Our proposed research seeks to understand the distribution, abundance, and diversity of life on
Earth and beyond by studying the evolution of microbial persistence traits (i.e., dormancy) under
extreme and fluctuating environmental conditions (i.e., energy limitation). We address this by
focusing on sporulation, an ancient trait found among diverse lineages in the Firmicutes. This
globally abundant phylum of bacteria plays a critical role in regulating biogeochemical cycles
across vast regions of Earth (Magnabosco et al. 2016). Spore formation allows some bacteria to
defy first-order constraints on maximum lifespan (Moger-Reischer and Lennon, In Review), while
facilitating dispersal around the globe (Hubert et al. 2009). Although complex traits are often
considered robust to perturbation, sporulation can rapidly be lost when it experiences conditions
that favor growth and reproduction. Our research will shed light on this problem using a
combination of theoretical modeling, laboratory experiments, and environmental metagenomics.
Objective 1: Based on first principles, we will estimate the bioenergetic cost of making a spore
by taking into account, among other things, ATP expenditures for synthesizing nucleotides,
ribonucleotides, and proteins that are encoded in up to 5 % of the Bacillus genome. With these
estimates, we will construct mechanistic simulation models that will generate predictions about
the energetic conditions that favor the evolutionary retention versus loss of sporulation.
Objective 2: Using an experimental evolution approach, we will quantify the genomic and
phenotypic rates of sporulation decay under contrasting energy regimes. Because spore-deficient
mutants can survive in energy-limited environments, we will identify alternate mechanisms of
persistence and assess how the modified fitness landscape influences trait refinement and the
degree of parallel evolution.
Objective 3: Leveraging large metagenomic databases, we will document the loss of sporulation
in in a range of ecosystems that are important for making inferences about the evolution of
dormancy in Early Earth history. Our phylogenetic approach will provide insight into the
persistence strategies of deep lineages that have recently been discovered, and test theoretical
predictions about how dormancy has affected diversification and rates of evolution.

NNH19ZDA001N-EXO

2019-11-22

2022-11-22