Simulated climate change and seasonal drought increase carbon and phosphorus demand in Mediterranean forest soils
Introduction
Climate models predict changes in precipitation patterns with increasing risk of drought (IPCC, 2014), a disturbance that induces physiological, physical and chemical perturbations to the soil system and profoundly alters carbon (C) and nutrient biogeochemistry (Van der Molen et al., 2011). However, our knowledge about how microbial functions respond to changing environmental conditions is still highly limited, thus the uncertainty of terrestrial C projections remains high (Berardi et al., 2020; Luo et al., 2016; Sulman et al., 2018).
Soil extracellular enzyme (EE) allocation patterns, as represented by enzyme stoichiometry, are good indicators of C and nutrient demands of soil organisms (but see Rosinger et al., 2019) and bioavailability of resources (Allison and Vitousek, 2004; Arnosti et al., 2014). Enzyme production increases in response to limiting nutrient resources and decays when nutrient resources are abundant, but ultimately, microbial resource allocation to different EEs is constrained by C and nitrogen (N) availability (Schimel and Weintraub, 2003). Our understanding of how the interactions between nutrient resources and soil water availabilities control enzyme production in soils is still very limited; yet, this knowledge is crucial to predict changes in biogeochemical cycles under future climate scenarios.
Drought limits soil extracellular enzyme activity directly through the reduction in substrate diffusion and accessibility imposed under low soil moisture conditions (Schimel, 2018), which in turn reduces substrate affinity (Tang and Riley, 2019) and hydrolytic reaction rates (Fuchslueger et al., 2016; Sardans and Peñuelas, 2010; Trasar-Cepeda et al., 2007). Indirectly, the physiological stress experienced under drought conditions decreases microbial and plant activity and so enzyme production declines as well (Allison et al., 2011). At longer temporal scales (seasonal to years) drought increases the pool of potentially available resources for microbial communities, via the increase in microbial necromass, litterfall (Ogaya and Penuelas, 2004; Schimel, 2018) and root-derived C (Preece and Peñuelas, 2016) and also induces changes in the stoichiometric composition of plants (Sardans et al., 2008; Sardans and Peñuelas, 2007a) thus altering the stoichiometry of the resources for heterotrophic microbial communities. Which is the outcome of these drought trade-offs at different time scales on the allocation to different C, N and P-acquiring enzymes by soil organisms, and how do the natural (seasonal) changes in soil moisture and plant and microbial physiology modulate this outcome?
While physical diffusion constraints under low soil moisture may affect equally the overall hydrolytic enzyme activity in soil (meaning the maximum potential activity of all hydrolytic enzymes active in the soil) (Sardans and Peñuelas, 2005, 2010), the initial concentration of substrates near the enzyme producers and the distance of substrates to the producers can be determining the enzyme synthesis strategies adopted by soil organisms, as shown by a mechanistic model of the effects of water on soil C fluxes (Manzoni et al., 2014). However, this model assumed no limitation by nutrients, which contrasts with the nature of many ecosystems.
A field study of soil enzyme stoichiometry in forest ecosystems along a North-South transect in eastern China showed that changes in soil enzyme stoichiometry were correlated with fluctuations in nutrient availability which were determined by mean annual temperature and precipitation (MAT and MAP) (Xu et al., 2017). Another field study showed significant seasonal change in soil enzyme stoichiometry associated with increased maintenance cost with freezing events in a temperate climate ecosystem (perennial grasses and forbs) (Steinweg et al., 2013). In the same study, enzyme stoichiometry was not affected by experimental drought (50% of ambient precipitation during one year). These two studies, however, were performed in ecosystems where water was not the main limitation, unlike semi-arid Mediterranean climate ecosystems that tend to be water and nutrient limited (Dirks et al., 2019). To our knowledge, there are few studies on the effects of changes in diffusion rates and substrate accessibility induced by decreased water availability in combination with nutrient scarcity, on enzyme stoichiometry in Mediterranean ecosystems (Zuccarini et al., 2020). Long-term field experiments examining the effects of drought on soil enzyme activity in dry ecosystems are thus highly needed because they integrate the ecosystem-level responses to drought and provide empirical evidence for testing the fundamental assumptions underlying mechanistic models.
In order to understand the complex interactions between drought and enzyme allocation strategies and fill the data gap in dry ecosystems, we investigated seasonal allocation strategies and responses of plant-microorganism EEs to prolonged drought in an experiment that had partially excluded rainfall and surface runoff for 16 years in a Mediterranean holm oak forest (Sardans and Peñuelas, 2005). We have interpreted the effects of changing environmental conditions on soil enzyme allocation patterns within the theoretical framework of optimum allocation theory and economic principles: soil communities should invest in the most needed resource maximizing the benefit:cost ratio of enzyme production (Allison et al., 2011). In addition, we have used the enzyme vector analysis developed by (Moorhead et al., 2016) that helps to interpret the relative resource demands of the microbial community independent of variations in total enzyme activity.
Our main hypothesis was that moisture strongly influences P and N-enzymes thus regulating the availability of nutrients in semi-arid ecosystems. To test this hypothesis, we investigated the enzyme production, resource availability, and enzyme stoichiometry in response to seasonal and climate change-simulated drought. We expected 1) a decreased activity of all enzymes depending on the relative availability of different substrates, 2) a higher investment in P-enzymes than in other enzymes reflected in low C/P and N/P enzyme ratios, and 3) a decreased short-term available inorganic P/organic P ratios as a result of increasing litterfall production which, in turn, would increase the activity of phosphatase relative to the activity of other enzymes.
Section snippets
Study site
The study was carried out in the Prades mountains, Catalonia, on the northeastern Iberian Peninsula (41°21′N, 1°2′E). The climate is typically Mediterranean, with hot and dry summers (June to August mean temperature and total precipitation: 19.4 °C and 100 mm, respectively), and mild, rainy springs (March to May mean temperature and total precipitation: 10.4 °C and 208.9 mm, respectively) and autumns (September to November mean temperature: 12.4 °C and 203.1 mm, respectively). The site has been
Climate
Average temperature and total rainfall for the study year (2014) were consistent with average values reported for the study site; however, average precipitation in January was much greater than the 60 year-series mean (1950–2010; Servei Meteorològic de Catalunya) (74.9 mm vs 29.2 ± 5.0 mm). Overall soil water content at the study site was greatest in winter, followed by spring and autumn, and it was reduced in the drought treatment by 33% across the year, especially in winter (P < 0.05, Fig. 1
Discussion
Evidence of higher investment in P acquisition than in C and N in low rainfall Mediterranean soil forests.
Based on the sensitivity of soil P concentrations and chemical forms to soil water availability in this low-rainfall Mediterranean forest (Sardans and Peñuelas, 2004, 2007b), our hypothesis that drought induces greater investment in P-acquiring enzymes was confirmed by the lower ratios of C/P and N/P enzymes than in other ecosystems. We found that average C/P and N/P enzyme ratios were
Summary and conclusions
We found that C/P and N/P enzyme ratios from the Mediterranean forest were lower than from other ecosystems and the V_angle values were consistently >45°, indicating higher levels of investment by soil organisms for the acquisition of P than for C and N in this ecosystem.
The C/N and C/P enzyme ratios and V_length showed that seasonal and experimental drought increased the relative C vs. N and P demand of soil microbial communities. It is likely that, under prolonged experimental drought
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
The authors would like to acknowledge the financial support from the European Research Council Synergy grant ERC-SyG2013-610028 IMBALANCE-P, the Spanish Government grant PID2019-110521 GB-I00, the Fundación Ramón Areces grant ELEMENTAL-CLIMATE, and the Catalan Government grant SGR 2017-1005.
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