The photosynthetic activity of aquatic microbial biofilms subjected to chemical stress varies over time - MICROBIOMIQ

Periphytic microbial communities are complex assemblages of micro-organisms (algea, bacteria, fundi, cyanobacteria, protozoa) that are attached to immerged substrates (inert or alive) in most of aquatic ecosystems. These communities play a tremendous role in ecosystems functions and associated services (e.g. primary production, biogeochemical cycles).

In the global change context, one major challenge for human and environmental health is to better understand the response of microbial communities to multiple stressors in terms of acclimation, adaptation and resilience in order to preserve ecosystem function and services. In particular, as regard chemical contamination of aquatic systems, one major goal is to characterize how the natural fluctuation of the structural biodiversity and microbial community functioning due to environmental changes might modulate their sensitivity to the chemical stress. 

In this context, the omics methods and their combination pave the way to new perspectives in microbial eco(toxi)cology to tackle the knowledge gap. Among others, these omics encompass:
Metagenomic allowing to explore simultaneously the diversity of species within a microbial community and its functional potential (gene reservoir); Untargeted meta-metabolomic providing a comprehensive picture of the microbial activity in response to the environment by analyzing all the small molecules from biochemical reactions within the community.

MICROBIOMIQ aims to better understand the link between the microbial activity (i.e. metabolome), the structural biodiversity (diversity of species and genes) and the sensitivity to the chemical stress associated to natural fluctuation in the species composition and the functioning of periphytic communities due to changing environmental conditions along the year. Thus, through the combination of metagenomic and meta-metabolomic on periphyton, this project will focus on the modulation of the photosynthetic function that is strongly involved in primary production and overall biogeochemical cycles. 
The outcomes of the project will allow to better understand the adaptive mechanisms (e.g. phenotypic plasticity) in the sensitivity of ecosystem functions (i.e. photosynthesis) to the chemical stress and their time sequence. The collected data would be further used to support the development of management tools in a water quality biomonitoring purpose.

Approaches

MICROBIOMIQ combines in situ investigations (longitudinal monitoring over 15 months – one measurement per month in a pond) with laboratory experiments (monthly acute exposures), based on a multidisciplinary approach that integrates metagenomics, meta-metabolomics, measurements of photosynthetic activity and the physico-chemical characterisation of the environments. The combination of these methods provides an innovative and precise understanding of the interrelationships between changes in environmental factors, taxonomic diversity, microbial activity and photosynthetic function, as well as their sensitivity to chemical stress under natural and controlled conditions, supported by bioinformatics approaches.

In situ sampling measured the taxonomic structure, microbial activity and photosynthesis of periphyton in parallel with monitoring of water physico-chemistry and meteorological conditions.

On a monthly basis, a portion of the collected periphyton was exposed to a model herbicide (terbuthylazine) for 4 hours to determine the community’s sensitivity at the molecular/biochemical (metabolomic) level and at the physiological/functional (photosynthetic yield) level.

A four-week exposure experiment was conducted in channels using periphyton collected from the same pond. The taxonomic composition, microbial activity and photosynthetic activity of the periphyton were measured at the start of the experiment and then after 24 hours, 72 hours, 1, 2, 3 and 4 weeks, alongside monitoring of the water’s physico-chemical parameters.

Results

No correlation was found between taxonomic diversity and metabolic diversity, indicating a certain degree of asynchrony between structural biodiversity and functional biodiversity (Q1). However, alpha taxonomic diversity was found to be correlated with temperature variations: the diversity of all taxa (presence/absence) decreases with temperature, whilst that of typical and dominant taxa increases with temperature. The predominant role of temperature in taxonomic structuring is highlighted, whilst microbial activity appears to be influenced by a greater number of factors, particularly nutrients (SO4, NO3) (Q1).

In parallel with these dynamics in community structure and function, a change in sensitivity was observed at the metabolome level, whilst the sensitivity of photosynthetic function remained relatively stable (Q2).

MICROBIOMIQ highlights significant heterogeneity in the metabolome’s response to terbuthylazine in terms of the number of metabolites, response profiles and metabolite classes, suggesting that toxicity pathways may vary over time. These results suggest that similar physiological responses may arise from various molecular pathways.

The project’s findings enhance our understanding of the link between natural changes in microbial biodiversity and the functioning of periphytic aquatic communities, as well as their sensitivity to chemical stress. This new knowledge is an essential prerequisite for establishing models capable of predicting, in the context of global change, the evolution of ecosystem functions and associated services based on the measurement of biodiversity descriptors (eDNA) and/or metabolomic descriptors. Thus, the metadata collected in this project will subsequently support the development of management tools within the framework of a biomonitoring approach to water quality.

Participants

INRAE units involved

• UR EABX - Unité de recherche Écosystèmes aquatiques et changements globaux
• UMR BIOGECO - Biodiversité, gènes et communautés