A spore quality\u2013quantity tradeoff favors diverse sporulation strategies in Bacillus subtilis

Alper Mutlu,Nils Becker,Ilka B Bischofs,Charlotte Kaspar

doi:10.1038/s41396-020-0721-4

Abstract

Quality–quantity tradeoffs govern the production of propagules across taxa and can explain variability in life-history traits in higher organisms. A quality–quantity tradeoff was recently discovered in spore forming bacteria, but whether it impacts fitness is unclear. Here we show both theoretically and experimentally that the nutrient supply during spore revival determines the fitness advantage associated with different sporulation behaviors in Bacillus subtilis. By tuning sporulation rates we generate spore-yield and spore-quality strategists that compete with each other in a microscopic life-cycle assay. The quality (yield) strategist is favored when spore revival is triggered by poor (rich) nutrients. We also show that natural isolates from the gut and soil employ different life-cycle strategies that result from genomic variations in the number of rap-phr signaling systems. Taken together, our results suggest that a spore quality–quantity tradeoff contributes to the evolutionary adaptation of sporulating bacteria.

Highlights

Endospores of the model organism Bacillus subtilis have been isolated from almost every niche on Earth, but primarily from the soil and from the gut flora of organisms that feed directly from the ground, including chickens, pigs, mice, and humans [1]
Guided by a theoretical model of the spore quality–quantity tradeoff in B. subtilis, we show experimentally that the nutrient supply during spore revival determines the fitness advantage associated with different sporulation behaviors, in both a synthetic model with a tunable life-cycle strategy and in natural isolates from the soil and the chicken gut, respectively
The model is informed by recent findings on a spore quality–quantity tradeoff in a B. subtilis laboratory strain [30], and was extended to incorporate plausible assumptions for the mechanism of revival based on additional experimental data that investigate the role of alanine dehydrogenase (Ald) in the metabolism of the germinated spore (Fig. S1, see Supplementary text for details)

Summary

Introduction

Endospores of the model organism Bacillus subtilis have been isolated from almost every niche on Earth, but primarily from the soil and from the gut flora of organisms that (partially) feed directly from the ground, including chickens, pigs, mice, and humans [1]. B. subtilis sporulates both in the rhizosphere environment of soil [2] and in the gut [3,4,5], and spores revive there [2, 5, 6]. Diverse natural isolates have been characterized, and it was noted repeatedly that their sporulation kinetics is strikingly

Methods

Results

Conclusion