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AbstractA decisive set of steps in the terrestrial carbon (C) cycle is the fixation of atmospheric C by plants and the subsequent C‐transfer to rhizosphere microorganisms. With climate change winters are expected to become milder in temperate ecosystems. Although the rate and pathways of rhizosphere C input to soil could be impacted by milder winters, the responses remain unknown. To address this knowledge‐gap, a winter‐warming experiment was established in a seminatural temperate grassland to follow the C flow from atmosphere, via the plants, to different groups of soil microorganisms. In situ 13CO2 pulse labelling was used to track C into signature fatty acids of microorganisms. The winter warming did not result in any changes in biomass of any of the groups of microorganisms. However, the C flow from plants to arbuscular mycorrhizal (AM) fungi, increased substantially by winter warming. Saprotrophic fungi also received large amounts of plant‐derived C—indicating a higher importance for the turnover of rhizosphere C than biomass estimates would suggest—still, this C flow was unaffected by winter warming. AM fungi was the only microbial group positively affected by winter warming—the group with the closest connection to plants. Winter warming resulted in higher plant productivity earlier in the season, and this aboveground change likely induced plant nutrient limitation in warmed plots, thus stimulating the plant dependence on, and C allocation to, belowground nutrient acquisition. The preferential C allocation to AM fungi was at the expense of C flow to other microbial groups, which were unaffected by warming. Our findings imply that warmer winters may shift rhizosphere C‐fluxes to become more AM fungal‐dominated. Surprisingly, the stimulated rhizosphere C flow was matched by increased microbial turnover, leading to no accumulation of soil microbial biomass.

Bacterial and fungal growth rate measurements are sensitive variables to detect changes in environmental conditions. However, while considerable progress has been made in methods to assess the species composition and biomass of fungi and bacteria, information about growth rates remains surprisingly rudimentary. We review the recent history of approaches to assess bacterial and fungal growth rates, leading up to current methods, especially focusing on leucine/thymidine incorporation to estimate bacterial growth and acetate incorporation into ergosterol to estimate fungal growth. We present the underlying assumptions for these methods, compare estimates of turnover times for fungi and bacteria based on them, and discuss issues, including for example elusive conversion factors. We review what the application of fungal and bacterial growth rate methods has revealed regarding the influence of the environmental factors of temperature, moisture (including drying/rewetting), pH, as well as the influence of substrate additions, the presence of plants and toxins. We highlight experiments exploring the competitive and facilitative interaction between bacteria and fungi enabled using growth rate methods. Finally, we predict that growth methods will be an important complement to molecular approaches to elucidate fungal and bacterial ecology, and we identify methodological concerns and how they should be addressed.

AbstractFuture climate warming in the Arctic will likely increase the vulnerability of soil carbon stocks to microbial decomposition. However, it remains uncertain to what extent decomposition rates will change in a warmer Arctic, because extended soil warming could induce temperature adaptation of bacterial communities. Here we show that experimental warming induces shifts in the temperature–growth relationships of bacterial communities, which is driven by community turnover and is common across a diverse set of 8 (sub) Arctic soils. The optimal growth temperature (Topt) of the soil bacterial communities increased 0.27 ± 0.039 (SE) and 0.07 ± 0.028°C per °C of warming over a 0–30°C gradient, depending on the sampling moment. We identify a potential role for substrate depletion and time‐lag effects as drivers of temperature adaption in soil bacterial communities, which possibly explain discrepancies between earlier incubation and field studies. The changes in Topt were accompanied by species‐level shifts in bacterial community composition, which were mostly soil specific. Despite the clear physiological responses to warming, there was no evidence for a common set of temperature‐responsive bacterial amplicon sequence variants. This implies that community composition data without accompanying physiological measurements may have limited utility for the identification of (potential) temperature adaption of soil bacterial communities in the Arctic. Since bacterial communities in Arctic soils are likely to adapt to increasing soil temperature under future climate change, this adaptation to higher temperature should be implemented in soil organic carbon modeling for accurate predictions of the dynamics of Arctic soil carbon stocks.

Global biogeochemical cycles of carbon and other nutrients are increasingly affected by human activities (Griggs et al., 2013). So far, modeling has been central for our understanding of how this will affect ecosystem functioning and the biogeochemical cycling of elements (Treseder et al., 2012). These models adopt a reductive approach built on the flow of elements between pools that are difficult or even impossible to verify with empirical evidence. Furthermore, while some of these models include the response in physiology, ecology and biogeography of primary producers to environmental change, the microbial part of the ecosystem is generally poorly represented or lacking altogether (Stein and Nicol, 2011; Treseder et al., 2012). The principal pool of carbon and other nutrients in soil is the organic matter (Schimel, 1995). The turnover time of this reservoir is governed by the rate at which microorganisms consume it. The rate of organic matter degradation in a soil is determined by both the indigenous microbial community and the environmental conditions (e.g., temperature, pH, soil water capacity, etc.), which govern the biogeochemical activities of the microorganisms (Waksman and Gerretsen, 1931; Schmidt et al., 2011). The dependences of these biogeochemical activity rates on environmental conditions such as pH, moisture and temperature have been frequently studied (Conant et al., 2011; Schmidt et al., 2011). However, while various microorganisms involved in carrying out biogeochemical processes have been identified, biogeochemical process rates are only rarely measured together with microbial growth, and one of the biggest challenges for advancing our understanding of biogeochemical processes is to systematically link biogeochemistry to the rate of specific metabolic processes (Rousk and Baath, 2011; Stein and Nicol, 2011). We also need to identify the factors governing these activities and if it results in feedback mechanisms that alter the growth, activity and interaction between primary producers and microorganisms (Treseder et al., 2012). By determining how different groups of microorganisms respond to individual environmental conditions by allocating e.g. carbon to production of biomass, CO2 and other products, a mechanistic as well as quantitative understanding of formation and decomposition of organic matter, and the production and consumption of greenhouse gases, can be achieved. In this Research Topic, supported by the Swedish research councils' program “Biodiversity and Ecosystem Services in a Changing Landscape” (BECC), we intend to promote an alternative framework to address how cycling of carbon and other nutrients will be altered in a changing environment from the first-principle mechanisms that drive them—namely the ecology, physiology and biogeography of microorganisms. In order to improve the predictive power of current models, the alternative framework supports the development of new models of biogeochemical cycles that factor in microbial physiology, ecology, and biogeochemistry. Our ambition has been richly rewarded by an extensive list of submissions. We are pleased to present contributions including primary research targeting the microbial control of biogeochemistry, comprehensive reviews of how microbial processes and communities relate to biogeochemical cycles, identification of critical challenges that remain, and new perspectives and ideas of how to optimize progress in our understanding of the microbial regulation of biogeochemistry. Our Research Topic presents new findings about the importance of the microbial community composition, their metabolic state, and the activity of enzymes for the fate and degradation of specific substrates such as chitin (Beier and Bertilsson, 2013), the degradation of more complex compounds such as those constituting plant litter (Moorhead et al., 2013; Rinkes et al., 2013), and the metabolism and biogeochemical cycling of one-carbon compounds (Aronson et al., 2013; Basiliko et al., 2013; Kappler and Nouwens, 2013). The environmental control and land-use perturbation of microbial communities and methane production were assessed in a comprehensive review (Aronson et al., 2013) as well as a case study (Basiliko et al., 2013) and a meta-analysis (Holden and Treseder, 2013). Other contributions have focused on how environmental variables that are affected by climate change can modulate microbial activities by e.g. their influence on the production and activity of enzymes (Steinweg et al., 2013), while Bradford (2013) has provided a comprehensive review of how microbial processes respond to warmer temperatures. These reviews are accompanied by a new suggestion for how we can achieve better predictions for microbial responses (and feedbacks) to climate change (de Vries and Shade, 2013), while Moorhead et al. (2013) identify knowledge gaps and provide important insights about how data on microbial communities, environmental conditions, and enzyme activities can be used to better inform enzyme-based models. Several submissions have highlighted the importance for plant-microbial feedbacks for the regulation of organic matter decomposition and formation (Moorhead et al., 2013; Thomson et al., 2013; Churchland and Grayston, under review), the production of biogenic volatile organic compounds (Rinnan et al., 2013), and the community composition of methanogens and sulfate reducing bacteria (Zeleke et al., 2013). A very active research area in soil microbial ecology is presently how small amounts of labile carbon sources can trigger, or “prime,” the decomposition of soil organic matter. A route toward a more general understanding of the regulation of plant-soil interaction for biogeochemistry, that may well facilitate our understanding of “priming effects,” could be the incorporation of stoichiometric concepts (Dijkstra et al., 2013; Mooshammer et al., 2014). Stoichiometric variations in the concentration of nutrients, combined with variations in carbon and nutrient demands of different decomposer groups, also seems to be reflected in the degradation rate of plant litter (Rinkes et al., 2013). A comprehensive review of biogenic fixation of nitrogen demonstrates the importance of interactions between different biogeochemical cycles for nitrogen fixation in ecosystems with nitrogen-limited plant productivity (Rousk et al., 2013). These contributions emphasize that stoichiometric variations in nutrient concentrations are of importance for both factors that could determine the propensity for organic matter to accumulate in an ecosystem, and thus for carbon to be sequestered. Some contributions to this Research Topic have also highlighted methodological challenges that urgently need attention. For instance, the ability of contemporary isotopic tracer methods to estimate microbial contributions to biogeochemical processes could be systematically overestimated (Hobbie and Hobbie, 2013), suggesting that estimates of the turnover of low molecular weight organic compounds, and possibly also for estimations of nitrogen transformation rates, need to be revised. Additionally, there is a need to move from laboratory-based estimations of the microbial role in ecosystem level processes, often omitting crucial components such as the presence of plants, to field-based assessments in intact systems (Rinkes et al., 2013). The contributions to our Research Topic have opened up new horizons and stimulated conceptual developments in our basic understanding of the regulating factors of global biogeochemical cycles. Within this forum, we have begun to bridge Microbial Ecology and Biogeochemistry, connecting microbial activities at the microcosm scale to carbon fluxes at the ecosystem-scale, and linking above- and belowground ecosystem functioning. We are hopeful that we have initiated conceptual developments that can reach far beyond this Research Topic. It is a mere first step, but we are confident it is directed toward a predictive understanding of the microbial regulation of global biogeochemical cycles.

AbstractClimate change predictions suggest that arctic and subarctic ecosystems will be particularly affected by rising temperatures and extreme weather events, including severe heat waves. Temperature is one of the most important environmental factors controlling and regulating microbial decomposition in soils; therefore, it is critical to understand its impact on soil microorganisms and their feedback to climate warming. We conducted a warming experiment in a subarctic birch forest in North Sweden to test the effects of summer heat waves on the thermal trait distributions that define the temperature dependences for microbial growth and respiration. We also determined the microbial temperature dependences 10 and 12 months after the heat wave simulation had ended to investigate the persistence of the thermal trait shifts. As a result of warming, the bacterial growth temperature dependence shifted to become warm‐adapted, with a similar trend for fungal growth. For respiration, there was no shift in the temperature dependence. The shifts in thermal traits were not accompanied by changes in α‐ or β‐diversity of the microbial community. Warming increased the fungal‐to‐bacterial growth ratio by 33% and decreased the microbial carbon use efficiency by 35%, and both these effects were caused by the reduction in moisture the warming treatments caused, while there was no evidence that substrate depletion had altered microbial processes. The warm‐shifted bacterial thermal traits were partially restored within one winter but only fully recovered to match ambient conditions after 1 year. To conclude, a summer heat wave in the Subarctic resulted in (i) shifts in microbial thermal trait distributions; (ii) lower microbial process rates caused by decreased moisture, not substrate depletion; and (iii) no detectable link between the microbial thermal trait shifts and community composition changes.

We show that the explosive microbial and biogeochemical dynamics triggered by rewetting dry soil in laboratory experiments also has relevance in intact ecosystems. This highlights an opportunity to use predictions derived from laboratory studies to provide targets in ecosystem-scale biogeochemical studies.

ABSTRACTClimate change is causing an intensification of soil drying and rewetting events, altering microbial functioning and potentially destabilizing soil organic carbon. After rewetting, changes in microbial community carbon use efficiency (CUE), investment in life history strategies, and fungal to bacterial dominance co‐occur. Still, we have yet to generalize what drives these dynamic responses. Here, we collated 123 time series of microbial community growth (G, sum of fungal and bacterial growth, evaluated by leucine and acetate incorporation, respectively) and respiration (R) after rewetting and calculated CUE = G/(G + R). First, we characterized CUE recovery by two metrics: maximum CUE and time to maximum CUE. Second, we translated microbial growth and respiration data into microbial investments in life history strategies (high yield (Y), resource acquisition (A), and stress tolerance (S)). Third, we characterized the temporal change in fungal to bacterial dominance. Finally, the metrics describing the CUE recovery, investment in life history strategies, and fungal to bacterial dominance after rewetting were explained by environmental factors and microbial properties. CUE increased after rewetting as fungal dominance declined, but the maximum CUE was explained by the CUE under moist conditions, rather than specific environmental factors. In contrast, higher soil pH and carbon availability accelerated the decline of microbial investment in stress tolerance and fungal dominance. We conclude that microbial CUE recovery is mostly driven by the shifting microbial community composition and the metabolic capacity of the community, whereas changes in microbial investment in life history strategies and fungal versus bacterial dominance depend on soil pH and carbon availability.

Fungal (acetate-in-ergosterol incorporation) and bacterial (leucine/thymidine incorporation) growth resulting from alfalfa (C/N=15) and barley straw (C/N=75) addition was studied in soil microcosms for 64 days. Nitrogen amendments were used to compensate for the C/N difference between the substrates. Fungal growth increased to a maximum after 3-7 days, at five to eight times the controls, following the addition of straw, and three to four times the controls following the addition of alfalfa. After 20-30 days, the fungal growth rate converged with the controls, resulting in a cumulative fungal growth two to three times the controls following straw addition and about 20% higher than the controls following alfalfa addition. The bacterial growth rate reached rates five times the controls following alfalfa addition and twice that of the controls following straw addition after 3-7 days. It remained elevated after 64 days. The cumulative bacterial growth was two and four times the controls following straw and alfalfa addition, respectively. A negative correlation was found between N addition and bacterial growth, while N stimulated fungal growth. Thus, the C/N ratio of the additions (substrate and extra N) could not entirely explain the different results regarding fungal and bacterial growths. Respiration was not always related to the combined growth of the microorganisms, emphasizing the requirement for a better understanding of growth efficiencies of fungi and bacteria.