Warming has been shown to cause soil carbon (C) loss in northern grasslands owing to accelerated microbial decomposition that offsets increased grass productivity. Yet, a multi-decadal survey indicated that the surface soil C stock in Tibetan alpine grasslands remained relatively stable. To investigate this inconsistency, we analyzed the feedback responses of soil microbial communities to simulated warming by soil transplant in Tibetan grasslands. Whereas microbial functional diversity decreased in response to warming, microbial community structure did not correlate with changes in temperature. The relative abundance of catabolic genes associated with nitrogen (N) and C cycling decreased with warming, most notably in genes encoding enzymes associated with more recalcitrant C substrates. By contrast, genes associated with C fixation increased in relative abundance. The relative abundance of genes associated with urease, glutamate dehydrogenase and ammonia monoxygenase (ureC, gdh and amoA) were significantly correlated with N2O efflux. These results suggest that unlike arid/semiarid grasslands, Tibetan grasslands maintain negative feedback mechanisms that preserve terrestrial C and N pools. To examine whether these trends were applicable to the whole plateau, we included these measurements in a model and verified that topsoil C stocks remained relatively stable. Thus, by establishing linkages between microbial metabolic potential and soil biogeochemical processes, we conclude that long-term C loss in Tibetan grasslands is ameliorated by a reduction in microbial decomposition of recalcitrant C substrates.

As climate cooling is increasingly regarded as important natural variability of long-term global warming trends, there is a resurging interest in understanding its impact on biodiversity and ecosystem functioning. Here, we report a soil transplant experiment from lower to higher elevations in a Tibetan alpine grassland to simulate the impact of cooling on ecosystem community structure and function. Three years of cooling resulted in reduced plant productivity and microbial functional potential (for example, carbon respiration and nutrient cycling). Microbial genetic markers associated with chemically recalcitrant carbon decomposition remained unchanged despite a decrease in genes associated with chemically labile carbon decomposition. As a consequence, cooling-associated changes correlated with a decrease in soil organic carbon (SOC). Extrapolation of these results suggests that for every 1 °C decrease in annual average air temperature, 0.1 Pg (0.3%) of SOC would be lost from the Tibetan plateau. These results demonstrate that microbial feedbacks to cooling have the potential to differentially impact chemically labile and recalcitrant carbon turnover, which could lead to strong, adverse consequences on soil C storage. Our findings are alarming, considering the frequency of short-term cooling and its scale to disrupt ecosystems and biogeochemical cycling.

Eutrophication and climate warming, induced by anthropogenic activities, are simultaneously occurring worldwide and jointly affecting soil carbon stability. Therefore, it is of great interest to examine whether and how they interactively affect soil microbial community, a major soil carbon driver. Here, we showed that climate warming, simulated by southward transferring Mollisol soil in agricultural ecosystems from the cold temperate climate zone (N) to warm temperate climate (C) and subtropical climate zone (S), decreased soil organic matter (SOM) by 6%-12%. In contrast, amendment with nitrogen, phosphorus and potassium enhanced plant biomass by 97% and SOM by 6% at the N site, thus stimulating copiotrophic taxa but reducing oligotrophic taxa in relative abundance. However, microbial responses to nutrient amendment were overridden by soil transfer in that nutrient amendment had little effect at the C site but increased recalcitrant carbon-degrading fungal Agaricomycetes and Microbotryomycetes taxa derived from Basidiomycota by 4-17 folds and recalcitrant carbon-degrading genes by 23%-40% at the S site, implying a possible priming effect. Consequently, SOM at the S site was not increased by nutrient amendment despite increased plant biomass by 108%. Collectively, we demonstrate that soil transfer to warmer regions overrides microbial responses to nutrient amendment and weakens soil carbon sequestration.

Rapid climate change and intensified human activities have resulted in water table lowering (WTL) and enhanced nitrogen (N) deposition in Tibetan alpine wetlands. These changes may alter the magnitude and direction of greenhouse gas (GHG) emissions, affecting the climate impact of these fragile ecosystems. We conducted a mesocosm experiment combined with a metagenomics approach (GeoChip 5.0) to elucidate the effects of WTL (-20 cm relative to control) and N deposition (30 kg N ha^-1  yr^-1 ) on carbon dioxide (CO₂ ), methane (CH₄ ) and nitrous oxide (N₂ O) fluxes as well as the underlying mechanisms. Our results showed that WTL reduced CH₄ emissions by 57.4% averaged over three growing seasons compared with no-WTL plots, but had no significant effect on net CO₂ uptake or N₂ O flux. N deposition increased net CO₂ uptake by 25.2% in comparison with no-N deposition plots and turned the mesocosms from N₂ O sinks to N₂ O sources, but had little influence on CH₄ emissions. The interactions between WTL and N deposition were not detected in all GHG emissions. As a result, WTL and N deposition both reduced the global warming potential (GWP) of growing season GHG budgets on a 100-year time horizon, but via different mechanisms. WTL reduced GWP from 337.3 to -480.1 g CO₂ -eq m^-2 mostly because of decreased CH₄ emissions, while N deposition reduced GWP from 21.0 to -163.8 g CO₂ -eq m^-2 , mainly owing to increased net CO₂ uptake. GeoChip analysis revealed that decreased CH₄ production potential, rather than increased CH₄ oxidation potential, may lead to the reduction in net CH₄ emissions, and decreased nitrification potential and increased denitrification potential affected N₂ O fluxes under WTL conditions. Our study highlights the importance of microbial mechanisms in regulating ecosystem-scale GHG responses to environmental changes.

Background

Bacteriophage-prokaryote dynamics and interaction are believed to be important in governing microbiome composition and ecosystem functions, yet our limited knowledge of the spatial and temporal variation in phage and prokaryotic community compositions precludes accurate assessment of their roles and impacts. Anaerobic digesters are ideal model systems to examine phage-host interaction, owing to easy access, stable operation, nutrient-rich environment, and consequently enormous numbers of phages and prokaryotic cells.

Results

Equipped with high-throughput, cutting-edge environmental genomics techniques, we examined phage and prokaryotic community composition of four anaerobic digesters in full-scale wastewater treatment plants across China. Despite the relatively stable process performance in biogas production, phage and prokaryotic groups fluctuated monthly over a year of study period, showing significant correlations between those two groups at the α- and β-diversity levels. Strikingly, phages explained 40.6% of total variations of the prokaryotic community composition, much higher than the explanatory power by abiotic factors (14.5%). Consequently, phages were significantly (P < 0.010) linked to parameters related to process performance including biogas production and volatile solid concentrations. Association network analyses showed phage-prokaryote pairs were shallowly conserved since they were detected only within small viral clades.

Conclusions

Those results collectively demonstrate phages as a major biotic factor in controlling prokaryotic composition and process performance. Therefore, phages may play a larger role in shaping prokaryotic community dynamics and process performance of anaerobic digesters than currently appreciated.