automated-3d-optical-coherence-tomography-to-elucidate-biofilm

Automated 3D Optical Coherence Tomography to Elucidate Biofilm Morphogenesis Over Large Spatial Scales

Biofilms are a most successful microbial lifestyle and prevail in a multitude of environmental and engineered settings. Understanding biofilm ...

combining-fluidic-devices-with-microscopy-flow-cytometry-to-study

Combining Fluidic Devices with Microscopy and Flow Cytometry to Study Microbial Transport in Porous Media Across Spatial Scales

Understanding the transport, dispersion and deposition of microorganisms in porous media is a complex scientific task comprising topics as diverse as ...

Ecole Polytechnique Fédérale de Lausanne

École Polytechnique Fédérale de Lausanne

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.

Hydrologic variability affects invertebrate grazing on phototrophic biofilms in stream microcosms.

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. 

Fluvial network organization imprints on microbial co-occurrence networks.

Resources structure ecological communities and potentially link biodiversity to energy flow. It is commonly believed that functional traits (generalists versus specialists) involved in the exploitation of resources depend on resource availability and environmental fluctuations. The longitudinal nature of stream ecosystems provides changing resources to stream biota with yet unknown effects on microbial functional traits and community structure. We investigated the impact of autochthonous (algal extract) and allochthonous (spruce extract) resources, as they change along alpine streams from above to below the treeline, on microbial diversity, community composition and functions of benthic biofilms. Combining bromodeoxyuridine labelling and 454 pyrosequencing, we showed that diversity was lower upstream than downstream of the treeline and that community composition changed along the altitudinal gradient. We also found that, especially for allochthonous resources, specialisation by biofilm bacteria increased along that same gradient. Our results suggest that in streams below the treeline biofilm diversity, specialisation and functioning are associated with increasing niche differentiation as potentially modulated by divers allochthonous and autochthonous constituents contributing to resources. These findings expand our current understanding on biofilm structure and function in alpine streams. 

Altitudinal patterns of diversity and functional traits of metabolically active microorganisms in stream biofilms.

Streams and rivers form dense networks, shape the Earth's 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. 

The ecology and biogeochemistry of stream biofilms.

Small-scale hydraulics affects microbial behaviour at the cell level, trophic interactions in marine aggregates and the physical structure and function of stream biofilms. However, it remains unclear how hydraulics, predictably changing from small streams to large rivers, impacts the structure and biodiversity of complex microbial communities in these ecosystems. Here, we present experimental evidence unveiling hydraulics as a hitherto poorly recognized control of microbial lifestyle differentiation in fluvial ecosystems. Exposing planktonic source communities from stream and floodplain ecosystems to different hydraulic environments revealed strong selective hydraulic pressures but only minor founder effects on the differentiation of attached biofilms and suspended aggregates and their biodiversity dynamics. Key taxa with a coherent phylogenetic underpinning drove this differentiation. Only a few resident and phylogenetically related taxa formed the backbone of biofilm communities, whereas numerous resident taxa characterized aggregate communities. Our findings unveil fundamental differences between biofilms and aggregates and build the basis for a mechanistic understanding of how hydraulics drives the distribution of microbial diversity along the fluvial continuum.

Attached biofilms and suspended aggregates are distinct microbial lifestyles emanating from differing hydraulics.

Glaciers cover ∼10% of the Earth's land surface, but they are shrinking rapidly across most parts of the world, leading to cascading impacts on downstream systems. Glaciers impart unique footprints on river flow at times when other water sources are low. Changes in river hydrology and morphology caused by climate-induced glacier loss are projected to be the greatest of any hydrological system, with major implications for riverine and near-shore marine environments. Here, we synthesize current evidence of how glacier shrinkage will alter hydrological regimes, sediment transport, and biogeochemical and contaminant fluxes from rivers to oceans. This will profoundly influence the natural environment, including many facets of biodiversity, and the ecosystem services that glacier-fed rivers provide to humans, particularly provision of water for agriculture, hydropower, and consumption. We conclude that human society must plan adaptation and mitigation measures for the full breadth of impacts in all affected regions caused by glacier shrinkage.

Glacier shrinkage driving global changes in downstream systems.

Microorganisms aggregated into matrix-enclosed biofilms dominate microbial life in most natural, engineered, and medical systems. Despite this, the ecological adaptations and metabolic trade-offs of the formation of complex biofilms are currently poorly understood. Here, exploring the dynamics of bacterial ribosomal RNA operon (rrn) copy numbers, we unravel the genomic underpinning of the formation and success of stream biofilms that contain hundreds of bacterial taxa. Experimenting with stream biofilms, we found that nascent biofilms in eutrophic systems had reduced lag phases and higher growth rates, and more taxa with higher rrn copy number than biofilms from oligotrophic systems. Based on these growth-related traits, our findings suggest that biofilm succession was dominated by slow-but-efficient bacteria likely with leaky functions, such as the production of extracellular polymeric substances at the cost of rapid growth. Expanding our experimental findings to biofilms from 140 streams, we found that rrn copy number distribution reflects functional trait allocation and ecological strategies of biofilms to be able to thrive in fluctuating environments. These findings suggest that alternative trade-offs dominating over rate-yield trade-offs contribute to the evolutionary success of stream biofilms.

Ecological strategies and metabolic trade-offs of complex environmental biofilms.

Streams are significant sources of CO to the atmosphere. Estimates of CO evasion fluxes (f ) from streams typically relate to the free flowing water but exclude geomorphological structures within the stream corridor. We found that gravel bars (GBs) are important sources of CO to the atmosphere, with on average more than twice as high f  as those from the streamwater, affecting f  at the level of entire headwater networks. Vertical temperature gradients resulting from the interplay between advective heat transfer and mixing with groundwater within GBs explained the observed variation in f  from the GBs reasonably well. We propose that increased temperatures and their gradients within GBs exposed to solar radiation stimulate heterotrophic metabolism therein and facilitate the venting of CO from external sources (e.g. downwelling streamwater, groundwater) within GBs. Our study shows that GB f  increased f  from stream corridors by [median, (95% confidence interval)] 16.69%, (15.85-18.49%); 30.44%, (30.40-34.68%) and 2.92%, (2.90-3.0%), for 3, 4 and 5 order streams, respectively. These findings shed new light on regional estimates of f  from streams, and are relevant given that streamwater thermal regimes change owing to global warming and human alteration of stream corridors.

Gravel bars are sites of increased CO outgassing in stream corridors.

Phototrophic biofilms are ubiquitous in freshwater and marine environments where they are critical for biogeochemical cycling, food webs and in industrial applications. In streams, phototrophic biofilms dominate benthic microbial life and harbour an immense prokaryotic and eukaryotic microbial biodiversity with biotic interactions across domains and trophic levels. Here, we examine how community structure and function of these biofilms respond to varying light availability, as the crucial energy source for phototrophic biofilms. Using metatranscriptomics, we found that under light limitation-dominant phototrophs, including diatoms and cyanobacteria, displayed a remarkable plasticity in their photosynthetic machinery manifested as higher abundance of messenger RNAs (mRNAs) involved in photosynthesis and chloroplast ribosomal RNA. Under higher light availability, bacterial mRNAs involved in phosphorus metabolism, mainly from Betaproteobacteria and Cyanobacteria, increased, likely compensating for nutrient depletion in thick biofilms with high biomass. Consumers, including diverse ciliates, displayed community shifts indicating preferential grazing on algae instead of bacteria under higher light. For the first time, we show that the functional integrity of stream biofilms under variable light availability is maintained by structure-function adaptations on several trophic levels. Our findings shed new light on complex biofilms, or "microbial jungles", where in analogy to forests, diverse and multitrophic level communities lend stability to ecosystem functioning. This multitrophic level perspective, coupling metatranscriptomics to process measurements, could advance understanding of microbial-driven ecosystems beyond biofilms, including planktonic and soil environments.

Light availability impacts structure and function of phototrophic stream biofilms across domains and trophic levels.

The loss of environmental heterogeneity threatens biodiversity and ecosystem functioning. It is therefore important to understand the relationship between environmental heterogeneity and spatial resilience as the capacity of ecological communities embedded in a landscape matrix to reorganize following disturbance. We experimented with phototrophic biofilms colonizing streambed landscapes differing in spatial heterogeneity and exposed to flow-induced disturbance. We show how streambed roughness and related features promote growth-related trait diversity and the recovery of biofilms towards carrying capacity (CC) and spatial resilience. At the scale of streambed landscapes, roughness and exposure to water flow promoted biofilm CC and growth trait diversity. Structural equation modelling identified roughness, post-disturbance biomass and a 'neighbourhood effect' to drive biofilm CC. Our findings suggest that the environment selecting for adaptive capacities prior to disturbance (that is, memory effects) and biofilm connectivity into spatial networks (that is, mobile links) contribute to the spatial resilience of biofilms in streambed landscapes. These findings are critical given the key functions biofilms fulfil in streams, now increasingly experiencing shifts in sedimentary and hydrological regimes.

Environmental heterogeneity promotes spatial resilience of phototrophic biofilms in streambeds.

Biofilms regulate critical processes in porous ecosystems. However, the biophysical underpinnings of the ecological success of these biofilms are poorly understood. Combining experiments with fluidic devices, sequencing and modeling, we reveal that architectural plasticity enhances space exploitation by multispecies biofilms in porous environments. Biofilms consistently differentiated into an annular base biofilm coating the grains and into streamers protruding from the grains into the pore space. Although different flow-related processes governed the differentiation of these architectures, both BB and streamers were composed of similar bacterial assemblages. This is evidence for architectural plasticity. Architectural plasticity allowed for complementary use of the space provided by the grain-pore complexes, which increased biofilm carrying capacity at the larger scale of the porous system. This increase comes potentially at the cost of a tradeoff. Contrasting time scales of oxygen replenishment and consumption, we show that streamers locally inhibit the growth of the BB downstream from the grains. Our study provides first insights into the biophysical underpinnings to the success of multispecies biofilms in porous environments.

ArticleTotal : 2	Year
Publication title	2019
Publication title	2020

Article	Year
Hydrologic variability affects invertebrate grazing on phototrophic biofilms in stream microcosms. PloS one\| PubMed ID: 23613735	2013
Fluvial network organization imprints on microbial co-occurrence networks. Proceedings of the National Academy of Sciences of the United States of America\| PubMed ID: 25136087	2014
Altitudinal patterns of diversity and functional traits of metabolically active microorganisms in stream biofilms. The ISME journal\| PubMed ID: 25978543	2015
The ecology and biogeochemistry of stream biofilms. Nature reviews. Microbiology\| PubMed ID: 26972916	2016
Attached biofilms and suspended aggregates are distinct microbial lifestyles emanating from differing hydraulics. Nature microbiology\| PubMed ID: 27694939	2016
Glacier shrinkage driving global changes in downstream systems. Proceedings of the National Academy of Sciences of the United States of America\| PubMed ID: 28874558	2017
Ecological strategies and metabolic trade-offs of complex environmental biofilms. NPJ biofilms and microbiomes\| PubMed ID: 28955480	2017
Gravel bars are sites of increased CO outgassing in stream corridors. Scientific reports\| PubMed ID: 29089508	2017
Light availability impacts structure and function of phototrophic stream biofilms across domains and trophic levels. Molecular ecology\| PubMed ID: 29679511	2018
Environmental heterogeneity promotes spatial resilience of phototrophic biofilms in streambeds. Biology letters\| PubMed ID: 30305460	2018
Unraveling the biophysical underpinnings to the success of multispecies biofilms in porous environments. The ISME journal\| PubMed ID: 30833685	2019

Tom J. Battin

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