Overcoming toxicity: How nonantagonistic microbes manage to thrive in boom-and-bust environments

• 成果类型: Article
• 署名作者: Wang, Mingyi; Vladimirsky, Alexander; Giometto, Andrea
• 署名单位: Cornell University; Cornell University; Cornell University
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-11238
• DOI: 10.1073/pnas.2424372122
• 发表日期: 2025-07-01
• 关键词: antagonistic interactions; community dynamics; gut microbiota; killer toxin; bacteria; diversity; EVOLUTION; LIFE; COMPETITION; resilience

摘要

Antagonistic interactions are critical determinants of microbial community stability and composition, offering host benefits such as pathogen protection and providing avenues for antimicrobial control. While the ability to eliminate competitors confers an advantage to antagonistic microbes, it often incurs a fitness cost. Consequently, many microbes only produce toxins or engage in antagonistic behavior in response to specific cues like quorum sensing molecules or environmental stress. In laboratory settings, antagonistic microbes typically dominate over sensitive ones, raising the question why both antagonistic and nonantagonistic microbes are found in natural environments and host microbiomes. Here, using both theoretical models and experiments with killer strains of Saccharomyces cerevisiae, we show that boom-and-bust dynamics- periods of rapid growth punctuated by episodic mortality events-caused by temporal environmental fluctuations can favor nonantagonistic microbes that do not incur the growth rate cost of toxin production. Additionally, using control theory, we derive bounds on the competitive performance and identify optimal regulatory toxin-production strategies in various boom-and-bust environments where population dilutions occur either deterministically or stochastically over time. Our mathematical investigation reveals that optimal toxin regulation is much more beneficial to killers stochastic, rather than deterministic, boom-and-bust environments. Overall, our findings show how both antagonistic and nonantagonistic microbes can thrive under varying environmental conditions.