Microcalorimetry reveals bacterial motility as an expensive trait during starvation

Quantifying the energetic costs of cellular traits is important to understand their evolutionary constraints and ecological function. However, direct measurements of energy expenditure of distinct traits are rare. Here, we present direct measurements of the power dissipation due to bacterial flagellar motility using microcalorimetry, based on measuring the power dissipation of a motile population and a non-motile mutant. For the single-flagellated marine bacterium Vibrio coralliilyticus , we determined the power dissipated by motility in cultures to be 0.91 µW/mL/OD. Per swimming cell this amounts to 2.0 ×10 − 15 W, or a turnover of 2.5 ×10 4 ATP molecules per second. The power dissipated for motility equals 35 % of total metabolism during starvation, indicating this is likely the most expensive cellular trait during starvation. The dissipation for motility is in good agreement with that predicted using resistive force theory, indicating that any thermodynamic inefficiencies upstream of the flagellar motor, such as metabolic inefficiencies, are small. We further show that the multiflagellated bacterium Escherichia coli dissipates 0.70 µW/mL/OD when in motility buffer, comparable to marine bacteria despite the much lower swimming speed, and hence indicating lower efficiency of swimming. Finally, we show that the energy spent by Vibrio coralliilyticus on motility can have major consequences on their survival under starvation, causing a 50 % reduction in survival of a motile wild type relative to a non-motile mutant after 3 weeks of starvation. These results reveal the large costs involved in an individual trait that shapes microbial life in heterogeneous environments. Significance Many bacteria live in heterogeneous environments where they use motility and chemotaxis to locate nutrient hotspots or hosts amid nutrient-poor waters. The energetics of this search process has not been measured directly. Here we use calorimetric measurements of cultures of swimming and non-swimming bacterial populations to measure the energy expenditure of motility and compare with theoretical predictions. We show that bacterial motility is among the most expensive cellular traits under starvation conditions, accounting for 35% of all metabolic costs. Quantifying the energetic cost of cellular traits helps understanding behavioral trade-offs and energy allocation in natural environments.