Spatial structure affects the establishment and persistence of closed microbial ecosystems

Why Earth has remained habitable for billions of years is a question that has long fostered debate in biology and earth sciences. Closed systems approaches have yielded information about the underlying mechanisms, including the persistence of matter recycling. However, the majority of these studies have been conducted under relatively homogenous conditions using aquatic systems. Here, we investigated the effect of spatial structure and heterogeneity on the persistence or failure of closed microbial biospheres. This mimics unsaturated soil-like conditions that were inoculated with a two species producer-decomposer community. Specifically, we investigated how microhabitat physical structure and necromass spatial distribution affected population dynamics and system time-to-failure. We observed strong effects of microhabitat structure, including particle size and moisture level, on persistence at both the population and system levels. Systems containing the smallest substrate particles failed quickly and on average did not support decomposer populations except at high initial cell densities. Persistence was promoted by larger substrate particles, likely due to larger pore sizes resulting in shorter movement distances and better accessibility to resource patches (i.e. necromass). Building on these findings, we manipulated necromass patch distribution and observed that algae clustered around necromass patches when present. Necromass patch distribution had small but significant effects on persistence, with lower persistence in intermediate vs. high or low necromass heterogeneity. Together these findings indicate a limit to the spatial/physical parameter space in which producer-decomposer communities can establish and self-sustain via self-recycling of necromass.