A stoichiometric approach to estimate sources of mineral-associated soil organic matter.

Mineral-associated soil organic matter (MAOM) is the largest, slowest cycling pool of carbon (C) in the terrestrial biosphere. MAOM is primarily derived from plant and microbial sources, yet the relative contributions of these two sources to MAOM remain unresolved. Resolving this issue is essential for managing and modeling soil carbon responses to environmental change. Microbial biomarkers, particularly amino sugars, are the primary method used to estimate microbial versus plant contributions to MAOM, despite systematic biases associated with these estimates. There is a clear need for independent lines of evidence to help determine the relative importance of plant versus microbial contributions to MAOM. Here, we synthesized 288 datasets of C/N ratios for MAOM, particulate organic matter (POM), and microbial biomass across the soils of forests, grasslands, and croplands. Microbial biomass is the source of microbial residues that form MAOM, whereas the POM pool is the direct precursor of plant residues that form MAOM. We then used a stoichiometric approach-based on two-pool, isotope-mixing models-to estimate the proportional contribution of plant residue (POM) versus microbial sources to the MAOM pool. Depending on the assumptions underlying our approach, microbial inputs accounted for between 34% and 47% of the MAOM pool, whereas plant residues contributed 53%-66%. Our results therefore challenge the existing hypothesis that microbial contributions are the dominant constituents of MAOM. We conclude that biogeochemical theory and models should account for multiple pathways of MAOM formation, and that multiple independent lines of evidence are required to resolve where and when plant versus microbial contributions are dominant in MAOM formation.

Shifts in soil ammonia-oxidizing community maintain the nitrogen stimulation of nitrification across climatic conditions.

Anthropogenic nitrogen (N) loading alters soil ammonia-oxidizing archaea (AOA) and bacteria (AOB) abundances, likely leading to substantial changes in soil nitrification. However, the factors and mechanisms determining the responses of soil AOA:AOB and nitrification to N loading are still unclear, making it difficult to predict future changes in soil nitrification. Herein, we synthesize 68 field studies around the world to evaluate the impacts of N loading on soil ammonia oxidizers and nitrification. Across a wide range of biotic and abiotic factors, climate is the most important driver of the responses of AOA:AOB to N loading. Climate does not directly affect the N-stimulation of nitrification, but does so via climate-related shifts in AOA:AOB. Specifically, climate modulates the responses of AOA:AOB to N loading by affecting soil pH, N-availability and moisture. AOB play a dominant role in affecting nitrification in dry climates, while the impacts from AOA can exceed AOB in humid climates. Together, these results suggest that climate-related shifts in soil ammonia-oxidizing community maintain the N-stimulation of nitrification, highlighting the importance of microbial community composition in mediating the responses of the soil N cycle to N loading.

Integrated biochar solutions can achieve carbon-neutral staple crop production.

Agricultural food production is a main driver of global greenhouse gas emissions, with unclear pathways towards carbon neutrality. Here, through a comprehensive life-cycle assessment using data from China, we show that an integrated biomass pyrolysis and electricity generation system coupled with commonly applied methane and nitrogen mitigation measures can help reduce staple crops' life-cycle greenhouse gas emissions from the current 666.5 to -37.9 Tg CO2-equivalent yr-1. Emission reductions would be achieved primarily through carbon sequestration from biochar application to the soil, and fossil fuel displacement by bio-energy produced from pyrolysis. We estimate that this integrated system can increase crop yield by 8.3%, decrease reactive nitrogen losses by 25.5%, lower air pollutant emissions by 125-2,483 Gg yr-1 and enhance net environmental and economic benefits by 36.2%. These results indicate that integrated biochar solutions could contribute to China's 2060 carbon neutrality objective while enhancing food security and environmental sustainability.

Nitrogen and water availability control plant carbon storage with warming.

Plants may slow global warming through enhanced growth, because increased levels of photosynthesis stimulate the land carbon (C) sink. However, how climate warming affects plant C storage globally and key drivers determining the response of plant C storage to climate warming remains unclear, causing uncertainty in climate projections. We performed a comprehensive meta-analysis, compiling 393 observations from 99 warming studies to examine the global patterns of plant C storage responses to climate warming and explore the key drivers. Warming significantly increased total biomass (+8.4 %), aboveground biomass (+12.6 %) and belowground biomass (+10.1 %). The effect of experimental warming on plant biomass was best explained by the availability of soil nitrogen (N) and water. Across the entire dataset, warming-induced changes in total, aboveground and belowground biomass all positively correlated with soil C:N ratio, an indicator of soil N availability. In addition, warming stimulated plant biomass more strongly in humid than in dry ecosystems, and warming tended to decrease root:shoot ratios at high soil C:N ratios. Together, these results suggest dual controls of warming effects on plant C storage; warming increases plant growth in ecosystems where N is limiting plant growth, but it reduces plant growth where water availability is limiting plant growth.

Unexpected Parabolic Temperature Dependency of CH4 Emissions from Rice Paddies.

Global warming is expected to affect methane (CH4) emissions from rice paddies, one of the largest human-induced sources of this potent greenhouse gas. However, the large variability in warming impacts on CH4 emissions makes it difficult to extrapolate the experimental results over large regions. Here, we show, through meta-analysis and multi-site warming experiments using the free air temperature increase facility, that warming stimulates CH4 emissions most strongly at background air temperatures during the flooded stage of ∼26 °C, with smaller responses of CH4 emissions to warming at lower and higher temperatures. This pattern can be explained by divergent warming responses of plant growth, methanogens, and methanotrophs. The effects of warming on rice biomass decreased with the background air temperature. Warming increased the abundance of methanogens more strongly at the medium air temperature site than the low and high air temperature sites. In contrast, the effects of warming on the abundance of methanotrophs were similar across the three temperature sites. We estimate that 1 °C warming will increase CH4 emissions from paddies in China by 12.6%─substantially higher than the estimates obtained from leading ecosystem models. Our findings challenge model assumptions and suggest that the estimates of future paddy CH4 emissions need to consider both plant and microbial responses to warming.

Predicting field N2O emissions from crop residues based on their biochemical composition: A meta-analytical approach.

Crop residue incorporation is a common practice to increase or restore organic matter stocks in agricultural soils. However, this practice often increases emissions of the powerful greenhouse gas nitrous oxide (N2O). Previous meta-analyses have linked various biochemical properties of crop residues to N2O emissions, but the relationships between these properties have been overlooked, hampering our ability to predict N2O emissions from specific residues. Here we combine comprehensive databases for N2O emissions from crop residues and crop residue biochemical characteristics with a random-meta-forest approach, to develop a predictive framework of crop residue effects on N2O emissions. On average, crop residue incorporation increased soil N2O emissions by 43% compared to residue removal, however crop residues led to both increases and reductions in N2O emissions. Crop residue effects on N2O emissions were best predicted by easily degradable fractions (i.e. water soluble carbon, soluble Van Soest fraction (NDS)), structural fractions and N returned with crop residues. The relationship between these biochemical properties and N2O emissions differed widely in terms of form and direction. However, due to the strong correlations among these properties, we were able to develop a simplified classification for crop residues based on the stage of physiological maturity of the plant at which the residue was generated. This maturity criteria provided the most robust and yet simple approach to categorize crop residues according to their potential to regulate N2O emissions. Immature residues (high water soluble carbon, soluble NDS and total N concentration, low relative cellulose, hemicellulose, lignin fractions, and low C:N ratio) strongly stimulated N2O emissions, whereas mature residues with opposite characteristics had marginal effects on N2O. The most important crop types belonging to the immature residue group - cover crops, grasslands and vegetables - are important for the delivery of multiple ecosystem services. Thus, these residues should be managed properly to avoid their potentially high N2O emissions.

The Functional Significance of Bacterial Predators.

Predation structures food webs, influences energy flow, and alters rates and pathways of nutrient cycling through ecosystems, effects that are well documented for macroscopic predators. In the microbial world, predatory bacteria are common, yet little is known about their rates of growth and roles in energy flows through microbial food webs, in part because these are difficult to quantify. Here, we show that growth and carbon uptake were higher in predatory bacteria compared to nonpredatory bacteria, a finding across 15 sites, synthesizing 82 experiments and over 100,000 taxon-specific measurements of element flow into newly synthesized bacterial DNA. Obligate predatory bacteria grew 36% faster and assimilated carbon at rates 211% higher than nonpredatory bacteria. These differences were less pronounced for facultative predators (6% higher growth rates, 17% higher carbon assimilation rates), though high growth and carbon assimilation rates were observed for some facultative predators, such as members of the genera Lysobacter and Cytophaga, both capable of gliding motility and wolf-pack hunting behavior. Added carbon substrates disproportionately stimulated growth of obligate predators, with responses 63% higher than those of nonpredators for the Bdellovibrionales and 81% higher for the Vampirovibrionales, whereas responses of facultative predators to substrate addition were no different from those of nonpredators. This finding supports the ecological theory that higher productivity increases predator control of lower trophic levels. These findings also indicate that the functional significance of bacterial predators increases with energy flow and that predatory bacteria influence element flow through microbial food webs.IMPORTANCE The word "predator" may conjure images of leopards killing and eating impala on the African savannah or of great white sharks attacking elephant seals off the coast of California. But microorganisms are also predators, including bacteria that kill and eat other bacteria. While predatory bacteria have been found in many environments, it has been challenging to document their importance in nature. This study quantified the growth of predatory and nonpredatory bacteria in soils (and one stream) by tracking isotopically labeled substrates into newly synthesized DNA. Predatory bacteria were more active than nonpredators, and obligate predators, such as Bdellovibrionales and Vampirovibrionales, increased in growth rate in response to added substrates at the base of the food chain, strong evidence of trophic control. This work provides quantitative measures of predator activity and suggests that predatory bacteria-along with protists, nematodes, and phages-are active and important in microbial food webs.

Towards optimal use of phosphorus fertiliser.

Because phosphorus (P) is one of the most limiting nutrients in agricultural systems, P fertilisation is essential to feed the world. However, declining P reserves demand far more effective use of this crucial resource. Here, we use meta-analysis to synthesize yield responses to P fertilisation in grasslands, the most common type of agricultural land, to identify under which conditions P fertilisation is most effective. Yield responses to P fertilisation were 40-100% higher in (a) tropical vs temperate regions; (b) grass/legume mixtures vs grass monocultures; and (c) soil pH of 5-6 vs other pHs. The agronomic efficiency of P fertilisation decreased for greater P application rates. Moreover, soils with low P availability reacted disproportionately strong to fertilisation. Hence, low fertiliser application rates to P-deficient soils result in stronger absolute yield benefits than high rates applied to soils with a higher P status. Overall, our results suggest that optimising P fertiliser use is key to sustainable intensification of agricultural systems.

Lower-than-expected CH4 emissions from rice paddies with rising CO2 concentrations.

Elevated atmospheric CO2 (eCO2 ) generally increases carbon input in rice paddy soils and stimulates the growth of methane-producing microorganisms. Therefore, eCO2 is widely expected to increase methane (CH4 ) emissions from rice agriculture, a major source of anthropogenic CH4 . Agricultural practices strongly affect CH4 emissions from rice paddies as well, but whether these practices modulate effects of eCO2 is unclear. Here we show, by combining a series of experiments and meta-analyses, that whereas eCO2 strongly increased CH4 emissions from paddies without straw incorporation, it tended to reduce CH4 emissions from paddy soils with straw incorporation. Our experiments also identified the microbial processes underlying these results: eCO2 increased methane-consuming microorganisms more strongly in soils with straw incorporation than in soils without straw, with the opposite pattern for methane-producing microorganisms. Accounting for the interaction between CO2 and straw management, we estimate that eCO2 increases global CH4 emissions from rice paddies by 3.7%, an order of magnitude lower than previous estimates. Our results suggest that the effect of eCO2 on CH4 emissions from rice paddies is smaller than previously thought and underline the need for judicious agricultural management to curb future CH4 emissions.

Soil carbon loss with warming: New evidence from carbon-degrading enzymes.

Climate warming affects soil carbon (C) dynamics, with possible serious consequences for soil C stocks and atmospheric CO2 concentrations. However, the mechanisms underlying changes in soil C storage are not well understood, hampering long-term predictions of climate C-feedbacks. The activity of the extracellular enzymes ligninase and cellulase can be used to track changes in the predominant C sources of soil microbes and can thus provide mechanistic insights into soil C loss pathways. Here we show, using meta-analysis, that reductions in soil C stocks with warming are associated with increased ratios of ligninase to cellulase activity. Furthermore, whereas long-term (≥5 years) warming reduced the soil recalcitrant C pool by 14%, short-term warming had no significant effect. Together, these results suggest that warming stimulates microbial utilization of recalcitrant C pools, possibly exacerbating long-term climate-C feedbacks.

Acclimation of methane emissions from rice paddy fields to straw addition.

Straw incorporation is a common long-term practice to improve soil fertility in croplands worldwide. However, straw amendments often increase methane (CH4) emissions from rice paddies, one of the main sources of anthropogenic CH4. Intergovernmental Panel on Climate Change (IPCC) methodologies to estimate CH4 emissions from rice agriculture assume that the effect of straw addition remains constant over time. Here, we show through a series of experiments and meta-analysis that these CH4 emissions acclimate. Effects of long-term (>5 years) straw application on CH4 emissions were, on average, 48% lower than IPCC estimates. Long-term straw incorporation increased soil methanotrophic abundance and rice root size, suggesting an increase in CH4 oxidation rates through improved O2 transport into the rhizosphere. Our results suggest that recent model projections may have overestimated CH4 emissions from rice agriculture and that CH4 emission estimates can be improved by considering the duration of straw incorporation and other management practices.

Limited potential of harvest index improvement to reduce methane emissions from rice paddies.

Rice is a staple food for nearly half of the world's population, but rice paddies constitute a major source of anthropogenic CH4 emissions. Root exudates from growing rice plants are an important substrate for methane-producing microorganisms. Therefore, breeding efforts optimizing rice plant photosynthate allocation to grains, i.e., increasing harvest index (HI), are widely expected to reduce CH4 emissions with higher yield. Here we show, by combining a series of experiments, meta-analyses and an expert survey, that the potential of CH4 mitigation from rice paddies through HI improvement is in fact small. Whereas HI improvement reduced CH4 emissions under continuously flooded (CF) irrigation, it did not affect CH4 emissions in systems with intermittent irrigation (II). We estimate that future plant breeding efforts aimed at HI improvement to the theoretical maximum value will reduce CH4 emissions in CF systems by 4.4%. However, CF systems currently make up only a small fraction of the total rice growing area (i.e., 27% of the Chinese rice paddy area). Thus, to achieve substantial CH4 mitigation from rice agriculture, alternative plant breeding strategies may be needed, along with alternative management.

A keystone microbial enzyme for nitrogen control of soil carbon storage.

Agricultural and industrial activities have increased atmospheric nitrogen (N) deposition to ecosystems worldwide. N deposition can stimulate plant growth and soil carbon (C) input, enhancing soil C storage. Changes in microbial decomposition could also influence soil C storage, yet this influence has been difficult to discern, partly because of the variable effects of added N on the microbial enzymes involved. We show, using meta-analysis, that added N reduced the activity of lignin-modifying enzymes (LMEs), and that this N-induced enzyme suppression was associated with increases in soil C. In contrast, N-induced changes in cellulase activity were unrelated to changes in soil C. Moreover, the effects of added soil N on LME activity accounted for more of the variation in responses of soil C than a wide range of other environmental and experimental factors. Our results suggest that, through responses of a single enzyme system to added N, soil microorganisms drive long-term changes in soil C accumulation. Incorporating this microbial influence on ecosystem biogeochemistry into Earth system models could improve predictions of ecosystem C dynamics.

Differential responses of carbon-degrading enzyme activities to warming: Implications for soil respiration.

Extracellular enzymes catalyze rate-limiting steps in soil organic matter decomposition, and their activities (EEAs) play a key role in determining soil respiration (SR). Both EEAs and SR are highly sensitive to temperature, but their responses to climate warming remain poorly understood. Here, we present a meta-analysis on the response of soil cellulase and ligninase activities and SR to warming, synthesizing data from 56 studies. We found that warming significantly enhanced ligninase activity by 21.4% but had no effect on cellulase activity. Increases in ligninase activity were positively correlated with changes in SR, while no such relationship was found for cellulase. The warming response of ligninase activity was more closely related to the responses of SR than a wide range of environmental and experimental methodological factors. Furthermore, warming effects on ligninase activity increased with experiment duration. These results suggest that soil microorganisms sustain long-term increases in SR with warming by gradually increasing the degradation of the recalcitrant carbon pool.

Faster turnover of new soil carbon inputs under increased atmospheric CO2.

Rising levels of atmospheric CO2 frequently stimulate plant inputs to soil, but the consequences of these changes for soil carbon (C) dynamics are poorly understood. Plant-derived inputs can accumulate in the soil and become part of the soil C pool ("new soil C"), or accelerate losses of pre-existing ("old") soil C. The dynamics of the new and old pools will likely differ and alter the long-term fate of soil C, but these separate pools, which can be distinguished through isotopic labeling, have not been considered in past syntheses. Using meta-analysis, we found that while elevated CO2 (ranging from 550 to 800 parts per million by volume) stimulates the accumulation of new soil C in the short term (<1 year), these effects do not persist in the longer term (1-4 years). Elevated CO2 does not affect the decomposition or the size of the old soil C pool over either temporal scale. Our results are inconsistent with predictions of conventional soil C models and suggest that elevated CO2 might increase turnover rates of new soil C. Because increased turnover rates of new soil C limit the potential for additional soil C sequestration, the capacity of land ecosystems to slow the rise in atmospheric CO2 concentrations may be smaller than previously assumed.

Higher yields and lower methane emissions with new rice cultivars.

Breeding high-yielding rice cultivars through increasing biomass is a key strategy to meet rising global food demands. Yet, increasing rice growth can stimulate methane (CH4 ) emissions, exacerbating global climate change, as rice cultivation is a major source of this powerful greenhouse gas. Here, we show in a series of experiments that high-yielding rice cultivars actually reduce CH4 emissions from typical paddy soils. Averaged across 33 rice cultivars, a biomass increase of 10% resulted in a 10.3% decrease in CH4 emissions in a soil with a high carbon (C) content. Compared to a low-yielding cultivar, a high-yielding cultivar significantly increased root porosity and the abundance of methane-consuming microorganisms, suggesting that the larger and more porous root systems of high-yielding cultivars facilitated CH4 oxidation by promoting O2 transport to soils. Our results were further supported by a meta-analysis, showing that high-yielding rice cultivars strongly decrease CH4 emissions from paddy soils with high organic C contents. Based on our results, increasing rice biomass by 10% could reduce annual CH4 emissions from Chinese rice agriculture by 7.1%. Our findings suggest that modern rice breeding strategies for high-yielding cultivars can substantially mitigate paddy CH4 emission in China and other rice growing regions.