Community assembly processes generate shifts in species abundances that influence ecosystem cycling of carbon and nutrients, yet our understanding of assembly remains largely separate from ecosystem-level functioning. In particular, subsurface groundwater-surface water mixing zones (hyporheic zones) are hotspots of biogeochemical activity, but assembly processes governing subsurface microbiomes remain a critical uncertainty in understanding hyporheic biogeochemistry.
Here, we sample two habitat types (i.e., attached and waterborne) through seasonal and sub-hourly fluctuations in groundwater-surface water mixing in the Columbia River corridor in eastern Washington State. We use ecological null modeling, co-occurrence network analysis, and temporally-explicit multivariate statistics to provide insight into microbiome biogeography in the hyporheic zone as well as assembly processes operating at discrete time scales to structure these microbiomes. Specifically, we investigate (a) biogeographical patterns in attached and waterborne microbiomes across three hydrologically-connected, physicochemically-distinct zones (inland hyporheic, nearshore hyporheic, and river); (b) assembly processes that generate these patterns; (c) groups of organisms that correspond to deterministic changes in the environment; and (d) correlations between these groups and hyporheic metabolism. Given dynamic hydrology in the nearshore hyporheic zone in particular, we further examine relationships between assembly and changes in microbial metabolism across space and time in these microbiomes.
Despite pronounced hydrologic connectivity throughout the hyporheic zone (and thus a strong potential for dispersal) we find that ecological selection deterministically governs microbiome composition within local environments, and we identify specific groups of organisms that correspond to seasonal changes in hydrology. In particular, we observe seasonal shifts from heterotrophic to autotrophic microorganisms associated with increases in selection from groundwater discharge. Also, the abundance of one statistical cluster of nearshore heterotrophic organisms increased with surface water intrusion, active biomass, and respiration, revealing organisms that may strongly influence hyporheic biogeochemistry.
Within the nearshore hyporheic zone, we demonstrate that multiple selective pressures (imposed by sediment and porewater physicochemistry) integrate to generate changes in microbiome composition at distinct timescales among habitat types. These changes in composition are reflective of contrasting associations of heterotrophic (Betaproteobacteria) and autotrophic (Thaumarchaeota) microorganisms with ecological selection and with seasonal changes in microbial metabolism.
Based on our results, we present a conceptual model in which metabolism increases when oscillating selective pressures oppose temporally stable selective pressures. Our conceptual model is pertinent to any ecosystem experiencing multiple selective pressures and presents an avenue for assimilating community assembly processes into predictions of ecosystem-level functioning.