Architectural differentiation reflects bacterial community structure in stream biofilms

Besemer, Katharina; Hödl, Iris; Singer, Gabriel; Battin, Tom J.

doi:10.1038/ismej.2009.73

Cited by 46 publications

(49 citation statements)

References 26 publications

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“…This is supported by findings suggesting that niche differentiation and competition are processes responsible for shifts in community composition in streamers 40 .…”

Section: Biodiversity Across Spatial Scalessupporting

confidence: 55%

supporting

confidence: 55%

“…These data suggest that the Proteobacteria Furthermore, depending on the turbulence of the water overlying the biofilms, the biofilm canopy can differentiate into streamers (see below), which can entail microscale shifts in bacterial community composition. This is supported by findings suggesting that niche differentiation and competition are processes responsible for shifts in community composition in streamers 40 .At an intermediate scale (that is, centimetres to metres), the interplay between streambed geomorphology and flow fields creates patchy landscapes. Environmental gradients emanating from hydraulic and microbial processes create potential niches in these landscapes and shape dispersal routes for microbial cells from the streamwater.…”

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confidence: 70%

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The ecology and biogeochemistry of stream biofilms

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The perception that most microorganisms live as complex communities that are attached to surfaces has profoundly changed microbiology over the past decades. Most, if not all, bacteria can form biofilms, which are communities of cells embedded in a porous extracellular matrix.Dental plaque, the microorganisms on catheters and implants that cause persistent infections and the fouling of ship hulls and pipework are all examples of biofilms with important implications for public health and industrial processes. Most contemporary biofilm research rests on the discovery made more than 35 years ago by Maurice Lock, Gill Geesey and Bill Costerton: bacteria attached to surfaces dominate microbial life in streams [1][2][3] . These microbiologists pioneered research into stream biofilms, also termed periphyton or epilithon, and described them as complex aggregates of bacteria, algae, protozoa, fungi and meiobenthos. The early study of stream biofilms also highlighted the relevance of interactions between microbial phototrophs and heterotrophs for energy fluxes and the role of the biofilm matrix as the site of extracellular enzyme activity and adsorption of dissolved organic matter (DOM) 3,4 .Since these early days, the study of the ecology and biogeochemistry of stream biofilms has slowly developed in the wake of thriving research on bacterial biofilms -often comprising 3 only a single strain, of interest to medical microbiology, rather than the polymicrobial communities found in stream biofilms -and on the microbial ecology of marine and lake planktonic communities 5 . Unlike bacterial biofilms grown in the laboratory, biofilms in streams are continuously exposed to a diverse inoculum that includes bacteria, archaea, algae, fungi, protozoa and even metazoa. These diverse biological 'building blocks', when combined with the dynamic flow of streamwater, generate biofilms with inherently complex and varying physical structures that have implications for microbial functioning and ecosystem processes 6 . In streams, biofilms are key sites of enzymatic activity 7 , including organic matter cycling, ecosystem respiration and primary production and, as such, form the basis of the food web.Why should we study the ecology and biogeochemistry of stream biofilms? Streams sculpt the continental surface, forming dense and conspicuous channel networks that can be thought of as ecological arteries that perfuse the landscape. Streams are connected to their catchments through various surface and subsurface flow paths and notably through the hyporheic zone in the streambed at the interface between groundwater and streamwater 8 . Microbial cells, solutes and particles enter streams through these flow paths and, en route to downstream ecosystems and ultimately to the oceans, they may interact with the biofilms that colonize the large surface area provided by the streambed as a 'microbial skin' (BOX 1). As a result, the streambed and its biofilm microbiome contribute to biogeochemical fluxes 8 . Indeed, stream biofilms are now recognized as su...

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“…This is supported by findings suggesting that niche differentiation and competition are processes responsible for shifts in community composition in streamers 40 .…”

Section: Biodiversity Across Spatial Scalessupporting

confidence: 55%

supporting

confidence: 55%

mentioning

confidence: 70%

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The ecology and biogeochemistry of stream biofilms

et al. 2016

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“…Swimming (40) and properties such as the coaggregation of single cells into larger entities (38) possibly help to overcome this barrier. Local hydrodynamics may also select for filamentous or chain-building bacteria that can contribute to the formation of streamers in high-shear microhabitats (6). Collectively, these properties may eventually affect the immigration behavior of dispersers and facilitate direct species sorting by hydrodynamics.…”

Section: Discussionmentioning

confidence: 99%

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

Besemer

Singer

Hödl

et al. 2009

Appl Environ Microbiol

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104

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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...

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“…In the case of diatoms, particularly the genera Achnanthes, Fragilaria, and Nitzschia may attach to empty substrata in a few days (Sabater and Romani, 1996). Some members of family Sphingomonadaceae have also been reported to pioneer biofilm formation (Besemer et al, 2009). Pohlon et al (2013) observed that a pioneer bacterial community dominated by members of the Cytophaga-Flavobacterium group settled onto the substratum within 12 h, and progressively incorporated Gammaproteobacteria and Betaproteobacteria.…”

Section: Biofilms In Temporary Streamsmentioning

confidence: 99%

Stream Biofilm Responses to Flow Intermittency: From Cells to Ecosystems

Sabater

Timoner

Borrego

et al. 2016

Front. Environ. Sci.

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Temporary streams are characterized by the alternation of dry and wet hydrological phases, creating both a harsh environment for the biota as well as a high diversity of opportunities for adaptation. These systems are mainly microbial-based during several of these hydrological phases, and those growing on all solid substrata (biofilms) accordingly change their physical structure and community composition. Biofilms experience large decreases in cell densities and biomass, both of bacteria and algae, during dryness. Algal and bacterial communities show remarkable decreases in their diversity, at least locally (at the habitat scale). Biofilms also respond with significant physiological plasticity to each of the hydrological changes. The decreasing humidity of the substrata through the drying process, and the changing quantity and quality of organic matter and nutrients available in the stream during that process, causes unequal responses on the biofilm bacteria and algae. Biofilm algae are affected faster than bacteria by the hydric stress, and as a result the ecosystem respiration resists longer than gross primary production to the increasing duration of flow intermittency. This response implies enhancing ecosystem heterotrophy, a pattern that can be exacerbated in temporary streams suffering of longer dry periods under global change.Keywords: biofilm, dry-rewetting cycle, temporary, intermittency, bacteria, algae, Mediterranean THE RELEVANCE OF TEMPORARY STREAMS IN THE WORLDFlow intermittency is part of the natural hydrology for streams and rivers, especially in arid and semi-arid landscapes. Temporary streams, or those that cease to flow at some points in space and time along their course, are a large fraction of many river networks, basically in tributaries of small order, but also in segments in the middle and lower parts of river networks. The number of temporary streams has been probably underestimated , as it appears from the application of novel on-site sensors, advances in remote sensing, and new modeling approaches. Flow intermittency has been estimated to account for 69% of first-order streams below 60 • , and up to 34% of larger order rivers (Raymond et al., 2013). Flow intermittency produces periodic or eventrelated loss of hydrologic connectivity between stream compartments, with consequences for all the processes ongoing in a waterway. Thus, flow intermittency triggers a chain of cascading effects eventually affecting water chemistry and biogeochemistry, as well as biodiversity, and ultimately community structure and ecosystem functioning.The direct implications of climate change and anomalous climatic events on flow regime are behind of the increasing temporality of many streams and rivers. Complex planetary scale processes, as well as local processes, may justify these situations. Anomalies such as the El Niño

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Architectural differentiation reflects bacterial community structure in stream biofilms

Cited by 46 publications

References 26 publications

The ecology and biogeochemistry of stream biofilms

The ecology and biogeochemistry of stream biofilms

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

Stream Biofilm Responses to Flow Intermittency: From Cells to Ecosystems

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