# Evolutionary bioenergetics of sporulation

## TL;DR

This paper calculates the energy cost of bacterial sporulation and explains when it is evolutionarily advantageous.

## Contribution

Quantifies the full ATP cost of sporulation and links it to evolutionary trade-offs and trait loss.

## Key findings

- Sporulation requires nearly 10^10 ATP and 10% of the bacterial energy budget.
- Translation, membrane synthesis, and protein turnover account for most of the energy cost.
- Sporulation is favored when harsh conditions last for months or longer.

## Abstract

Evolutionary bioenergetics examines how energetic constraints influence the origin, maintenance, and evolution of cellular components and organismal traits. It takes a bottom–up approach to quantifying the ATP required to assemble biological structures ranging from genes and membranes to virus particles, whole cells, and multicellular organisms. Here, we apply this framework to estimate the full energetic cost of making a bacterial endospore, one of the most abundant and persistent forms of life on Earth. By accounting for macromolecule synthesis, regulatory checkpoints, maternal investment, and subcellular coordination, we identify conditions under which sporulation is favored rather than alternative strategies and reveal the evolutionary forces that have driven the repeated loss of this complex trait across lineages over billions of years.

Energy is required for the expression and maintenance of complex traits. In many habitats, however, free energy available to support biosynthesis is in vanishingly short supply. As a result, many taxa have evolved persistence strategies that support survival in unfavorable environments. Among these is sporulation, an ancient bacterial program governed by a large genetic network that requires energy for both regulation and execution. Yet sporulation is a last resort, initiated when cellular energy is nearly exhausted. To resolve this paradox, we quantified the energetic cost of sporulation in units of ATP by integrating time-resolved genome, transcriptome, and proteome profiles. The full cost of the spore cycle, including both formation and revival, ranks among the most energy-intensive processes in the bacterial cell, requiring almost 1010 ATP and consuming about 10% of the total energy budget. The majority of this cost arises from translation, membrane synthesis, and protein turnover. Despite its considerable upfront investment, sporulation enables long-term survival and becomes optimal when harsh conditions extend over timescales of months or longer. This trade-off between immediate cost and delayed benefit helps explain when sporulation is maintained or replaced by alternative strategies. By incorporating our estimates into mechanistic models, we show how metabolic constraints shape sporulation efficiency, while genome-wide mutation accumulation data reveal that even modest energetic burdens can become visible to selection, influencing the evolutionary fate of this complex and widespread trait.