Soils store at least twice as much carbon (C) as plant biomass 1 , and, each year, soil microbial respiration releases ~60 Pg of C to the atmosphere as carbon dioxide (CO 2 ) 2 .In the short term, soil microbial respiration increases exponentially with temperature 3 , and thus models predict that warming-induced increases in CO 2 release from soils could represent an important positive feedback to 21 st century climate change 4 . However, the magnitude of this feedback remains uncertain, not least because the adaptation of soil microbial communities to changing temperatures has the potential to either substantially decrease ('compensatory adaptation' 5-7 ) or substantially increase ('enhancing adaptation' 8,9 ) warming-induced C losses. By collecting contrasting soils along a climatic gradient from the Arctic to the Amazon, we undertook the first global analysis of the role microbial thermal adaptation plays in controlling rates of CO 2 release from soils. Here we show that, enhancing adaptation was between three and ten times more common than compensatory adaptation. Furthermore, the strongest enhancing responses were observed in soils with high C contents and from cold climates; enhancing thermal adaptation increased the temperature sensitivity of respiration in these soils by a factor of 1.4. This suggests that the substantial stores of C present in organic and high-latitude soils may be more vulnerable to climate warming than currently predicted. Text:Short-term experiments have demonstrated that the rate of microbial respiration in soil increases exponentially with temperature, and this general relationship has been used in parameterising soil C and Earth system models 4,10 . However, plant physiologists have demonstrated that short-term measurements are inadequate for representing the dynamic response of plant respiration to changes in temperature. In plants, thermal acclimation, defined as the "subsequent adjustment in the rate of respiration to compensate for an initial change in temperature" 11 greatly reduces the impact of temperature change on plant respiration in the medium-to long-term, with major consequences for modelling C-cycle feedbacks to climate change 12 . In soil there is growing evidence of the potential for a similar compensatory effect through microbial adaptation to temperature 13 ('compensatory adaptation': defined here to include the potential for physiological acclimation, adaptation within populations, and changes in microbial community size and structure). However, it is unclear if microbial community-level responses should always be compensatory. In fact, responses that enhance the direct and instantaneous effect of temperature changes on soil respiration ('enhancing adaptation') have also been observed 8,9,14 . To date there has been no large-scale evaluation of the role of microbial adaptation in controlling the temperature sensitivity of soil respiration. This lack of understanding adds considerable uncertainty to predictions of the magnitude and direction of carbon-cycle feedb...
Tropical soils contain a third of global soil carbon 1 , so destabilization of soil organic matter caused by the approximate 4°C warming predicted for tropical regions this century could accelerate climate change by releasing additional carbon dioxide (CO2) to the atmosphere 2-5 . Theory predicts that warming should cause only modest carbon loss in tropical soils relative to those at higher latitudes 4,6 , but there have been no warming experiments in tropical forests to test this prediction 7 . Here we show that in situ experimental warming of a lowland tropical forest soil on Barro Colorado Island, Panama, caused an unexpectedly large increase in soil CO2 emissions. Two years of warming of the whole soil profile by 4 o C increased CO2 emission by 55% compared to soils at ambient temperature. The additional CO2 originated from heterotrophic rather than autotrophic sources and equated to a loss of 8.2 ± 4.2 (± 1 SE) Mg C ha -1 yr -1 from the breakdown of soil organic matter. During this time, we detected no acclimation of respiration rates, no thermal compensation or change in temperature sensitivity of enzyme activities, and no change in microbial carbon-use efficiency. These results demonstrate a high sensitivity of soil carbon in tropical forests to warming, which represents a potentially substantial positive feedback to climate change.
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.
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