Andrew T. Nottingham

Temperature sensitivity of soil respiration rates enhanced by microbial community response

Soils store about four times as much carbon as plant biomass, and soil microbial respiration releases about 60 petagrams of carbon per year to the atmosphere as carbon dioxide. Short-term experiments have shown that soil microbial respiration increases exponentially with temperature. This information has been incorporated into soil carbon and Earth-system models, which suggest that warming-induced increases in carbon dioxide release from soils represent an important positive feedback loop that could influence twenty-first-century climate change. The magnitude of this feedback remains uncertain, however, not least because the response of soil microbial communities to changing temperatures has the potential to either decrease or increase warming-induced carbon losses substantially. Here we collect soils from different ecosystems along a climate gradient from the Arctic to the Amazon and investigate how microbial community-level responses control the temperature sensitivity of soil respiration. We find that the microbial community-level response more often enhances than reduces the mid- to long-term (90 days) temperature sensitivity of respiration. Furthermore, the strongest enhancing responses were observed in soils with high carbon-to-nitrogen ratios and in soils from cold climatic regions. After 90 days, microbial community responses increased the temperature sensitivity of respiration in high-latitude soils by a factor of 1.4 compared to the instantaneous temperature response. This suggests that the substantial carbon stores in Arctic and boreal soils could be more vulnerable to climate warming than currently predicted.

Priming and microbial nutrient limitation in lowland tropical forest soils of contrasting fertility

Priming is an increase in soil organic carbon decomposition following input of labile organic carbon. In temperate soils where biological activity is limited commonly by nitrogen availability, priming is expected to occur through microbial acquisition of nitrogen from organic matter or stimulated activity of recalcitrant-carbon degrading microorganisms. However, these priming mechanisms have not yet been assessed in strongly weathered tropical forest soils where biological activity is often limited by the availability of phosphorus. We examined whether microbial nutrient limitation or community dynamics drive priming in three lowland tropical forest soils of contrasting fertility (‘low’, ‘mid’ and ‘high’) by applying C4-sucrose (alone or in combination with nutrients; nitrogen, phosphorus and potassium) and measuring (1) the δ13C-signatures in respired CO2 and in phospholipid fatty acid (PLFA) biomarkers, and (2) the activities of enzymes involved in nitrogen (N-acetyl β-glucosaminidase), phosphorus (phosphomonoesterase) and carbon (β-glucosidase, cellobiohydrolase, xylanase, phenol oxidase) acquisition from organic compounds. Priming was constrained in part by nutrient availability, because priming was greater when sucrose was added alone compared to when added with nutrients. However, the greatest priming with sucrose addition alone was detected in the medium fertility soil. Priming occurred in parallel with stimulated activity of phosphomonoesterase and phenol oxidase (but not N-acetyl β-glucosaminidase); when sucrose was added with nutrients there were lower activities of phosphomonoesterase and phenol oxidase. There was no evidence according to PLFA δ13C-incorporation that priming was caused by specific groups of recalcitrant-carbon degrading microorganisms. We conclude that priming occurred in the intermediate fertility soil following microbial mineralization of organic nutrients (phosphorus in particular) and suggest that priming was constrained in the high fertility soil by high nutrient availability and in the low fertility soil by the low concentration of soil organic matter amenable to priming. This first study of priming mechanisms in tropical forest soils indicates that input of labile carbon can result in priming by microbial mineralization of organic nutrients, which has important implications for understanding the fate of organic carbon in tropical forest soils.

Microbial community composition explains soil respiration responses to changing carbon inputs along an Andes-to-Amazon elevation gradient

1. The Andes are predicted to warm by 3–5 °C this century with the potential to alter the processes regulating carbon (C) cycling in these tropical forest soils. This rapid warming is expected to stimulate soil microbial respiration and change plant species distributions, thereby affecting the quantity and quality of C inputs to the soil and influencing the quantity of soil-derived CO2 released to the atmosphere. 2. We studied tropical lowland, premontane and montane forest soils taken from along a 3200-m elevation gradient located in south-east Andean Peru. We determined how soil microbial communities and abiotic soil properties differed with elevation. We then examined how these differences in microbial composition and soil abiotic properties affected soil C-cycling processes, by amending soils with C substrates varying in complexity and measuring soil heterotrophic respiration (RH). 3. Our results show that there were consistent patterns of change in soil biotic and abiotic properties with elevation. Microbial biomass and the abundance of fungi relative to bacteria increased significantly with elevation, and these differences in microbial community composition were strongly correlated with greater soil C content and C:N (nitrogen) ratios. We also found that RH increased with added C substrate quality and quantity and was positively related to microbial biomass and fungal abundance. 4. Statistical modelling revealed that RH responses to changing C inputs were best predicted by soil pH and microbial community composition, with the abundance of fungi relative to bacteria, and abundance of gram-positive relative to gram-negative bacteria explaining much of the model variance. 5. Synthesis. Our results show that the relative abundance of microbial functional groups is an important determinant of RH responses to changing C inputs along an extensive tropical elevation gradient in Andean Peru. Although we do not make an experimental test of the effects of climate change on soil, these results challenge the assumption that different soil microbial communities will be ‘functionally equivalent’ as climate change progresses, and they emphasize the need for better ecological metrics of soil microbial communities to help predict C cycle responses to climate change in tropical biomes.

Arbuscular mycorrhizal mycelial respiration in a moist tropical forest.

*Arbuscular mycorrhizal fungi (AMF) are widespread in tropical forests and represent a major sink of photosynthate, yet their contribution to soil respiration in such ecosystems remains unknown. *Using in-growth mesocosms we measured AMF mycelial respiration in two separate experiments: (1) an experiment in a semi-evergreen moist tropical forest, and (2) an experiment with 6-m-tall Pseudobombax septenatum in 4.5-m(3) containers, for which we also determined the dependence of AMF mycelial respiration on the supply of carbon from the plant using girdling and root-cutting treatments. *In the forest, AMF mycelia respired carbon at a rate of 1.4 t ha(-1) yr(-1), which accounted for 14 +/- 6% of total soil respiration and 26 +/- 12% of root-derived respiration. For P. septenatum, 40 +/- 6% of root-derived respiration originated from AMF mycelia and carbon was respired < 4 h after its supply from roots. *We conclude that arbuscular mycorrhizal mycelial respiration can be substantial in lowland tropical forests. As it is highly dependent on the recent supply of carbon from roots, a function of aboveground fixation, AMF mycelial respiration is therefore an important pathway of carbon flux from tropical forest trees to the atmosphere.

Root and arbuscular mycorrhizal mycelial interactions with soil microorganisms in lowland tropical forest

Tropical forests have high rates of soil carbon cycling, but little information is available on how roots, arbuscular mycorrhizal fungi (AMF), and free-living microorganisms interact and influence organic matter mineralization in these ecosystems. We used mesh ingrowth cores and isotopic tracers in phospholipid fatty acid biomarkers to investigate the effects of roots and AMF mycelia on (1) microbial community composition, microbial carbon utilization, and hydrolytic enzyme activities for large, potted tropical trees and (2) enzyme activities and litter mass loss in a lowland tropical forest. Under the tropical tree, plant-derived carbon was incorporated predominantly into bacterial groups in both rhizosphere and AMF-only soils. Gram-positive bacteria incorporated additional soil-derived carbon in rhizosphere soils, which also contained the highest microbial biomass. For hydrolytic enzymes, β-glucosidase and N-acetyl β-glucosaminidase activities were highest in rhizosphere soils, while phosphomonoesterase activity was highest in AMF-only soil. In the forest, leaf litter mass loss was increased by the presence of roots, but not by the presence of AMF mycelia only. Root-microbial interactions influenced organic matter cycling, with evidence for rhizosphere priming and accelerated leaf litter decomposition in the presence of roots. Although AMF mycelia alone did not stimulate organic matter mineralization, they were a conduit of carbon to other soil microorganisms.

Climate Warming and Soil Carbon in Tropical Forests: Insights from an Elevation Gradient in the Peruvian Andes

The temperature sensitivity of soil organic matter (SOM) decomposition in tropical forests will influence future climate. Studies of a 3.5-kilometer elevation gradient in the Peruvian Andes, including short-term translocation experiments and the examination of the long-term adaptation of biota to local thermal and edaphic conditions, have revealed several factors that may regulate this sensitivity. Collectively this work suggests that, in the absence of a moisture constraint, the temperature sensitivity of decomposition is regulated by the chemical composition of plant debris (litter) and both the physical and chemical composition of preexisting SOM: higher temperature sensitivities are found in litter or SOM that is more chemically complex and in SOM that is less occluded within aggregates. In addition, the temperature sensitivity of SOM in tropical montane forests may be larger than previously recognized because of the presence of “cold-adapted” and nitrogen-limited microbial decomposers and the possible future alterations in plant and microbial communities associated with warming. Studies along elevation transects, such as those reviewed here, can reveal factors that will regulate the temperature sensitivity of SOM. They can also complement and guide in situ soil-warming experiments, which will be needed to understand how this vulnerability to temperature may be mediated by altered plant productivity under future climatic change.

Microbial carbon mineralization in tropical lowland and montane forest soils of Peru

Climate change is affecting the amount and complexity of plant inputs to tropical forest soils. This is likely to influence the carbon (C) balance of these ecosystems by altering decomposition processes e.g., “positive priming effects” that accelerate soil organic matter mineralization. However, the mechanisms determining the magnitude of priming effects are poorly understood. We investigated potential mechanisms by adding 13C labeled substrates, as surrogates of plant inputs, to soils from an elevation gradient of tropical lowland and montane forests. We hypothesized that priming effects would increase with elevation due to increasing microbial nitrogen limitation, and that microbial community composition would strongly influence the magnitude of priming effects. Quantifying the sources of respired C (substrate or soil organic matter) in response to substrate addition revealed no consistent patterns in priming effects with elevation. Instead we found that substrate quality (complexity and nitrogen content) was the dominant factor controlling priming effects. For example a nitrogenous substrate induced a large increase in soil organic matter mineralization whilst a complex C substrate caused negligible change. Differences in the functional capacity of specific microbial groups, rather than microbial community composition per se, were responsible for these substrate-driven differences in priming effects. Our findings suggest that the microbial pathways by which plant inputs and soil organic matter are mineralized are determined primarily by the quality of plant inputs and the functional capacity of microbial taxa, rather than the abiotic properties of the soil. Changes in the complexity and stoichiometry of plant inputs to soil in response to climate change may therefore be important in regulating soil C dynamics in tropical forest soils.

Temperature drives plant and soil microbial diversity patterns across an elevation gradient from the Andes to the Amazon

More than 200 years ago, von Humboldt reported decreases in tropical plant species richness with increasing elevation and decreasing temperature. Surprisingly, co-ordinated patterns in plant, bacterial and fungal diversity on tropical mountains are yet to be observed, despite the central role of soil microorganisms in terrestrial biogeochemistry. We studied an Andean transect traversing 3.5 km in elevation to test whether the species diversity and composition of tropical forest plants, soil bacteria and fungi can follow similar biogeographical patterns with shared environmental drivers. We found co-ordinated changes with elevation in all three groups: species richness declined as elevation increased, and the compositional-dissimilarity of communities increased with increased separation in elevation, although changes in plant diversity were larger than in bacteria and fungi. Temperature was the dominant driver of these diversity gradients, with weak influences of edaphic properties, including soil pH. The gradients in microbial diversity were strongly correlated with the activities of enzymes involved in organic matter cycling, and were accompanied by a transition in microbial traits towards slower-growing, oligotrophic taxa at higher elevations. We provide the first evidence of co-ordinated temperature-driven patterns in the diversity and distribution of three major biotic groups in tropical ecosystems: soil bacteria, fungi and plants. These findings suggest that, across landscape scales of relatively constant soil pH, inter-related patterns of plant and microbial communities with shared environmental drivers can occur, with large implications for tropical forest communities under future climate change.Climate strongly regulates plant community composition and diversity, exemplified by gradients in plant diversity and community structure with elevation. However, we do not know if soil bacteria and fungi, key drivers of terrestrial biogeochemical cycling, follow similar biogeographical patterns determined by the same climatic drivers. We studied an Andean tropical forest transect traversing 3.5 km in elevation. The species richness (α-diversity) and compositional dissimilarity of communities (β-diversity) were determined for plants, bacteria and fungi. We determined the environmental drivers of these patterns, using 31 environmental and edaphic predictor variables, and the relationship between microbial communities and soil organic matter cycling (extracellular enzymes). We found co-ordinated changes with elevation in the species richness and composition of plants, soil bacteria and fungi. Across all groups, α-diversity declined significantly as elevation increased, and β-diversity increased with increased elevation difference. Temperature was the dominant driver of these diversity gradients, with only weak influences of edaphic properties, including soil pH, which did not vary substantially across the study transect. The gradients in microbial diversity were strongly correlated with the activities of enzymes involved in soil organic matter cycling, and were accompanied by a transition in microbial traits, towards slower-growing, more oligotrophic taxa at higher elevations. We provide the first evidence of co-ordinated temperature-driven patterns in the diversity and distribution of plants, soil bacteria and fungi in tropical ecosystems. This finding suggest that, across landscape scales of relatively constant soil pH, shared patterns and environmental drivers of plant and microbial communities can occur, with large implications for tropical forest communities under future climate change.

Nutrient limitations to bacterial and fungal growth during cellulose decomposition in tropical forest soils

Nutrients constrain the soil carbon cycle in tropical forests, but we lack knowledge on how these constraints vary within the soil microbial community. Here, we used in situ fertilization in a montane tropical forest and in two lowland tropical forests on contrasting soil types to test the principal hypothesis that there are different nutrient constraints to different groups of microorganisms during the decomposition of cellulose. We also tested the hypotheses that decomposers shift from nitrogen to phosphorus constraints from montane to lowland forests, respectively, and are further constrained by potassium and sodium deficiency in the western Amazon. Cellulose and nutrients (nitrogen, phosphorus, potassium, sodium, and combined) were added to soils in situ, and microbial growth on cellulose (phospholipid fatty acids and ergosterol) and respiration were measured. Microbial growth on cellulose after single nutrient additions was highest following nitrogen addition for fungi, suggesting nitrogen as the primary limiting nutrient for cellulose decomposition. This was observed at all sites, with no clear shift in nutrient constraints to decomposition between lowland and montane sites. We also observed positive respiration and fungal growth responses to sodium and potassium addition at one of the lowland sites. However, when phosphorus was added, and especially when added in combination with other nutrients, bacterial growth was highest, suggesting that bacteria out-compete fungi for nitrogen where phosphorus is abundant. In summary, nitrogen constrains fungal growth and cellulose decomposition in both lowland and montane tropical forest soils, but additional nutrients may also be of critical importance in determining the balance between fungal and bacterial decomposition of cellulose.

Microbes follow Humboldt: temperature drives plant and soil microbial diversity patterns from the Amazon to the Andes

Abstract More than 200 years ago, Alexander von Humboldt reported that tropical plant species richness decreased with increasing elevation and decreasing temperature. Surprisingly, coordinated patterns in plant, bacterial, and fungal diversity on tropical mountains have not yet been observed, despite the central role of soil microorganisms in terrestrial biogeochemistry and ecology. We studied an Andean transect traversing 3.5 km in elevation to test whether the species diversity and composition of tropical forest plants, soil bacteria, and fungi follow similar biogeographical patterns with shared environmental drivers. We found coordinated changes with elevation in all three groups: species richness declined as elevation increased, and the compositional dissimilarity among communities increased with increased separation in elevation, although changes in plant diversity were larger than in bacteria and fungi. Temperature was the dominant driver of these diversity gradients, with weak influences of edaphic properties, including soil pH. The gradients in microbial diversity were strongly correlated with the activities of enzymes involved in organic matter cycling, and were accompanied by a transition in microbial traits towards slower‐growing, oligotrophic taxa at higher elevations. We provide the first evidence of coordinated temperature‐driven patterns in the diversity and distribution of three major biotic groups in tropical ecosystems: soil bacteria, fungi, and plants. These findings suggest that interrelated and fundamental patterns of plant and microbial communities with shared environmental drivers occur across landscape scales. These patterns are revealed where soil pH is relatively constant, and have implications for tropical forest communities under future climate change.