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The Single-Stranded RNA Bacteriophage Q? Adapts Rapidly to High Temperatures: An Evolution Experiment.

ABSTRACT: Single-stranded (ss)RNA viruses are thought to evolve rapidly due to an inherently high mutation rate. However, it remains unclear how ssRNA viruses adapt to novel environments and/or how many and what types of substitutions are needed to facilitate this evolution. In this study, we followed the adaptation of the ssRNA bacteriophage Q? using thermally adapted Escherichia coli as a host, which can efficiently grow at temperatures between 37.2 and 45.3 °C. This made it possible to evaluate Q? adaptation to the highest known temperature that supports growth, 45.3 °C. We found that Q? was capable of replication at this temperature; within 114 days (~1260 generations), we detected more than 34 novel point mutations in the genome of the thermally adapted Q? population, representing 0.8% of the total Q? genome. In addition, we returned the 45.3 °C-adapted Q? populations to 37.2 °C and passaged them for 8 days (~124 generations). We found that the reverse-adapted Q? population showed little to no decrease in fitness. These results indicate that Q? can evolve in response to increasing temperatures in a short period of time with the accumulation of point mutations.

SUBMITTER: Hossain MT

PROVIDER: S-EPMC7354602 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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The Single-Stranded RNA Bacteriophage Qβ Adapts Rapidly to High Temperatures: An Evolution Experiment.

Hossain Md Tanvir MT Yokono Toma T Kashiwagi Akiko A

Viruses 20200612 6

Single-stranded (ss)RNA viruses are thought to evolve rapidly due to an inherently high mutation rate. However, it remains unclear how ssRNA viruses adapt to novel environments and/or how many and what types of substitutions are needed to facilitate this evolution. In this study, we followed the adaptation of the ssRNA bacteriophage Qβ using thermally adapted <i>Escherichia coli</i> as a host, which can efficiently grow at temperatures between 37.2 and 45.3 °C. This made it possible to evaluate ...[more]

PMID: 32545482

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Project description:UnlabelledChanges in protein function and other biological properties, such as RNA structure, are crucial for adaptation of organisms to novel or inhibitory environments. To investigate how mutations that do not alter amino acid sequence may be positively selected, we performed a thermal adaptation experiment using the single-stranded RNA bacteriophage Qβ in which the culture temperature was increased from 37.2°C to 41.2°C and finally to an inhibitory temperature of 43.6°C in a stepwise manner in three independent lines. Whole-genome analysis revealed 31 mutations, including 14 mutations that did not result in amino acid sequence alterations, in this thermal adaptation. Eight of the 31 mutations were observed in all three lines. Reconstruction and fitness analyses of Qβ strains containing only mutations observed in all three lines indicated that five mutations that did not result in amino acid sequence changes but increased the amplification ratio appeared in the course of adaptation to growth at 41.2°C. Moreover, these mutations provided a suitable genetic background for subsequent mutations, altering the fitness contribution from deleterious to beneficial. These results clearly showed that mutations that do not alter the amino acid sequence play important roles in adaptation of this single-stranded RNA virus to elevated temperature.ImportanceRecent studies using whole-genome analysis technology suggested the importance of mutations that do not alter the amino acid sequence for adaptation of organisms to novel environmental conditions. It is necessary to investigate how these mutations may be positively selected and to determine to what degree such mutations that do not alter amino acid sequences contribute to adaptive evolution. Here, we report the roles of these silent mutations in thermal adaptation of RNA bacteriophage Qβ based on experimental evolution during which Qβ showed adaptation to growth at an inhibitory temperature. Intriguingly, four synonymous mutations and one mutation in the untranslated region that spread widely in the Qβ population during the adaptation process at moderately high temperature provided a suitable genetic background to alter the fitness contribution of subsequent mutations from deleterious to beneficial at a higher temperature.

Dataset Information

The Single-Stranded RNA Bacteriophage Q? Adapts Rapidly to High Temperatures: An Evolution Experiment.

Publications

The Single-Stranded RNA Bacteriophage Qβ Adapts Rapidly to High Temperatures: An Evolution Experiment.

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