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Selective pressure causes an RNA virus to trade reproductive fitness for increased structural and thermal stability of a viral enzyme.

ABSTRACT: The modulation of fitness by single mutational substitutions during environmental change is the most fundamental consequence of natural selection. The antagonistic tradeoffs of pleiotropic mutations that can be selected under changing environments therefore lie at the foundation of evolutionary biology. However, the molecular basis of fitness tradeoffs is rarely determined in terms of how these pleiotropic mutations affect protein structure. Here we use an interdisciplinary approach to study how antagonistic pleiotropy and protein function dictate a fitness tradeoff. We challenged populations of an RNA virus, bacteriophage ?6, to evolve in a novel temperature environment where heat shock imposed extreme virus mortality. A single amino acid substitution in the viral lysin protein P5 (V207F) favored improved stability, and hence survival of challenged viruses, despite a concomitant tradeoff that decreased viral reproduction. This mutation increased the thermostability of P5. Crystal structures of wild-type, mutant, and ligand-bound P5 reveal the molecular basis of this thermostabilization--the Phe207 side chain fills a hydrophobic cavity that is unoccupied in the wild-type--and identify P5 as a lytic transglycosylase. The mutation did not reduce the enzymatic activity of P5, suggesting that the reproduction tradeoff stems from other factors such as inefficient capsid assembly or disassembly. Our study demonstrates how combining experimental evolution, biochemistry, and structural biology can identify the mechanisms that drive the antagonistic pleiotropic phenotypes of an individual point mutation in the classic evolutionary tug-of-war between survival and reproduction.

SUBMITTER: Dessau M

PROVIDER: S-EPMC3510033 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Selective pressure causes an RNA virus to trade reproductive fitness for increased structural and thermal stability of a viral enzyme.

Dessau Moshe M Goldhill Daniel D McBride Robert C R Turner Paul E PE Modis Yorgo Y

PLoS genetics 20121129 11

The modulation of fitness by single mutational substitutions during environmental change is the most fundamental consequence of natural selection. The antagonistic tradeoffs of pleiotropic mutations that can be selected under changing environments therefore lie at the foundation of evolutionary biology. However, the molecular basis of fitness tradeoffs is rarely determined in terms of how these pleiotropic mutations affect protein structure. Here we use an interdisciplinary approach to study how ...[more]

PMID: 23209446

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Project description:Copepod females invest a quantity of resources in their reproduction. Depending on several biotic and abiotic factors and their evolutionary history a trade-off can be commonly observed between producing a large number of smaller offspring or a small number of larger offspring. In this study, a multi-generational approach was applied to determine whether a trade-off between clutch size and egg size existed in the copepod Eurytemora affinis under different controlled conditions of temperature and salinity. This protocol was based on the follow-up of reproductive (Clutch Size 'CS', Egg Diameter 'ED') and morphological (Prosome Length 'PL') traits during several generations. Copepods were acclimated to cold (7 °C) and warm (20 °C) temperatures, and then their reproductive output was tested at the higher temperature of 24 °C. CS and ED were positively correlated to PL, so as a first step linear regressions between each reproductive trait and female PL were performed. The residuals from the regression lines of CS and ED with PL were calculated to remove the effect of female size. When the normalized data (residuals) of CS and ED plotted together a negative relationship between egg size and egg number revealed the existence of a trade-off. Copepod populations initially acclimated to cold temperature are commonly characterized by relatively smaller CS and larger ED. Conversely, warm temperature adapted females produced relatively larger CS and smaller ED. After transfer to a temperature of 24 °C, the ED did not change but the CS showed high variability indicating stressful conditions and no trade-off was observed. These observations suggest that E. affinis is able to modulate its reproduction depending on the encountered temperature. It seems that this copepod species can shift between a K- and an r-strategy in response to colder or warmer conditions. In a late winter-early spring like cold temperature, copepod females seem to invest more on offspring quality by producing relatively larger eggs. This ecological strategy ensures a high recruitment of the spring generation that is responsible for the strength of the maximum population size usually observed in late spring-early summer (May-June). To the contrary, at summer-like temperature, where the population density decreases significantly in the Seine estuary, copepod females seem to switch from K to r strategy by favoring offspring number compared to offspring size. Finally, the use of a higher temperature of 24 °C seems to disrupt the observed reproductive trade-off even after several generations. These results suggest that a switching between K- or r-strategy of E. affinis depends highly on temperature effects. The effect of salinity increase during a summer-like temperature of 20 °C as well as after transfer to 24 °C decreased PL and CS but the ED did not change significantly.

Dataset Information

Selective pressure causes an RNA virus to trade reproductive fitness for increased structural and thermal stability of a viral enzyme.

Publications

Selective pressure causes an RNA virus to trade reproductive fitness for increased structural and thermal stability of a viral enzyme.

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