Katharina Besemer

Biophysical controls on community succession in stream biofilms.

ABSTRACT 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.

The ecology and biogeochemistry of stream biofilms.

Streams and rivers form dense networks, shape the Earths surface and, in their sediments, provide an immensely large surface area for microbial growth. Biofilms dominate microbial life in streams and rivers, drive crucial ecosystem processes and contribute substantially to global biogeochemical fluxes. In turn, water flow and related deliveries of nutrients and organic matter to biofilms constitute major constraints on microbial life. In this Review, we describe the ecology and biogeochemistry of stream biofilms and highlight the influence of physical and ecological processes on their structure and function. Recent advances in the study of biofilm ecology may pave the way towards a mechanistic understanding of the effects of climate and environmental change on stream biofilms and the biogeochemistry of stream ecosystems.

Unraveling assembly of stream biofilm communities.

Microbial biofilms assemble from cells that attach to a surface, where they develop into matrix-enclosed communities. Mechanistic insights into community assembly are crucial to better understand the functioning of natural biofilms, which drive key ecosystem processes in numerous aquatic habitats. We studied the role of the suspended microbial community as the source of the biofilm community in three streams using terminal-restriction fragment length polymorphism and 454 pyrosequencing of the 16S ribosomal RNA (rRNA) and the 16S rRNA gene (as a measure for the active and the bulk community, respectively). Diversity was consistently lower in the biofilm communities than in the suspended stream water communities. We propose that the higher diversity in the suspended communities is supported by continuous inflow from various sources within the catchment. Community composition clearly differed between biofilms and suspended communities, whereas biofilm communities were similar in all three streams. This suggests that biofilm assembly did not simply reflect differences in the source communities, but that certain microbial groups from the source community proliferate in the biofilm. We compared the biofilm communities with random samples of the respective community suspended in the stream water. This analysis confirmed that stochastic dispersal from the source community was unlikely to shape the observed community composition of the biofilms, in support of species sorting as a major biofilm assembly mechanism. Bulk and active populations generated comparable patterns of community composition in the biofilms and the suspended communities, which suggests similar assembly controls on these populations.

Headwaters are critical reservoirs of microbial diversity for fluvial networks

Streams and rivers form conspicuous networks on the Earth and are among natures most effective integrators. Their dendritic structure reaches into the terrestrial landscape and accumulates water and sediment en route from abundant headwater streams to a single river mouth. The prevailing view over the last decades has been that biological diversity also accumulates downstream. Here, we show that this pattern does not hold for fluvial biofilms, which are the dominant mode of microbial life in streams and rivers and which fulfil critical ecosystem functions therein. Using 454 pyrosequencing on benthic biofilms from 114 streams, we found that microbial diversity decreased from headwaters downstream and especially at confluences. We suggest that the local environment and biotic interactions may modify the influence of metacommunity connectivity on local biofilm biodiversity throughout the network. In addition, there was a high degree of variability in species composition among headwater streams that could not be explained by geographical distance between catchments. This suggests that the dendritic nature of fluvial networks constrains the distributional patterns of microbial diversity similar to that of animals. Our observations highlight the contributions that headwaters make in the maintenance of microbial biodiversity in fluvial networks.

Microbial biodiversity in glacier-fed streams

While glaciers become increasingly recognised as a habitat for diverse and active microbial communities, effects of their climate change-induced retreat on the microbial ecology of glacier-fed streams remain elusive. Understanding the effect of climate change on microorganisms in these ecosystems is crucial given that microbial biofilms control numerous stream ecosystem processes with potential implications for downstream biodiversity and biogeochemistry. Here, using a space-for-time substitution approach across 26 Alpine glaciers, we show how microbial community composition and diversity, based on 454-pyrosequencing of the 16S rRNA gene, in biofilms of glacier-fed streams may change as glaciers recede. Variations in streamwater geochemistry correlated with biofilm community composition, even at the phylum level. The most dominant phyla detected in glacial habitats were Proteobacteria, Bacteroidetes, Actinobacteria and Cyanobacteria/chloroplasts. Microorganisms from ice had the lowest α diversity and contributed marginally to biofilm and streamwater community composition. Rather, streamwater apparently collected microorganisms from various glacial and non-glacial sources forming the upstream metacommunity, thereby achieving the highest α diversity. Biofilms in the glacier-fed streams had intermediate α diversity and species sorting by local environmental conditions likely shaped their community composition. α diversity of streamwater and biofilm communities decreased with elevation, possibly reflecting less diverse sources of microorganisms upstream in the catchment. In contrast, β diversity of biofilms decreased with increasing streamwater temperature, suggesting that glacier retreat may contribute to the homogenisation of microbial communities among glacier-fed streams.

Fluvial network organization imprints on microbial co-occurrence networks

Significance Microbial communities orchestrate most biogeochemical processes on Earth. In streams and rivers, surface-attached and matrix-enclosed biofilms dominate microbial life. Despite the relevance of these biofilms for ecosystem processes (e.g., metabolism and nutrient cycling), it remains unclear how features inherent to stream and river networks affect the fundamental organization of biofilm communities in these ecosystems. We combined co-occurrence analyses of biofilms based on next-generation sequencing with a probabilistic hydrological model, and showed how fragementation of microbial co-occurrence networks change across stream networks. Our analyses offer potential insights into the response of microbial community organization and persistence to human pressures that increasingly change the hydrological regime and biodiversity dynamics in fluvial networks. Recent studies highlight linkages among the architecture of ecological networks, their persistence facing environmental disturbance, and the related patterns of biodiversity. A hitherto unresolved question is whether the structure of the landscape inhabited by organisms leaves an imprint on their ecological networks. We analyzed, based on pyrosequencing profiling of the biofilm communities in 114 streams, how features inherent to fluvial networks affect the co-occurrence networks that the microorganisms form in these biofilms. Our findings suggest that hydrology and metacommunity dynamics, both changing predictably across fluvial networks, affect the fragmentation of the microbial co-occurrence networks throughout the fluvial network. The loss of taxa from co-occurrence networks demonstrates that the removal of gatekeepers disproportionately contributed to network fragmentation, which has potential implications for the functions biofilms fulfill in stream ecosystems. Our findings are critical because of increased anthropogenic pressures deteriorating stream ecosystem integrity and biodiversity.

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

ABSTRACT 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.

Physical heterogeneity increases biofilm resource use and its molecular diversity in stream mesocosms.

Background Evidence 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 Findings Using 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/Significance Our 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.

Complexity of bacterial communities in a river-floodplain system (Danube, Austria)

ABSTRACT Natural floodplains play an essential role in the processing and decomposition of organic matter and in the self-purification ability of rivers, largely due to the activity of bacteria. Knowledge about the composition of bacterial communities and its impact on organic-matter cycling is crucial for the understanding of ecological processes in river-floodplain systems. Particle-associated and free-living bacterial assemblages from the Danube River and various floodplain pools with different hydrological characteristics were investigated using terminal restriction fragment length polymorphism analysis. The particle-associated bacterial community exhibited a higher number of operational taxonomic units (OTUs) and was more heterogeneous in time and space than the free-living community. The temporal dynamics of the community structure were generally higher in isolated floodplain pools. The community structures of the river and the various floodplain pools, as well as those of the particle-associated and free-living bacteria, differed significantly. The compositional dynamics of the planktonic bacterial communities were related to changes in the algal biomass, temperature, and concentrations of organic and inorganic nutrients. The OTU richness of the free-living community was correlated with the concentration and origin of organic matter and the concentration of inorganic nutrients, while no correlation with the OTU richness of the particle-associated assemblage was found. Our results demonstrate the importance of the river-floodplain interactions and the influence of damming and regulation on the bacterial-community composition.

Architectural differentiation reflects bacterial community structure in stream biofilms.

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 α-Proteobacteria and Gemmatimonadetes to preferentially colonize the biofilm base, whereas β-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.