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

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.