Metabolic insight into bacterial community assembly across ecosystem boundaries

Nathan I. Wisnoski, WyGISC, University of Wyoming, Laramie, WY, Mario E. Muscarella, University of Alaska Fairbanks, Megan L. Larsen, Phylagen, San Francisco, CA, Ariane L. Peralta, Department of Biology, East Carolina University, Greenville, NC and Jay T. Lennon, Department of Biology, Indiana University, Bloomington, IN

Background/Question/Methods
Material fluxes across habitat boundaries can have important consequences for the structure and function of recipient ecosystems. At the terrestrial-aquatic interface, spatial subsidies of terrestrial-derived organic matter can also be coupled with the transport of large quantities of microorganisms into aquatic ecosystems. Such high rates of cross-boundary dispersal are thought to maintain sink populations of terrestrial-derived bacteria, but the abrupt change in environmental conditions could filter out many taxa poorly adapted to aquatic environments. However, many bacteria have evolved life history strategies (e.g., dormancy, slow growth) that could buffer against the suboptimal conditions associated with the transition between habitats. As such, the fate of terrestrial-derived bacteria in aquatic ecosystems and their implications for community assembly remain unclear.
In this study, we explored microbial community assembly along a hydrological flow path of a small reservoir. We collected surface water samples along a transect of University Lake, Bloomington, IN, USA, and characterized the composition of total and active portions of the bacterial community by sequencing 16S rRNA genes (DNA) and transcripts (RNA), respectively. We then compared patterns of diversity in the reservoir to the composition of nearby terrestrial soil communities that may serve as source communities for aquatic community assembly.
Results/Conclusions
When metabolic heterogeneity was ignored (i.e., using DNA-based assessments), our data were consistent with views that cross-boundary dispersal is important for structuring aquatic bacterial communities. That is, we found elevated richness and increased compositional similarity to nearby soils in the aquatic community, but these effects were localized near the terrestrial-aquatic interface. In contrast, we found evidence for strong species sorting in the active portion of the aquatic community (inferred from RNA). The active community was consistently less diverse and highly dissimilar in composition to the nearby soil community. The vast majority of terrestrial-derived bacteria detected in the aquatic community were never detected in a metabolically active state. However, some taxa were detected in an active state in the aquatic habitat. Of these active terrestrial-derived bacteria, some became less common with distance from the terrestrial-aquatic interface (potentially indicating a reliance on dispersal for persistence), while others became more abundant (potentially indicating successful colonization).
Taken together, these patterns suggest that dispersal may play a weaker role than previously thought relative to other persistence strategies, like dormancy, during aquatic community assembly. By accounting for metabolic heterogeneity in complex communities, our findings clarify the roles of local- and regional-scale assembly processes in terrestrial-aquatic meta-ecosystems.