolutionary barriers - gene function and the number of protein-protein interactions - did not predict the fitness effects of transferred genes. In contrast, dosage sensitivity, gene length, and the intrinsic protein disorder significantly impact the likelihood of a successful horizontal transfer. Conclusion: While computational approaches have been successful in describing long-term barriers to horizontal gene transfer, our experimental results identified previously underappreciated barriers that determine the fitness effects of newly transferred genes, and hence their short-term eco-evolutionary dynamics.
MeSH term(s)	Escherichia coli/genetics ; Escherichia coli/metabolism ; Gene Transfer, Horizontal ; Genes, Bacterial ; Genetic Fitness ; Models, Genetic ; Salmonella typhimurium/genetics ; Salmonella typhimurium/metabolism
Language	English
Publishing date	2020-10-28
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1471-2180
ISSN (online)	1471-2180
DOI	10.1186/s12866-020-01983-5
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Article ; Online: Predicting bacterial promoter function and evolution from random sequences.

Lagator, Mato / Sarikas, Srdjan / Steinrueck, Magdalena / Toledo-Aparicio, David / Bollback, Jonathan P / Guet, Calin C / Tkačik, Gašper

eLife

2022 Volume 11

Abstract: Predicting function from sequence is a central problem of biology. Currently, this is possible only locally in a narrow mutational neighborhood around a wildtype sequence rather than globally from any sequence. Using random mutant libraries, we developed ...

Abstract	Predicting function from sequence is a central problem of biology. Currently, this is possible only locally in a narrow mutational neighborhood around a wildtype sequence rather than globally from any sequence. Using random mutant libraries, we developed a biophysical model that accounts for multiple features of σ
MeSH term(s)	Escherichia coli/genetics ; Escherichia coli/metabolism ; Evolution, Molecular ; Gene Expression ; Genome, Bacterial ; Models, Theoretical ; Mutation ; Promoter Regions, Genetic
Language	English
Publishing date	2022-01-26
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.64543
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Article ; Online: Predicting bacterial promoter function and evolution from random sequences

Mato Lagator / Srdjan Sarikas / Magdalena Steinrueck / David Toledo-Aparicio / Jonathan P Bollback / Calin C Guet / Gašper Tkačik

eLife, Vol

2022 Volume 11

Abstract	Predicting function from sequence is a central problem of biology. Currently, this is possible only locally in a narrow mutational neighborhood around a wildtype sequence rather than globally from any sequence. Using random mutant libraries, we developed a biophysical model that accounts for multiple features of σ70 binding bacterial promoters to predict constitutive gene expression levels from any sequence. We experimentally and theoretically estimated that 10–20% of random sequences lead to expression and ~80% of non-expressing sequences are one mutation away from a functional promoter. The potential for generating expression from random sequences is so pervasive that selection acts against σ70-RNA polymerase binding sites even within inter-genic, promoter-containing regions. This pervasiveness of σ70-binding sites implies that emergence of promoters is not the limiting step in gene regulatory evolution. Ultimately, the inclusion of novel features of promoter function into a mechanistic model enabled not only more accurate predictions of gene expression levels, but also identified that promoters evolve more rapidly than previously thought.
Keywords	gene regulation ; RNA polymerase ; genotype-phenotype map ; adaptive evolution ; promoter ; Medicine ; R ; Science ; Q ; Biology (General) ; QH301-705.5
Subject code	612
Language	English
Publishing date	2022-01-01T00:00:00Z
Publisher	eLife Sciences Publications Ltd
Document type	Article ; Online
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Article ; Online: Evolutionary potential of transcription factors for gene regulatory rewiring.

Igler, Claudia / Lagator, Mato / Tkačik, Gašper / Bollback, Jonathan P / Guet, Călin C

Nature ecology & evolution

2018 Volume 2, Issue 10, Page(s) 1633–1643

Abstract: Gene regulatory networks evolve through rewiring of individual components-that is, through changes in regulatory connections. However, the mechanistic basis of regulatory rewiring is poorly understood. Using a canonical gene regulatory system, we ... ...

Abstract	Gene regulatory networks evolve through rewiring of individual components-that is, through changes in regulatory connections. However, the mechanistic basis of regulatory rewiring is poorly understood. Using a canonical gene regulatory system, we quantify the properties of transcription factors that determine the evolutionary potential for rewiring of regulatory connections: robustness, tunability and evolvability. In vivo repression measurements of two repressors at mutated operator sites reveal their contrasting evolutionary potential: while robustness and evolvability were positively correlated, both were in trade-off with tunability. Epistatic interactions between adjacent operators alleviated this trade-off. A thermodynamic model explains how the differences in robustness, tunability and evolvability arise from biophysical characteristics of repressor-DNA binding. The model also uncovers that the energy matrix, which describes how mutations affect repressor-DNA binding, encodes crucial information about the evolutionary potential of a repressor. The biophysical determinants of evolutionary potential for regulatory rewiring constitute a mechanistic framework for understanding network evolution.
MeSH term(s)	Bacteriophage lambda/genetics ; Biological Evolution ; Evolution, Molecular ; Gene Regulatory Networks ; Models, Genetic ; Mutation ; Transcription Factors/genetics ; Viral Proteins/genetics
Chemical Substances	Transcription Factors ; Viral Proteins
Language	English
Publishing date	2018-09-10
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	2397-334X
ISSN (online)	2397-334X
DOI	10.1038/s41559-018-0651-y
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Article ; Online: On the mechanistic nature of epistasis in a canonical

Lagator, Mato / Paixão, Tiago / Barton, Nicholas H / Bollback, Jonathan P / Guet, Călin C

eLife

2017 Volume 6

Abstract: Understanding the relation between genotype and phenotype remains a major challenge. The difficulty of predicting individual mutation effects, and particularly the interactions between them, has prevented the development of a comprehensive theory that ... ...

Abstract	Understanding the relation between genotype and phenotype remains a major challenge. The difficulty of predicting individual mutation effects, and particularly the interactions between them, has prevented the development of a comprehensive theory that links genotypic changes to their phenotypic effects. We show that a general thermodynamic framework for gene regulation, based on a biophysical understanding of protein-DNA binding, accurately predicts the sign of epistasis in a canonical
Language	English
Publishing date	2017-05-18
Publishing country	England
Document type	Journal Article
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.25192
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Article ; Online ; Research data: (with research data) Role of sex and migration in adaptation to sink environments.

Lagator, Mato / Morgan, Andrew / Neve, Paul / Colegrave, Nick

Evolution; international journal of organic evolution

2014 Volume 68, Issue 8, Page(s) 2296–2305

Abstract: Understanding the effects of sex and migration on adaptation to novel environments remains a key problem in evolutionary biology. Using a single-cell alga Chlamydomonas reinhardtii, we investigated how sex and migration affected rates of evolutionary ... ...

Abstract	Understanding the effects of sex and migration on adaptation to novel environments remains a key problem in evolutionary biology. Using a single-cell alga Chlamydomonas reinhardtii, we investigated how sex and migration affected rates of evolutionary rescue in a sink environment, and subsequent changes in fitness following evolutionary rescue. We show that sex and migration affect both the rate of evolutionary rescue and subsequent adaptation. However, their combined effects change as the populations adapt to a sink habitat. Both sex and migration independently increased rates of evolutionary rescue, but the effect of sex on subsequent fitness improvements, following initial rescue, changed with migration, as sex was beneficial in the absence of migration but constraining adaptation when combined with migration. These results suggest that sex and migration are beneficial during the initial stages of adaptation, but can become detrimental as the population adapts to its environment.
MeSH term(s)	Adaptation, Physiological/genetics ; Biological Evolution ; Chlamydomonas reinhardtii/genetics ; Environment ; Genetic Fitness ; Reproduction
Language	English
Publishing date	2014-08
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2036375-8
ISSN	1558-5646 ; 0014-3820 ; 0014-3820
ISSN (online)	1558-5646
ISSN	0014-3820
DOI	10.1111/evo.12440
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Article ; Online: (with research data) Selection history and epistatic interactions impact dynamics of adaptation to novel environmental stresses.

Lagator, Mato / Colegrave, Nick / Neve, Paul

Proceedings. Biological sciences

2014 Volume 281, Issue 1794, Page(s) 20141679

Abstract: In rapidly changing environments, selection history may impact the dynamics of adaptation. Mutations selected in one environment may result in pleiotropic fitness trade-offs in subsequent novel environments, slowing the rates of adaptation. Epistatic ... ...

Abstract	In rapidly changing environments, selection history may impact the dynamics of adaptation. Mutations selected in one environment may result in pleiotropic fitness trade-offs in subsequent novel environments, slowing the rates of adaptation. Epistatic interactions between mutations selected in sequential stressful environments may slow or accelerate subsequent rates of adaptation, depending on the nature of that interaction. We explored the dynamics of adaptation during sequential exposure to herbicides with different modes of action in Chlamydomonas reinhardtii. Evolution of resistance to two of the herbicides was largely independent of selection history. For carbetamide, previous adaptation to other herbicide modes of action positively impacted the likelihood of adaptation to this herbicide. Furthermore, while adaptation to all individual herbicides was associated with pleiotropic fitness costs in stress-free environments, we observed that accumulation of resistance mechanisms was accompanied by a reduction in overall fitness costs. We suggest that antagonistic epistasis may be a driving mechanism that enables populations to more readily adapt in novel environments. These findings highlight the potential for sequences of xenobiotics to facilitate the rapid evolution of multiple-drug and -pesticide resistance, as well as the potential for epistatic interactions between adaptive mutations to facilitate evolutionary rescue in rapidly changing environments.
MeSH term(s)	Adaptation, Physiological/genetics ; Chlamydomonas reinhardtii/genetics ; Epistasis, Genetic ; Genetic Fitness ; Herbicide Resistance/genetics ; Herbicides/toxicity ; Models, Genetic ; Selection, Genetic
Chemical Substances	Herbicides
Language	English
Publishing date	2014-09-17
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	209242-6
ISSN	1471-2954 ; 0080-4649 ; 0962-8452 ; 0950-1193
ISSN (online)	1471-2954
ISSN	0080-4649 ; 0962-8452 ; 0950-1193
DOI	10.1098/rspb.2014.1679
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