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Dryad

Energy allocation explains how protozoan metabolic traits adapt to temperature and nutrient supply

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Mar 15, 2024 version files 186.33 MB
Mar 15, 2024 version files 186.33 MB
Mar 15, 2024 version files 186.33 MB

Abstract

To survive and reproduce, living organisms need to maintain an efficient balance between energy intake and energy expenditure. When the environment changes, a previously efficient energy allocation strategy may become inefficient in the new environment, and organisms are required to change their physiology, morphology, and behaviour. However, how multiple phenotypic traits interact with each other and with the characteristics of the environment to determine energy allocation is poorly understood. To address this knowledge gap, we develop a predictive framework, based on energetic and biophysical principles, to characterise phenotype-environment interactions. We tested this by adapting axenic populations of the ciliate Tetrahymena pyriformis to different environmental conditions of temperature and resource levels and measured population growth, cell size, respiration, and movement. Movement speed and respiration rate increased with acute changes in environmental temperature in a way that could be predicted from simple physical scaling relations such as the Boltzmann-Arrhenius equation and the `viscous drag impacting movement. Based on theoretical arguments, we argue that these short-term changes in metabolic rate and movement speed introduce a mismatch between energy intake and energy expenditure and are not sustainable in the long term. In fact, by around 3.5 days after the introduction of Tetrahymena into a novel environment, all measured quantities were further modulated in a direction that likely restored the energy allocation balance of the cells. Changes in cell size played a substantial role in mediating these adaptations, by simultaneously affecting multiple phenotypic traits, such as metabolic rate and the energetic costs of movement. In a small microbial consumer like Tetrahymena, size changes can happen over rapid timescales, relative to the timescales of ecological changes and of seasonal environmental fluctuations. Changes in body size can therefore be effectively leveraged -- alongside physiological and biochemical regulations -- to cope with environmental changes.