Philippe Binet

Above- and belowground linkages in Sphagnum peatland: climate warming affects plant-microbial interactions

Peatlands contain approximately one third of all soil organic carbon (SOC). Warming can alter above- and belowground linkages that regulate soil organic carbon dynamics and C-balance in peatlands. Here we examine the multiyear impact of in situ experimental warming on the microbial food web, vegetation, and their feedbacks with soil chemistry. We provide evidence of both positive and negative impacts of warming on specific microbial functional groups, leading to destabilization of the microbial food web. We observed a strong reduction (70%) in the biomass of top-predators (testate amoebae) in warmed plots. Such a loss caused a shortening of microbial food chains, which in turn stimulated microbial activity, leading to slight increases in levels of nutrients and labile C in water. We further show that warming altered the regulatory role of Sphagnum-polyphenols on microbial community structure with a potential inhibition of top predators. In addition, warming caused a decrease in Sphagnum cover and an increase in vascular plant cover. Using structural equation modelling, we show that changes in the microbial food web affected the relationships between plants, soil water chemistry, and microbial communities. These results suggest that warming will destabilize C and nutrient recycling of peatlands via changes in above- and belowground linkages, and therefore, the microbial food web associated with mosses will feedback positively to global warming by destabilizing the carbon cycle. This study confirms that microbial food webs thus constitute a key element in the functioning of peatland ecosystems. Their study can help understand how mosses, as ecosystem engineers, tightly regulate biogeochemical cycling and climate feedback in peatlands.

Challenges in tracing the fate and effects of atmospheric polycyclic aromatic hydrocarbon deposition in vascular plants.

Polycyclic aromatic hydrocarbons (PAHs) are ubiquitous organic pollutants that raise environmental concerns because of their toxicity. Their accumulation in vascular plants conditions harmful consequences to human health because of their position in the food chain. Consequently, understanding how atmospheric PAHs are taken up in plant tissues is crucial for risk assessment. In this review we synthesize current knowledge about PAH atmospheric deposition, accumulation in both gymnosperms and angiosperms, mechanisms of transfer, and ecological and physiological effects. PAHs emitted in the atmosphere partition between gas and particulate phases and undergo atmospheric deposition on shoots and soil. Most PAH concentration data from vascular plant leaves suggest that contamination occurs by both direct (air-leaf) and indirect (air-soil-root) pathways. Experimental studies demonstrate that PAHs affect plant growth, interfering with plant carbon allocation and root symbioses. Photosynthesis remains the most studied physiological process affected by PAHs. Among scientific challenges, identifying specific physiological transfer mechanisms and improving the understanding of plant-symbiont interactions in relation to PAH pollution remain pivotal for both fundamental and applied environmental sciences.

Effect of a temperature gradient on Sphagnum fallax and its associated living microbial communities: a study under controlled conditions.

Microbial communities living in Sphagnum are known to constitute early indicators of ecosystem disturbances, but little is known about their response (including their trophic relationships) to climate change. A microcosm experiment was designed to test the effects of a temperature gradient (15, 20, and 25°C) on microbial communities including different trophic groups (primary producers, decomposers, and unicellular predators) in Sphagnum segments (0-3 cm and 3-6 cm of the capitulum). Relationships between microbial communities and abiotic factors (pH, conductivity, temperature, and polyphenols) were also studied. The density and the biomass of testate amoebae in Sphagnum upper segments increased and their community structure changed in heated treatments. The biomass of testate amoebae was linked to the biomass of bacteria and to the total biomass of other groups added and, thus, suggests that indirect effects on the food web structure occurred. Redundancy analysis revealed that microbial assemblages differed strongly in Sphagnum upper segments along a temperature gradient in relation to abiotic factors. The sensitivity of these assemblages made them interesting indicators of climate change. Phenolic compounds represented an important explicative factor in microbial assemblages and outlined the potential direct and (or) indirect effects of phenolics on microbial communities.

Atmospheric phenanthrene pollution modulates carbon allocation in red clover (Trifolium pratense L.)

The influence of atmospheric phenanthrene (PHE) exposure (160 μg m(-3)) during one month on carbon allocation in clover was investigated by integrative (plant growth analysis) and instantaneous (13)CO(2) pulse-labelling approaches. PHE exposure diminished plant growth parameters (relative growth rate and net assimilation rate) and disturbed photosynthesis (carbon assimilation rate and chlorophyll content), leading to a 25% decrease in clover biomass. The root-shoot ratio was significantly enhanced (from 0.32 to 0.44). Photosynthates were identically allocated to leaves while less allocated to stems and roots. PHE exposure had a significant overall effect on the (13)C partitioning among clover organs as more carbon was retained in leaves at the expense of roots and stems. The findings indicate that PHE decreases root exudation or transfer to symbionts and in leaves, retains carbon in a non-structural form diverting photosynthates away from growth and respiration (emergence of an additional C loss process).

Evidences of Bryophyte Allelochemical Interactions: The Case of Sphagnum

In most terrestrial ecosystems, allelochemical interactions are involved in vascular plants. Nevertheless, bryophytes represent also a crucial group found in many ecosystems with a specific morphology and physiology (e.g. secondary metabolism). Among bryophytes, Sphagnum genus is of particular interest because they form a dense homogeneous carpet which is slowly decomposed (the peat) in peatlands. Such ecosystems represent a terrestrial sink of carbon and so are crucial to be studied, especially under a climate change. Objectives of this chapter were (1) to synthesize current bryophyte allelochemical interactions and (2) to illustrate recent research on Sphagnum with the case of Sphagnum fallax phenolics (production and degradation) recovered in a french peatland. The top layer of living Sphagnum represents the active allelopathic part where water-soluble phenolics were mostly recovered. Their concentrations were found to change along the seasons. The transformation of phenolic compounds is performed by an enzymatic system O2 (phenoloxidases) or H2O2 (peroxidases) dependent. Sphagnum-peroxidases constituted the main oxidative system and fungal phenoloxidases were proposed to be regulated by phenolics. Moreover, Sphagnum was able to regulate its secondary metabolism under a climate forcing by decreasing its phenolic concentrations. Allelopathic potential of Sphagnum phenolics was stated with their role in the microdistribution of associated Sphagnum microorganisms. Finally, Sphagnum extracts also strongly delayed Pine and Lolium germination seeds and inhibited Lolium radicle growth and delayed Raphanus and Pinus radicles. Ecological and agronomic perspectives of Sphagnum extracts are discussed.

Exposure chambers for studying the partitioning of atmospheric PAHs in environmental compartments: validation and calibration using experimental and computational approaches.

The environmental partitioning of atmospheric polycyclic aromatic hydrocarbons (PAHs) conditions their entry into food chains and subsequent risks for human health. The need for new experimental exposure devices for elucidating the mechanisms governing ecosystemic PAH transfer motivated the elaboration of an original small-scale exposure chamber (EC). A dual approach pairing experimentation and computational fluid dynamics (CFD) was selected to provide comprehensive validation of this EC as a tool to study the transfer and biological effects of atmospheric PAH pollution in microsystems. Soil samples and passive air samplers (PASs) were exposed to atmospheric pollution by phenanthrene (PHE), a gaseous PAH, for 2 weeks in examples of the EC being tested, set up under different conditions. Dynamic concentrations of atmospheric PHE and its uptake by PASs were simulated with CFD, results showing homogeneous distribution and constant atmospheric PHE concentrations inside the ECs. This work provides insight into the setting of given concentrations and pollution levels when using such ECs. The combination of experimentation and CFD is a successful ECs calibration method that should be developed with other semivolatile organic pollutants, including those that tend to partition in the aerosol phase.

Sphagnum Species Modulate their Phenolic Profiles and Mycorrhizal Colonization of Surrounding Andromeda polifolia along Peatland Microhabitats

Sphagnum mosses mediate long-term carbon accumulation in peatlands. Given their functional role as keystone species, it is important to consider their responses to ecological gradients and environmental changes through the production of phenolics. We compared the extent to which Sphagnum phenolic production was dependent on species, microhabitats and season, and how surrounding dwarf shrubs responded to Sphagnum phenolics. We evaluated the phenolic profiles of aqueous extracts of Sphagnum fallax and Sphagnum magellanicum over a 6-month period in two microhabitats (wet lawns versus dry hummocks) in a French peatland. Phenolic profiles of water-soluble extracts were measured by UHPLC-QTOF-MS. Andromeda polifolia mycorrhizal colonization was quantified by assessing the intensity of global root cortex colonization. Phenolic profiles of both Sphagnum mosses were species-, season- and microhabitat- dependant. Sphagnum-derived acids were the phenolics mostly recovered; relative quantities were 2.5-fold higher in S. fallax than in S. magellanicum. Microtopography and vascular plant cover strongly influenced phenolic profiles, especially for minor metabolites present in low abundance. Higher mycorrhizal colonization of A. polifolia was found in lawns as compared to hummocks. Mycorrhizal abundance, in contrast to environmental parameters, was correlated with production of minor phenolics in S. fallax. Our results highlight the close interaction between mycorrhizae such as those colonizing A. polifolia and the release of Sphagnum phenolic metabolites and suggest that Sphagnum-derived acids and minor phenolics play different roles in this interaction. This work provides new insight into the ecological role of Sphagnum phenolics by proposing a strong association with mycorrhizal colonization of shrubs.

Predator-prey mass ratio drives microbial activity under dry conditions in Sphagnum peatlands

Abstract Mid‐ to high‐latitude peatlands are a major terrestrial carbon stock but become carbon sources during droughts, which are increasingly frequent as a result of climate warming. A critical question within this context is the sensitivity to drought of peatland microbial food webs. Microbiota drive key ecological and biogeochemical processes, but their response to drought is likely to impact these processes. Peatland food webs have, however, been little studied, especially the response of microbial predators. We studied the response of microbial predators (testate amoebae, ciliates, rotifers, and nematodes) living in Sphagnum moss carpet to droughts, and their influence on lower trophic levels and on related microbial enzyme activity. We assessed the impact of reduced water availability on microbial predators in two peatlands using experimental (Linje mire, Poland) and natural (Forbonnet mire, France) water level gradients, reflecting a sudden change in moisture regime (Linje), and a typically drier environment (Forbonnet). The sensitivity of different microbial groups to drought was size dependent; large sized microbiota such as testate amoebae declined most under dry conditions (−41% in Forbonnet and −80% in Linje). These shifts caused a decrease in the predator–prey mass ratio (PPMR). We related microbial enzymatic activity to PPMR; we found that a decrease in PPMR can have divergent effects on microbial enzymatic activity. In a community adapted to drier conditions, decreasing PPMR stimulated microbial enzyme activity, while in extreme drought experiment, it reduced microbial activity. These results suggest that microbial enzymatic activity resulting from food web structure is optimal only within a certain range of PPMR, and that different trophic mechanisms are involved in the response of peatlands to droughts. Our findings confirm the importance of large microbial consumers living at the surface of peatlands on the functioning of peatlands, and illustrate their value as early warning indicators of change.