Biofilm formation is controlled by an array of coupled physical, chemical, and biotic processes. Despite the ecological relevance of microbial biofilms, their community formation and succession remain poorly understood. We investigated the effect of flow velocity, as the major physical force in stream ecosystems, on biofilm community succession (as continuous shifts in community composition) in microcosms under laminar, intermediate, and turbulent flow. Flow clearly shaped the development of biofilm architecture and community composition, as revealed by microscopic investigation, denaturing gradient gel electrophoresis (DGGE) analysis, and sequencing. While biofilm growth patterns were undirected under laminar flow, they were clearly directed into ridges and conspicuous streamers under turbulent flow. A total of 51 biofilm DGGE bands were detected; the average number ranged from 13 to 16. Successional trajectories diverged from an initial community that was common in all flow treatments and increasingly converged as biofilms matured. We suggest that this developmental pattern was primarily driven by algae, which, as "ecosystem engineers," modulate their microenvironment to create similar architectures and flow conditions in all treatments and thereby reduce the physical effect of flow on biofilms. Our results thus suggest a shift from a predominantly physical control to coupled biophysical controls on bacterial community succession in stream biofilms.
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 postemigratio...
BackgroundEvidence increasingly shows that stream ecosystems greatly contribute to global carbon fluxes. This involves a tight coupling between biofilms, the dominant form of microbial life in streams, and dissolved organic carbon (DOC), a very significant pool of organic carbon on Earth. Yet, the interactions between microbial biodiversity and the molecular diversity of resource use are poorly understood.Methodology/Principal FindingsUsing six 40-m-long streamside flumes, we created a gradient of streambed landscapes with increasing spatial flow heterogeneity to assess how physical heterogeneity, inherent to streams, affects biofilm diversity and DOC use. We determined bacterial biodiversity in all six landscapes using 16S-rRNA fingerprinting and measured carbon uptake from glucose and DOC experimentally injected to all six flumes. The diversity of DOC molecules removed from the water was determined from ultrahigh-resolution Fourier Transform Ion Cyclotron Resonance mass spectrometry (FTICR-MS). Bacterial beta diversity, glucose and DOC uptake, and the molecular diversity of DOC use all increased with increasing flow heterogeneity. Causal modeling and path analyses of the experimental data revealed that the uptake of glucose was largely driven by physical processes related to flow heterogeneity, whereas biodiversity effects, such as complementarity, most likely contributed to the enhanced uptake of putatively recalcitrant DOC compounds in the streambeds with higher flow heterogeneity.Conclusions/SignificanceOur results suggest biophysical mechanisms, including hydrodynamics and microbial complementarity effects, through which physical heterogeneity induces changes of resource use and carbon fluxes in streams. These findings highlight the importance of fine-scale streambed heterogeneity for microbial biodiversity and ecosystem functioning in streams, where homogenization and loss of habitats increasingly reduce biodiversity.
Laboratory studies have documented the extensive architectural differentiation of biofilms into complex structures, including filamentous streamers generated by turbulent flow. Still, it remains elusive whether this spatial organization of natural biofilms is reflected in the community structure. We analyzed bacterial community differentiation between the base and streamers (filamentous structures floating in the water) of stream biofilms under various flow conditions using denaturing gradient gel electrophoresis (DGGE) and sequencing. Fourth-corner analysis showed pronounced deviation from random community structure suggesting that streamers constitute a more competitive zone within the biofilm than its base. The same analysis also showed members of the a-Proteobacteria and Gemmatimonadetes to preferentially colonize the biofilm base, whereas b-Proteobacteria and Bacteroidetes were comparatively strong competitors in the streamers. We suggest this micro-scale differentiation as a response to the environmental dynamics in natural ecosystems. The ISME Journal (
The temporal variability of streamflow is known to be a key feature structuring and controlling fluvial ecological communities and ecosystem processes. Although alterations of streamflow regime due to habitat fragmentation or other anthropogenic factors are ubiquitous, a quantitative understanding of their implications on ecosystem structure and function is far from complete. Here, by experimenting with two contrasting flow regimes in stream microcosms, we provide a novel mechanistic explanation for how fluctuating flow regimes may affect grazing of phototrophic biofilms (i.e., periphyton) by an invertebrate species (Ecdyonurus sp.). In both flow regimes light availability was manipulated as a control on autotroph biofilm productivity and grazer activity, thereby allowing the test of flow regime effects across various ratios of biofilm biomass to grazing activity. Average grazing rates were significantly enhanced under variable flow conditions and this effect was highest at intermediate light availability. Our results suggest that stochastic flow regimes, characterised by suitable fluctuations and temporal persistence, may offer increased windows of opportunity for grazing under favourable shear stress conditions. This bears important implications for the development of comprehensive schemes for water resources management and for the understanding of trophic carbon transfer in stream food webs.
Biofilms represent the dominant form of microbial life in stream ecosystems. Research of complex environmental biofilms requires appropriate cultivation techniques to address questions central to biofilm structure-functioncoupling and ecosystem implications. Whereas the cultivation of medical and industrial biofilms has received considerable attention, cultivation devices for environmental biofilms have not. Here we describe and systematically assess the reproducibility of laboratory-based microcosms that allow the study of the structure and function of stream biofilms under different flow regimes. Microcosms were assembled from 1.3-m-long Plexiglas flumes fed with water that recirculated between a header tank and a sink. Each flume was paved with 104 individual unglazed ceramic coupons that served as growth substratum. We operated 3 microcosms designed to simulate laminar, transitional, and turbulent flow. Each microcosm consisted of two duplicate sets of flumes where two flumes shared the same water. We monitored biofilm coverage, bacterial abundance, and chlorophyll a as bulk biomass parameters over a growth period of 28 days and tested for community composition shifts using denaturing gradient gel electrophoresis (DGGE). Based on these variables, we assessed the reproducibility at different levels of microcosm assembly: (1) within individual flumes (i.e., longitudinal gradients), (2) within a shared water body, and (3) within flow regime treatments. Our results revealed good reproducibility at the various levels of the experimental setup and suggest microcosm flumes as highly valuable tools for biofilm studies with multitreatment and multireference designs.
Ecology, with a traditional focus on plants and animals, seeks to understand the mechanisms underlying structure and dynamics of communities. In microbial ecology, the focus is changing from planktonic communities to attached biofilms that dominate microbial life in numerous systems. Therefore, interest in the structure and function of biofilms is on the rise. Biofilms can form reproducible physical structures (i.e. architecture) at the millimetre-scale, which are central to their functioning. However, the spatial dynamics of the clusters conferring physical structure to biofilms remains often elusive. By experimenting with complex microbial communities forming biofilms in contrasting hydrodynamic microenvironments in stream mesocosms, we show that morphogenesis results in ‘ripple-like’ and ‘star-like’ architectures – as they have also been reported from monospecies bacterial biofilms, for instance. To explore the potential contribution of demographic processes to these architectures, we propose a size-structured population model to simulate the dynamics of biofilm growth and cluster size distribution. Our findings establish that basic physical and demographic processes are key forces that shape apparently universal biofilm architectures as they occur in diverse microbial but also in single-species bacterial biofilms.
Biofilms dominate microbial life in numerous aquatic ecosystems, and in engineered and medical systems, as well. The formation of biofilms is initiated by single primary cells colonizing surfaces from the bulk liquid. The next steps from primary cells towards the first cell clusters as the initial step of biofilm formation remain relatively poorly studied. Clonal growth and random migration of primary cells are traditionally considered as the dominant processes leading to organized microcolonies in laboratory grown monocultures. Using Voronoi tessellation, we show that the spatial distribution of primary cells colonizing initially sterile surfaces from natural streamwater community deviates from uniform randomness already during the very early colonisation. The deviation from uniform randomness increased with colonisation — despite the absence of cell reproduction — and was even more pronounced when the flow of water above biofilms was multidirectional and shear stress elevated. We propose a simple mechanistic model that captures interactions, such as cell-to-cell signalling or chemical surface conditioning, to simulate the observed distribution patterns. Model predictions match empirical observations reasonably well, highlighting the role of biotic interactions even already during very early biofilm formation despite few and distant cells. The transition from single primary cells to clustering accelerated by biotic interactions rather than by reproduction may be particularly advantageous in harsh environments — the rule rather than the exception outside the laboratory.
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