Rapid evolution in necromass use under resource limitation reduces persistence in producer-decomposer microbial...

Decomposer bacteria recycle necromass, the organic remnants of dead cells. This process underlies ecological system persistence via provisioning matter for future generations; however, it is unknown if more efficient necromass recycling also improves the persistence of the microbial ecosystem reliant upon it. Here, we utilize severely resource-limited conditions to force a decomposer bacterium, Escherichia coli, to grow using only its own necromass and subsequently use these adapted populations to test if improved necromass recycling ability contributes to longer persistence times of closed microbial biospheres. E. coli strain MC4100 was incubated in matter-closed systems in an isotonic saline solution without added nutrients for 60 days in spatially homogeneous or heterogeneous conditions. We observed phenotypic adaptive changes in E. coli populations, including improved growth on various carbon sources, loss of motility, and enhanced biofilm formation, which were specific to the spatial structure conditions. While these changes were beneficial for E. coli in monoculture, during co-culture with the alga Chlamydomonas reinhardtii, biospheres containing the adapted populations exhibited a 25% reduction in persistence under spatially heterogeneous conditions compared to those containing non-adapted E. coli populations. While nutrient cycling must occur for life in biospheres to self-sustain, enhanced recycling of necromass may actually undermine biosphere persistence.