Microbial carbon and nitrogen cycling responses to drought and temperature in differently managed mountain grasslands

Grassland management can modify soil microbial carbon (C)and nitrogen (N)cycling, affecting the resistance to extreme weather events, which are predicted to increase in frequency and magnitude in the near future. However, effects of grassland management on microbial C and N cycling and their responses to extreme weather events, such as droughts and heatwaves, have rarely been tested in a combined approach. We therefore investigated whether grassland management affects microbial C and N cycling responses to drought and temperature manipulation. We collected soils from in situ drought experiments conducted in an extensively managed and an abandoned mountain grassland and incubated them at two temperature levels. We measured microbial respiration and substrate incorporation, as well as gross rates of organic and inorganic N cycling to estimate microbial C and N use efficiencies (CUE and NUE). The managed grassland was characterized by lower microbial biomass, lower fungi to bacteria ratio, and higher microbial CUE, but only slightly different microbial NUE. At both sites drought induced a shift in microbial community composition driven by an increase in Gram-positive bacterial abundance. Drought significantly reduced C substrate respiration and incorporation by microbes at both sites, while microbial CUE remained constant. In contrast, drought increased gross rates of N mineralization at both sites, whereas gross amino acid uptake rates only marginally changed. We observed a significant direct, as well as interactive effect between land management and drought on microbial NUE. Increased temperatures significantly stimulated microbial respiration and reduced microbial CUE independent of drought or land management. Although microbial N processing rates showed no clear response, microbial NUE significantly decreased at higher temperatures. In summary in our study, microbial CUE, in particular respiration, is more responsive to temperature changes. Although N processing rates were stronger responding to drought than to temperature microbial NUE was affected by both drought and temperature increase. We conclude that direct effects of drought and heatwaves can induce different responses in soil microbial C and N cycling similarly in the studied land management systems

Microbial carbon limitation : the need for integrating microorganisms into our understanding of ecosystem carbon cycling

Numerous studies have demonstrated that fertilization with nutrients such as nitrogen, phosphorus, and potassium increases plant productivity in both natural and managed ecosystems, demonstrating that primary productivity is nutrient limited in most terrestrial ecosystems. In contrast, it has been demonstrated that heterotrophic microbial communities in soil are primarily limited by organic carbon or energy. While this concept of contrasting limitations, that is, microbial carbon and plant nutrient limitation, is based on strong evidence that we review in this paper, it is often ignored in discussions of ecosystem response to global environment changes. The plant-centric perspective has equated plant nutrient limitations with those of whole ecosystems, thereby ignoring the important role of the heterotrophs responsible for soil decomposition in driving ecosystem carbon storage. To truly integrate carbon and nutrient cycles in ecosystem science, we must account for the fact that while plant productivity may be nutrient limited, the secondary productivity by heterotrophic communities is inherently carbon limited. Ecosystem carbon cycling integrates the independent physiological responses of its individual components, as well as tightly coupled exchanges between autotrophs and heterotrophs. To the extent that the interacting autotrophic and heterotrophic processes are controlled by organisms that are limited by nutrient versus carbon accessibility, respectively, we propose that ecosystems by definition cannot be 'limited' by nutrients or carbon alone. Here, we outline how models aimed at predicting non-steady state ecosystem responses over time can benefit from dissecting ecosystems into the organismal components and their inherent limitations to better represent plant-microbe interactions in coupled carbon and nutrient models

Seasonal fluctuations of extracellular enzyme activities are related to the biogeochemical cycling of C, N and P in a tropical terra-firme forest

Extracellular enzymes (EE) play a vital role in soil nutrient cycling and thus affect terrestrial ecosystem functioning. Yet the drivers that regulate microbial activity, and therefore EE activity, remain under debate. In this study we investigate the temporal variation of soil EE in a tropical terra-firme forest. We found that EE activity peaked during the drier season in association with increased leaf litterfall, which was also reflected in negative relationships between EE activities and precipitation. Soil nutrients were weakly related to EE activities, although extractable N was related to EE activities in the top 5 cm of the soil. These results suggest that soil EE activity is synchronized with precipitation-driven substrate inputs and depends on the availability of N. Our results further indicate high investments in P acquisition, with a higher microbial N demand in the month before the onset of the drier season, shifting to higher P demand towards the end of the drier season. These seasonal fluctuations in the potential acquisition of essential resources imply dynamic shifts in microbial activity in coordination with climate seasonality and resource limitation of central-eastern Amazon forests

Fungal and bacterial utilization of organic substrates depends on substrate complexity and N availability

There is growing evidence of a direct relationship between microbial community composition and function, which implies that distinct microbial communities vary in their functional properties. The aim of this study was to determine whether differences in initial substrate utilization between distinct microbial communities are due to the activities of certain microbial groups. We performed a short-term experiment with beech forest soils characterized by three different microbial communities (winter and summer community, and a community from a tree-girdling plot). We incubated these soils with different 13C-labelled substrates with or without inorganic N addition and analyzed microbial substrate utilization by 13C-phospholipid fatty acid (PLFA) analysis. Our results revealed that the fate of labile C (glucose) was similar in the three microbial communities, despite differences in absolute substrate incorporation between the summer and winter community. The active microbial community involved in degradation of complex C substrates (cellulose, plant cell walls), however, differed between girdling and control plots and was strongly affected by inorganic N addition. Enhanced N availability strongly increased fungal degradation of cellulose and plant cell walls. Our results indicate that fungi, at least in the presence of a high N supply, are the main decomposers of polymeric C substrates

Extracellular enzyme activities in tropical soils are driven by seasonal litter input

Background It is relatively unknown if and how seasonal fluctuations of tropical microbial activity affect soil nutrient availability. In tropical forests, nutrient economics are often considered to be centered around phosphorus, which might be a limiting factor to sustain crucial ecosystem processes, such as primary production and decomposition of organic material, thus in turn affecting microbial processes and associated nutrient dynamics of the forest ecosystem. Aims We investigate seasonal fluctuations in extracellular hydrolytic soil enzyme activities and soil nutrients and its relationship with precipitation and litterfall input, in a lowland tropical forest in the Central Amazon region. Methods We analyzed data obtained from monitoring microbial enzyme activity and nutrient dynamics in litter and soil and use stoichiometric enzyme theory and proportional vectors for assessing relative nutrient limitation throughout a year. Results Our results show that precipitation seasonality was driving leaf litterfall, which was subsequently synchronized with extracellular enzyme activities in soil, such that both litterfall and enzyme activities peaked during the dry season. Conclusions Our study indicates that soil extractable nutrient concentrations were positively related to microbial enzyme activities, which thus highlights the importance of soil microbial processes for nutrient cycling in this phosphorus limited ecosystem. Our results suggest that projected shifts in climate seasonality that result in longer and more pronounced dry seasons, might desynchronize seasonal patterns of aboveground nutrient input and belowground microbial activity, and thus leading to a decoupling of nutrient cycling in tropical forest ecosystems

Do fine root morphological and functional adaptations support regrowth success in a tropical forest restoration experiment?

In early stages of forest succession plants have a high nutrient demand, but it is still a matter of debate if regrowth success of pioneer species is related to plant functional traits favoring fast soil colonization and nutrient acquisition. In general, we would expect trade-offs between plant growth performance and fine root morphological properties in association with different plant life-history strategies. Hence, we hypothesized that fast growing plants should have a more efficient root system that allows them to outcompete slow-growing neighbors in a resource-limited environment. To test our hypothesis we monitored plant successional growth dynamics in a tropical lowland rainforest reforestation experiment conducted in southwest Costa Rica. We collected absorptive roots (<2mm diameter) from plant individuals (comprising 20 tree species and 11 plant families) with different growth dynamics (as indicated by measurements of stem diameter and height). For these samples we assessed a suite of fine root morphological traits, such as legume nodulation status, and furthermore quantified fine root nutrient concentration and phosphatase activities, as well as microbial biomass and phosphatase activity in soils in the close vicinity of fine roots. We found stark differences in fine root characteristics between the tree species investigated in this study, such that fast growing species exhibited relatively larger specific root length and higher turnover, whereas slow growing species tend to rely on mechanical resistance by increasing root tissue density and root life span. Our results suggest that the identified differences in the root trait spectrum between fast and slow growing species reflect plant functional adaptions to resource limitation, edaphic properties and soil microbial symbioses. Our findings further highlight the crucial need to foster our understanding of belowground root morphological and physiological traits during forest succession, especially so when aiming to restore forest ecosystem functioning in formerly intensified land-use systems

Multiple phosphorus acquisition strategies adopted by fine roots in low-fertility soils in Central Amazonia

This is the final version. Available from Springer Verlag via the DOI in this record.Background and aims Ancient Amazon soils are characterised by low concentrations of soil phosphorus (P). Therefore, it is hypothesised that plants may invest a substantial proportion of their resources belowground to adjust their P-uptake strategies, including root morphological, physiological (phosphatase enzyme activities) and biotic (arbuscular mycorrhizal (AM) associations) adaptations. Since these strategies are energy demanding, we hypothesise that trade-offs between morphological traits and root phosphatase exudation and symbiotic associations would occur. Specifically, we expected that plants which invest in finer roots, and therefore have greater ability to explore large soil volumes, would have a high investment in physiological adaptations such as enhanced phosphatase production. In contrast, we expected that plants with predominantly thicker roots would invest more in symbiotic associations, in which carbon is traded for P acquired from AM fungal communities. Methods We collected absorptive roots (<2 mm diameter) from a lowland Central Amazon forest near Manaus, Brazil. We measured fine root diameter, specific root length (SRL), specific root area (SRA), root tissue density (RTD), root phosphatase activity (APase) and arbuscular mycorrhizal (AM) fungi colonisation. Results Root morphological traits were related to APase activity, with higher APase activity in roots with higher SRL and SRA but lower RTD. However, the degree of AM colonisation was not related to any measured root morphological trait. Conclusions Fine absorptive roots likely benefit from having low RTD, high SRL, SRA and APase exudation to acquire P efficiently. However, because AM colonisation was not related to root morphology, we suggest that investment in multiple P-uptake strategies is required for maintaining productivity in Central Amazon forests.Natural Environment Research Council (NERC)Brazilian National Council for Scientific and Technological Development (CNPq)Australian Research Counci

Litter inputs and phosphatase activity affect the temporal variability of organic phosphorus in a tropical forest soil in the Central Amazon

Purpose The tropical phosphorus cycle and its relation to soil phosphorus (P) availability are a major uncertainty in projections of forest productivity. In highly weathered soils with low P concentrations, plant and microbial communities depend on abiotic and biotic processes to acquire P. We explored the seasonality and relative importance of drivers controlling the fluctuation of common P pools via processes such as litter production and decomposition, and soil phosphatase activity. Methods We analyzed intra-annual variation of tropical soil phosphorus pools using a modified Hedley sequential fractionation scheme. In addition, we measured litterfall, the mobilization of P from litter and soil extracellular phosphatase enzyme activity and tested their relation to fluctuations in P- fractions. Results Our results showed clear patterns of seasonal variability of soil P fractions during the year. We found that modeled P released during litter decomposition was positively related to change in organic P fractions, while net change in organic P fractions was negatively related to phosphatase activities in the top 5 cm. Conclusion We conclude that input of P by litter decomposition and potential soil extracellular phosphatase activity are the two main factors related to seasonal soil P fluctuations, and therefore the P economy in P impoverished soils. Organic soil P followed a clear seasonal pattern, indicating tight cycling of the nutrient, while reinforcing the importance of studying soil P as an integrated dynamic system in a tropical forest context

Compared to conventional, ecological intensive management promotes beneficial proteolytic soil microbial communities for agro-ecosystem functioning under climate change-induced rain regimes

Projected climate change and rainfall variability will affect soil microbial communities, biogeochemical cycling and agriculture. Nitrogen (N) is the most limiting nutrient in agroecosystems and its cycling and availability is highly dependent on microbial driven processes. In agroecosystems, hydrolysis of organic nitrogen (N) is an important step in controlling soil N availability. We analyzed the effect of management (ecological intensive vs. conventional intensive) on N-cycling processes and involved microbial communities under climate change-induced rain regimes. Terrestrial model ecosystems originating from agroecosystems across Europe were subjected to four different rain regimes for 263 days. Using structural equation modelling we identified direct impacts of rain regimes on N-cycling processes, whereas N-related microbial communities were more resistant. In addition to rain regimes, management indirectly affected N-cycling processes via modifications of N-related microbial community composition. Ecological intensive management promoted a beneficial N-related microbial community composition involved in N-cycling processes under climate change-induced rain regimes. Exploratory analyses identified phosphorus-associated litter properties as possible drivers for the observed management effects on N-related microbial community composition. This work provides novel insights into mechanisms controlling agro-ecosystem functioning under climate change