Vincent E. J. Jassey

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.

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.

Peatland vascular plant functional types affect methane dynamics by altering microbial community structure

Peatlands are natural sources of atmospheric methane (CH4), an important greenhouse gas. It is established that peatland methane dynamics are controlled by both biotic and abiotic conditions, yet the interactive effect of these drivers is less studied and consequently poorly understood. Climate change affects the distribution of vascular plant functional types (PFTs) in peatlands. By removing specific PFTs, we assessed their effects on peat organic matter chemistry, microbial community composition and on potential methane production (PMP) and oxidation (PMO) in two microhabitats (lawns and hummocks). Whilst PFT removal only marginally altered the peat organic matter chemistry, we observed considerable changes in microbial community structure. This resulted in altered PMP and PMO. PMP was slightly lower when graminoids were removed, whilst PMO was highest in the absence of both vascular PFTs (graminoids and ericoids), but only in the hummocks. Path analyses demonstrate that different plant-soil interactions drive PMP and PMO in peatlands and that changes in biotic and abiotic factors can have auto-amplifying effects on current CH4 dynamics.Synthesis. Changing environmental conditions will, both directly and indirectly, affect peatland processes, causing unforeseen changes in CH4 dynamics. The resilience of peatland CH4 dynamics to environmental change therefore depends on the interaction between plant community composition and microbial communities.

To What Extent Do Food Preferences Explain the Trophic Position of Heterotrophic and Mixotrophic Microbial Consumers in a Sphagnum Peatland

Although microorganisms are the primary drivers of biogeochemical cycles, the structure and functioning of microbial food webs are poorly studied. This is the case in Sphagnum peatlands, where microbial communities play a key role in the global carbon cycle. Here, we explored the structure of the microbial food web from a Sphagnum peatland by analyzing (1) the density and biomass of different microbial functional groups, (2) the natural stable isotope (δ13C and δ15N) signatures of key microbial consumers (testate amoebae), and (3) the digestive vacuole contents of Hyalosphenia papilio, the dominant testate amoeba species in our system. Our results showed that the feeding type of testate amoeba species (bacterivory, algivory, or both) translates into their trophic position as assessed by isotopic signatures. Our study further demonstrates, for H. papilio, the energetic benefits of mixotrophy when the density of its preferential prey is low. Overall, our results show that testate amoebae occupy different trophic levels within the microbial food web, depending on their feeding behavior, the density of their food resources, and their metabolism (i.e., mixotrophy vs. heterotrophy). Combined analyses of predation, community structure, and stable isotopes now allow the structure of microbial food webs to be more completely described, which should lead to improved models of microbial community function.

An unexpected role for mixotrophs in the response of peatland carbon cycling to climate warming

Mixotrophic protists are increasingly recognized for their significant contribution to carbon (C) cycling. As phototrophs they contribute to photosynthetic C fixation, whilst as predators of decomposers, they indirectly influence organic matter decomposition. Despite these direct and indirect effects on the C cycle, little is known about the responses of peatland mixotrophs to climate change and the potential consequences for the peatland C cycle. With a combination of field and microcosm experiments, we show that mixotrophs in the Sphagnum bryosphere play an important role in modulating peatland C cycle responses to experimental warming. We found that five years of consecutive summer warming with peaks of +2 to +8°C led to a 50% reduction in the biomass of the dominant mixotrophs, the mixotrophic testate amoebae (MTA). The biomass of other microbial groups (including decomposers) did not change, suggesting MTA to be particularly sensitive to temperature. In a microcosm experiment under controlled conditions, we then manipulated the abundance of MTA, and showed that the reported 50% reduction of MTA biomass in the field was linked to a significant reduction of net C uptake (-13%) of the entire Sphagnum bryosphere. Our findings suggest that reduced abundance of MTA with climate warming could lead to reduced peatland C fixation.

Functional traits as a new approach for interpreting testate amoeba palaeo-records in peatlands and assessing the causes and consequences of past changes in species composition

Subfossil remains of various groups of organisms preserved in peat and sediment archives are commonly used to infer past environmental changes using transfer functions based on species composition. However, the changes in community structure can also be explored using the functional trait approach. Investigation of functional traits in palaeoecological records can inform about the mechanisms through which abiotic variables such as temperature or moisture impact communities. Moreover, changes in functional traits provide information about changes in ecosystem functioning and can potentially lead to the reconstruction of past processes at the ecosystem scale. Here, we use five key functional traits of arcellinid testate amoebae (TAs), a group of protozoa that are key actors in the microbial foodwebs in peatlands. We apply this approach to the subfossil TA Holocene record of four geographically independent peatlands from Alaska, Switzerland, Poland and Russia. We found that species with larger shells were frequently eliminated from the communities most likely as a result of a switch towards drier conditions. However, when conditions were wetter, species with large shells and species with small shells could coexist because they differed in their trophic niche (i.e. preys). Our results show direct but site-specific links between TA trait data and the depth to water table and pH data inferred from TA species composition. This suggests that past environmental changes influenced both species composition and community function in these ecosystems. Overall, this study demonstrates that species- and trait-based approaches yield complementary information on past environmental changes. For instance, while taxonomic approaches reveal the changes in community composition over time, investigation of traits informs both on the causes and the consequences of these changes on ecosystem functioning.

Snow cover manipulation effects on microbial community structure and soil chemistry in a mountain bog

Background and AimsAlterations in snow cover driven by climate change may impact ecosystem functioning, including biogeochemistry and soil (microbial) processes. We elucidated the effects of snow cover manipulation (SCM) on above-and belowground processes in a temperate peatland.MethodsIn a Swiss mountain-peatland we manipulated snow cover (addition, removal and control), and assessed the effects on Andromeda polifolia root enzyme activity, soil microbial community structure, and leaf tissue and soil biogeochemistry.ResultsReduced snow cover produced warmer soils in our experiment while increased snow cover kept soil temperatures close-to-freezing. SCM had a major influence on the microbial community, and prolonged ‘close-to-freezing’ temperatures caused a shift in microbial communities toward fungal dominance. Soil temperature largely explained soil microbial structure, while other descriptors such as root enzyme activity and pore-water chemistry interacted less with the soil microbial communities.ConclusionsWe envisage that SCM-driven changes in the microbial community composition could lead to substantial changes in trophic fluxes and associated ecosystem processes. Hence, we need to improve our understanding on the impact of frost and freeze-thaw cycles on the microbial food web and its implications for peatland ecosystem processes in a changing climate; in particular for the fate of the sequestered carbon.

A novel testate amoebae trait-based approach to infer environmental disturbance in Sphagnum peatlands

Species’ functional traits are closely related to ecosystem processes through evolutionary adaptation, and are thus directly connected to environmental changes. Species’ traits are not commonly used in palaeoecology, even though they offer powerful advantages in understanding the impact of environmental disturbances in a mechanistic way over time. Here we show that functional traits of testate amoebae (TA), a common group of palaeoecological indicators, can serve as an early warning signal of ecosystem disturbance and help determine thresholds of ecosystem resilience to disturbances in peatlands. We analysed TA traits from two Sphagnum-dominated mires, which had experienced different kinds of disturbances in the past 2000 years – fire and peat extraction, respectively. We tested the effect of disturbances on the linkages between TA community structure, functional trait composition and functional diversity using structural equation modelling. We found that traits such as mixotrophy and small hidden apertures (plagiostomic apertures) are strongly connected with disturbance, suggesting that these two traits can be used as palaeoecological proxies of peatland disturbance. We show that TA functional traits may serve as a good proxy of past environmental changes, and further analysis of trait-ecosystem relationships could make them valuable indicators of the contemporary ecosystem state.

Experimental warming differentially affects microbial structure and activity in two contrasted moisture sites in a Sphagnum-dominated peatland.

Several studies on the impact of climate warming have indicated that peat decomposition/mineralization will be enhanced. Most of these studies deal with the impact of experimental warming during summer when prevalent abiotic conditions are favorable to decomposition. Here, we investigated the effect of experimental air warming by open-top chambers (OTCs) on water-extractable organic matter (WEOM), microbial biomasses and enzymatic activities in two contrasted moisture sites named Bog and Fen sites, the latter considered as the wetter ones. While no or few changes in peat temperature and water content appeared under the overall effect of OTCs, we observed that air warming smoothed water content differences and led to a decrease in mean peat temperature at the warmed Bog sites. This thermal discrepancy between the two sites led to contrasting changes in microbial structure and activities: a rise in hydrolytic activity at the warmed Bog sites and a relative enhancement of bacterial biomass at the warmed Fen sites. These features were not associated with any change in WEOM properties namely carbon and sugar contents and aromaticity, suggesting that air warming did not trigger any shift in OM decomposition. Using various tools, we show that the use of single indicators of OM decomposition can lead to fallacious conclusions. Lastly, these patterns may change seasonally as a consequence of complex interactions between groundwater level and air warming, suggesting the need to improve our knowledge using a high time-resolution approach.

Subordinate plants mitigate drought effects on soil ecosystem processes by stimulating fungi

1. The subordinate insurance hypothesis suggests that highly diverse communities contain greater numbers of subordinate species than less diverse communities. It has previously been reported that subordinate species can improve grassland productivity during drought, but the underlying mechanisms remain undetermined. 2. Using a combination of subordinate species removal and summer drought, we show that soil processes play a critical role in community resistance to drought. Interestingly, subordinate species drive soil microbial community structure and largely mitigate the effect of drought on grassland soil functioning. Our results highlight subordinate species in shifting the balance within the phospholipid fatty acid (PLFA) microbial community towards more fungal dominance. 3. Fungal communities promoted by subordinate species were more resistant to drought and maintained higher rates of litter decomposition and soil respiration. These results emphasize the important role of subordinate species in mitigating drought effects on soil ecosystem functions. Reciprocal effects between fungi and subordinate species explain also how subordinate species better resisted to drought conditions. 4. Our results point to a delayed plant-soil feedback following environmental perturbation. Additionally, they extend the diversity insurance hypothesis by showing that more diverse communities not only contain species well adapted to perturbations, but also species with higher impacts on soil microbial communities and related ecosystem functions.