Bacterial Community Composition of Stream Biofilms in Spatially Variable-Flow Environments

Streams are highly heterogeneous ecosystems, in terms of both geomorphology and hydrodynamics. While flow is recognized to shape the physical architecture of benthic biofilms, we do not yet understand what drives community assembly and biodiversity of benthic biofilms in the heterogeneous flow landscapes of streams. Within a metacommunity ecology framework, we experimented with streambed landscapes constructed from bedforms in large-scale flumes to illuminate the role of spatial flow heterogeneity in biofilm community composition and biodiversity in streams. Our results show that the spatial variation of hydrodynamics explained a remarkable percentage (up to 47%) of the variation in community composition along bedforms. This suggests species sorting as a model of metacommunity dynamics in stream biofilms, though natural biofilm communities will clearly not conform to a single model offered by metacommunity ecology. The spatial variation induced by the hydrodynamics along the bedforms resulted in a gradient of bacterial beta diversity, measured by a range of diversity and similarity indices, that increased with bedform height and hence with spatial flow heterogeneity at the flume level. Our results underscore the necessity to maintain small-scale physical heterogeneity for community composition and biodiversity of biofilms in stream ecosystems.Biofilms (attached and matrix-enclosed microbial communities) are an important form of microbial life in streams and rivers, where they can greatly contribute to ecosystem functions and even large-scale carbon fluxes (1, 3). Streams are inherently heterogeneous and are characterized by a largely unidirectional downstream flow of water that controls the dispersal of suspended microorganisms (21), biofilm community composition (7), architecture (2), and metabolism (13), for instance. However, we do not understand how diverse microorganisms assemble into biofilm communities based on flow heterogeneity and related dispersal in these ecosystems.Dispersal, as the propagation and immigration of biota, can have important consequences for biodiversity and ecosystem functioning in heterogeneous landscapes (18, 25). Landscape topography and turbulent transport affect dispersal, a relationship that is well studied in the dispersal of plant seeds (31) but not in the microbial world. Only recently have microbial ecologists begun to understand the role of dispersal in large-scale biogeographic patterns (29) and metacommunity ecology (24, 44). This growing body of research on microbial dispersal and its consequences for spatial patterns of community assembly and composition rests entirely on free-living bacteria, while no comparable data exist for microbial biofilms. The confirmation of detachment as an intrinsic behavior in many biofilms has led to the appreciation of dispersal as an insurance policy for these microbial communities to seed new habitats during resource limitation or aging of the parental biofilm (4). However, microbial ecology lacks conceptual models to predict postemigration processes, such as cell propagation, immigration, and community assembly during colonization of new surfaces. The perception of biofilms as microbial landscapes and, at the same time, as integrated parts of the landscape they inhabit offers the possibility to test models for habitat selection by dispersal cells (4). In this study, we focused on the assembly of biofilm communities by dispersal cells in spatially variable-flow environments; we did not measure dispersal as the emigration of cells from established biofilms. We adopted metacommunity ecology as a framework that encapsulates environmental heterogeneity and dispersal (18) to illuminate the mechanisms underlying community assembly.If the effects of microbial diversity on ecosystem functions are to be understood, we need to address the proper spatial resolution at which microorganisms assemble into communities and at which their functioning becomes manifest. In streams, this is typically at the level of habitats and microhabitats ranging from meters to centimeters, where characteristic geomorphological features (e.g., bedforms) and induced hydrodynamic fields develop and where spatial variations in biofilm metabolism become apparent (13). The ensemble of these small-scale variations translates into the landscape heterogeneity of the streambed.The aim of this study was to test whether spatial flow heterogeneity generating diverse microhabitats induces spatial species turnover and increases the biodiversity of microbial biofilms. Microbial metacommunity ecology predicts mass effects rather than species sorting to drive community composition in ecosystems with low residence time, such as streams (14, 18, 24). To test this prediction, we constructed six streambed landscapes from bedforms of defined dimensions differing in height; the mean flow (at flume scale) was kept constant, whereas the spatial heterogeneity of flow increased across the gradient of the six landscapes. The inoculum (i.e., the stream water and naturally contained microorganisms) and water chemistry were equal in all flumes. This allowed us to isolate flow heterogeneity as a potential driver of biofilm community composition in a high-energy ecosystem. We used terminal restriction fragment length polymorphism (T-RFLP) analysis of bacterial 16S rRNA gene sequences from winter and summer communities and related bacterial community composition and microbial biomass to the hydrodynamics in representative microhabitats using causal modeling and forward selection of explanatory variables (9, 23).