Environmental connectivity controls diversity in soil microbial communities

Abstract

Interspecific interactions are thought to govern the stability and functioning of microbial communities, but the influence of the spatial environment and its structural connectivity on the potential of such interactions to unfold remain largely unknown. Here we studied the effects on community growth and microbial diversity as a function of environmental connectivity, where we define environmental connectivity as the degree of habitat fragmentation preventing microbial cells from living together. We quantitatively compared growth of a naturally-derived high microbial diversity community from soil in a completely mixed liquid suspension (high connectivity) to growth in a massively fragmented and poorly connected environment (low connectivity). The low connectivity environment consisted of homogenously-sized miniature agarose beads containing random single or paired founder cells. We found that overall community growth was the same in both environments, but the low connectivity environment dramatically reduced global community-level diversity compared to the high connectivity environment. Experimental observations were supported by community growth modeling. The model predicts a loss of diversity in the low connectivity environment as a result of negative interspecific interactions becoming more dominant at small founder species numbers. Counterintuitively for the low connectivity environment, growth of isolated single genotypes was less productive than that of random founder genotype cell pairs, suggesting that the community as a whole profited from emerging positive interspecific interactions. Our work demonstrates the importance of environmental connectivity for growth of natural soil microbial communities, which aids future efforts to intervene in or restore community composition to achieve engineering and biotechnological objectives.

Reproducible Propagation of Species-Rich Soil Bacterial Communities Suggests Robust Underlying Deterministic Principles of Community Formation

“…Simulation of stochastic subsampling effects from a species-rich inoculum on the community composition after one week of growth. (A) Communities are randomly subsampled to 200,000 cells from a soil community distribution with n = 314 measured taxa and their relative abundances ( 25 ). Growth rates are assigned between 0.01–0.4 h −1 skewed by the log 10 -relative species abundance.…”

“…Interspecific interactions further emerge in dependency of initial growth conditions and environments ( 21 , 22 ), and with increasing species complexity, non-additive effects may arise ( 23 ). The emergence of interspecific interactions depends on the spatial distance between cells ( 24 ) and, consequently, may be different in highly fractured environments such as soil, as opposed to liquid suspension ( 25 – 28 ). The question is thus whether developmental paths of species-rich communities are inherently stochastic and, in that sense, mostly irreproducible, or whether their taxa-composition provides robust self-organizing properties that will only diverge as a result of differences in environmental boundary conditions.…”

Reproducible Propagation of Species-Rich Soil Microbiomes Suggests Robust Underlying Deterministic Principles of Community Formation

“…Soils are expected to provide unique ecological niches (1, 50), and their aggregates affect nutrient availability and gradients in electron donors and acceptors (26-28, 48, 51). Indeed, SynComs and NatComs maintained on average higher species diversity in soil microcosms than equivalent liquid cultures, suggesting emerging favorable dependencies, which permitted more phyla to sustain and grow (25). Suggestive for this is that members belonging to the Acidobacteria, Verrucomicrobia and Planctomycetes proliferated in all NatCom microcosms, whereas we did not manage to culture them individually using the same nutrient substrates.…”

“…Indeed, both NatCom and SynCom development seemed strongly determined by their starting taxa compositions, on top of which the environmental boundary conditions (i.e., soil versus liquid) influencing the community trajectories. The difference in compositional trajectories and states in soil and liquid, despite containing the same complex nutrient resource availability (soil extract), may be due to different types or magnitudes of interspecific interactions arising in the spatially structured, disconnected and heterogenous growth environment of the soil as opposed to the liquid-suspended growth (25). Soils are expected to provide unique ecological niches (1, 50), and their aggregates affect nutrient availability and gradients in electron donors and acceptors (26-28, 48, 51).…”

“…Interspecific interactions further emerge in dependency of initial growth conditions and environments (21,22), and with increasing species complexity, non-additive effects may arise (23). The emergence of interspecific interactions depends on the spatial distance between cells (24) and, consequently, may be different in highly fractured environments such as soil, as opposed to liquid suspension (25)(26)(27)(28). The question is thus whether developmental paths of species-rich communities are inherently stochastic and, in that sense, mostly irreproducible, or whether their taxa-composition provides robust self-organizing properties that will only diverge as a result of differences in environmental boundary conditions.…”