ena-STUDY-Swiss Federal Institute of Aquatic Science and Technology - Eawag-14-02-2021-19:41:10:152-845
Initial community composition determines the long-term fate and phenotypic trajectory of a microbial cross-feeding interaction
Sequential metabolism is common; most biosynthetic pathways are multi-step enzymatic reactions including many global biogeochemical processes such as the nitrogen cycle. Ideally, a cell would retain intermediates within the cell, while higher fluxes through subsequent enzymatic steps would prevent intermediates from reaching toxic levels. Alternatively, a cell could release excess intermediates and utilize them at a later point, or allow them to be consumed by neighboring cells with complementary metabolism. Albeit counterintuitive, such 'division of labor' may be detrimental for community diversity over longer timespans. Whenever present, generalist cells that retain intermediates and perform the entire metabolic pathway would gain more energy per unit substrate and possibly outcompete specialist cells within mixed communities.We experimentally explored the consequences of metabolic strategies on community diversity and evolution. We assembled isogenic Pseudomonas stutzeri knockout mutants that are partial (specialists) or complete (generalists) denitrifiers into synthetic communities and allowed them to compete and evolve together in mineral medium. Competition between a denitrifying generalist and a nitrite specialist resulted in frequency convergence regardless of starting frequencies, demonstrating that different metabolic strategies can co-exist provided sufficient exogenous accumulation of the intermediate substrate (nitrite). Later on, however, the generalist evolved streamlined metabolism where intermediates no longer accumulated and outcompeted the nitrite specialists. Such response, however, only takes place when nitrite specialists are initially absent or rare. Our results indicate that during colonization, early transient conditions can have major impacts on diversity, and that in some cases competition may prevent species radiation and thus slow evolutionary responses.
Sequential metabolism is common; most biosynthetic pathways are multi-step enzymatic reactions including many global biogeochemical processes such as the nitrogen cycle. Ideally, a cell would retain intermediates within the cell, while higher fluxes through subsequent enzymatic steps would prevent intermediates from reaching toxic levels. Alternatively, a cell could release excess intermediates and utilize them at a later point, or allow them to be consumed by neighboring cells with complementary metabolism. Albeit counterintuitive, such 'division of labor' may be detrimental for community diversity over longer timespans. Whenever present, generalist cells that retain intermediates and perform the entire metabolic pathway would gain more energy per unit substrate and possibly outcompete specialist cells within mixed communities.We experimentally explored the consequences of metabolic strategies on community diversity and evolution. We assembled isogenic Pseudomonas stutzeri knockout mutants that are partial (specialists) or complete (generalists) denitrifiers into synthetic communities and allowed them to compete and evolve together in mineral medium. Competition between a denitrifying generalist and a nitrite specialist resulted in frequency convergence regardless of starting frequencies, demonstrating that different metabolic strategies can co-exist provided sufficient exogenous accumulation of the intermediate substrate (nitrite). Later on, however, the generalist evolved streamlined metabolism where intermediates no longer accumulated and outcompeted the nitrite specialists. Such response, however, only takes place when nitrite specialists are initially absent or rare. Our results indicate that during colonization, early transient conditions can have major impacts on diversity, and that in some cases competition may prevent species radiation and thus slow evolutionary responses.