Deciphering microbiomes dozens of meters under our feet and their edaphoclimatic and spatial drivers

24 páginas.- 7 figuras.- referenciasMicrobes inhabiting deep soil layers are known to be different from their counterpart in topsoil yet remain under investigation in terms of their structure, function, and how their diversity is shaped. The microbiome of deep soils (>1 m) is expected to be relatively stable and highly independent from climatic conditions. Much less is known, however, on how these microbial communities vary along climate gradients. Here, we used amplicon sequencing to investigate bacteria, archaea, and fungi along fifteen 18-m depth profiles at 20-50-cm intervals across contrasting aridity conditions in semi-arid forest ecosystems of China's Loess Plateau. Our results showed that bacterial and fungal α diversity and bacterial and archaeal community similarity declined dramatically in topsoil and remained relatively stable in deep soil. Nevertheless, deep soil microbiome still showed the functional potential of N cycling, plant-derived organic matter degradation, resource exchange, and water coordination. The deep soil microbiome had closer taxa-taxa and bacteria-fungi associations and more influence of dispersal limitation than topsoil microbiome. Geographic distance was more influential in deep soil bacteria and archaea than in topsoil. We further showed that aridity was negatively correlated with deep-soil archaeal and fungal richness, archaeal community similarity, relative abundance of plant saprotroph, and bacteria-fungi associations, but increased the relative abundance of aerobic ammonia oxidation, manganese oxidation, and arbuscular mycorrhizal in the deep soils. Root depth, complexity, soil volumetric moisture, and clay play bridging roles in the indirect effects of aridity on microbes in deep soils. Our work indicates that, even microbial communities and nutrient cycling in deep soil are susceptible to changes in water availability, with consequences for understanding the sustainability of dryland ecosystems and the whole-soil in response to aridification. Moreover, we propose that neglecting soil depth may underestimate the role of soil moisture in dryland ecosystems under future climate scenarios.This project was supported by the Joint Key Funds of the National Natural Science Foundation of China (U21A20237), the Strategic Priority Research Program of Chinese Academy of Sciences (XDB40020202). M.D.-B. acknowledges support from TED2021-130908B-C41/AEI/10.13039/501100011033/Unión Europea NextGenerationEU/PRTR and from the Spanish Ministry of Science and Innovation for the I + D + i project PID2020-115813RA-I00 funded by MCIN/AEI/10.13039/501100011033. R.O.H. was funded by the Ramón y Cajal program of the MICINN (RYC-2017 22032), by the R&D Project of the Ministry of Science and Innovation PID2019-106004RA-I00 funded by MCIN/AEI/10.13039/501100011033, and by the European Agricultural Fund for Rural Development (EAFRD) through the “Aid to operational groups of the European Association of Innovation (AEI) in terms of agricultural productivity and sustainability,” Reference: GOPC-CA-20-0001Peer reviewe

Pathways from research to sustainable development: insights from ten research projects in sustainability and resilience

Drawing on collective experience from ten collaborative research projects focused on the Global South, we identify three major challenges that impede the translation of research on sustainability and resilience into better-informed choices by individuals and policy-makers that in turn can support transformation to a sustainable future. The three challenges comprise: (i) converting knowledge produced during research projects into successful knowledge application; (ii) scaling up knowledge in time when research projects are short-term and potential impacts are long-term; and (iii) scaling up knowledge across space, from local research sites to larger-scale or even global impact. Some potential pathways for funding agencies to overcome these challenges include providing targeted prolonged funding for dissemination and outreach, and facilitating collaboration and coordination across different sites, research teams, and partner organizations. By systematically documenting these challenges, we hope to pave the way for further innovations in the research cycle

Do the respiration pulses induced by drying–rewetting matter for the soil–atmosphere carbon balance?

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.[Image: see text

Soil depth and tillage can characterize the soil microbial responses to drying-rewetting

The influence of climate on soil microorganisms governs the input and output fluxes of carbon (C) from soils. The study of the drastic responses to drying-rewetting offers an opportunity to assess an aspect of ‘soil health’ via evaluating the role of microbes in soil biochemistry and C cycling. Recent evidence has consistently shown that communities exposed to extreme moisture fluctuations recurrently can better cope with the stress generated by them and exhibit a ‘resilient’ microbial response after rewetting (fast recovery of microbial communities to the pre-disturbance growth levels), whereas otherwise they show a more ‘sensitive’ response (slow recovery). However, it is still not known if land-use management can alter these responses. In this study, we investigated this issue by performing a drying-rewetting experiment on soil samples from two land-uses (permanent pastures and tilled croplands) and two depths (0–5 cm and 20–30 cm), and measured bacterial growth, fungal growth, and respiration at high temporal resolution. We then derived a series of indicators of soil health based on the characteristics of these microbial responses to drying-rewetting. Results showed categorically different patterns in soils from pastures and croplands, confirming the capacity of land use to change soil functioning. Tillage practices cancelled the stratification in the top 30 cm of soil and increased the exposure and adaptation of soil microorganisms to conditions of water stress, which caused shifts in the microbial responses to drying-rewetting. The sensitive patterns in bacterial growth found in undisturbed pastures were replaced by resilient responses in both shallow and deep croplands. Fungi showed a tendency for faster recoveries in croplands but patterns were consistently resilient in all sites and depths, indicating that fungi were little affected by land-use-induced dis- turbances. Respiration exhibited resilient-like responses in shallow samples, but in depth, they were sensitive in pastures and resilient in croplands. We also observed an alternated sequence of bacterial and fungal growth over time that suggested competition and different strategies of reactivation after rewetting by the two types of microorganisms

A soil microbial model to analyze decoupled microbial growth and respiration during soil drying and rewetting

Soils are continuously exposed to cycles of drying and rewetting (D/RW), which drive pronounced fluctuations in soil carbon (C) fluxes. These C dynamics are characterized by a decoupled behavior between microbial biomass synthesis (growth) and CO2 production (respiration). In general, respiration rates peak shortly after RW and subsequently decrease, while the growth peaks lag several hours behind. Despite the significance of these dynamics for the soil C budget and the global C cycle, this feature has so far been overlooked in biogeochemical models and the underlying mechanisms are still unclear. We present a new process-based soil microbial model that incorporates a wide range of physical, chemical and biological mechanisms thought to affect D/RW responses. Results show that the model is able to capture the respiration dynamics in soils exposed to repeated cycles of D/RW, and also to single events in which moisture was kept constant after RW. In addition, the model reproduces, for the first time, the responses of microbial growth to D/RW. We have identified the C accumulation during dry periods, the drought-legacy effect on the synthesis of new biomass, and osmoregulation as the strongest candidate mechanisms to explain these C dynamics. The model outputs are further compared to earlier process-based models, highlighting the advances generated by the new model. This work thus represents a step towards unravelling the microbial responses to drought and rainfall events, with implications for our understanding of C cycle and C sequestration in soils

Higher resistance and resilience of bacterial growth to drought in grasslands with historically lower precipitation

Climate change is expected to alter precipitation regimes, resulting in longer periods of drought and heavier precipitation events. Even though the direct effect of water availability on soil microbial processes is well documented, the influence of precipitation legacy on microbial resistance and resilience to drought remains unclear. Using soils from a natural mean annual precipitation (MAP) gradient (∼550–950 mm yr−1) equipped with long-term (>8 yr) rain-out shelters, we investigated how the history of precipitation influenced microbial ‘resistance’ (tolerance to drying) and ‘resilience’ (ability to recover growth rates following rewetting) to drought. We found that bacterial growth was more resistant and resilient to drought in sites with lower MAP. In contrast, the precipitation-reduction treatments had no detectable influence on microbial drought resistance or resilience. The microbial carbon-use efficiency immediately after rewetting was higher in soils from lower precipitation sites. In contrast, the steady-state microbial growth rates and respiration (under standardized moisture conditions) were consistent along the precipitation gradient. The variation in microbial drought resistance and resilience across the precipitation gradient was linked to the microbial community structure. Taken together, our results suggest that historical precipitation regimes – and the associated differences in exposure to drought – had selected for bacterial communities that were more resistant and resilient to drought

Comparing soil microbial responses to drying-rewetting and freezing-thawing events

Climate change is expected to alter the frequency and intensity of soil drying-rewetting (D/RW) and freezing-thawing (F/TW) events, with consequences for the activities of microorganisms. Although both D/RW and F/TW events cause respiration pulses from soil to the atmosphere, it remains unknown whether the underlying microbial control is similar. Recent work has revealed that soil microbial responses to D/RW vary between two extremes: (Type 1) a resilient response, with a fast recovery of growth rates associated with a brief respiration pulse, or (Type 2) a sensitive response, where growth rates recover only after a lag period of no apparent growth associated with a prolonged respiration pulse. However, it remains unknown if these different microbial perturbation responses also occur after F/TW. Here, we directly compared microbial growth, respiration, and carbon-use efficiency (CUE) in response to D/RW and F/TW events. To do this, we selected two forest soils characterized by either sensitive or resilient responses to D/RW. We could confirm that D/RW induced either sensitive or resilient bacterial growth and respiration responses, but also that these distinct responses were found after F/TW. Additionally, F/TW resulted in shorter lag periods before the increase of bacterial growth, smaller respiration pulses, and lower levels of cumulative respiration, bacterial growth and fungal growth after the perturbation than did D/RW. These findings are consistent with a F/TW event imposing a similar stress on soil microorganisms to a D/RW event, but with lower severity. However, there was no significant difference in the microbial CUE between D/RW and F/TW, indicating that microorganisms maintain the stability of their C allocation in response to both types of perturbation. Altogether, our findings suggest that microbial communities are exposed to similar environmental pressures during D/RW and F/TW, implying that strategies to cope with drought can also provide protection to winter frost, and vice versa

The effects of sediment depth and oxygen concentration on the use of organic matter: An experimental study using an infiltration sediment tank

Water flowing through hyporheic river sediments or artificial recharge facilities promotes the development of microbial communities with sediment depth. We performed an 83-day mesocosm infiltration experment, to study howmicrobial functions (e.g., extracellular enzyme activities and carbon substrate utilization) are affected by sediment depth (up to 50 cm) and different oxygen concentrations. Results indicated that surface sediment layers were mainly colonized bymicroorganisms capable of using awide range of substrates (although they preferred to degrade carbon polymeric compounds, as indicated by the higher ß-glucosidase activity). In contrast, at a depth of 50 cm, the microbial community became specialized in using fewer carbon substrates, showing decreased functional richness and diversity. At this depth, microorganisms picked nitrogenous compounds, including amino acids and carboxyl acids. After the 83-day experiment, the sediment at the bottomof the tank became anoxic, inhibiting phosphatase activity. Coexistence of aerobic and anaerobic communities, promoted by greater physicochemical heterogeneity, was also observed in deeper sediments. The presence of specific metabolic fingerprints under oxic and anoxic conditions indicated that the microbial community was adapted to use organic matter under different oxygen conditions. Overall the heterogeneity of oxygen concentrations with depth and in time would influence organic matter metabolism in the sediment tan

The effects of sediment depth and oxygen concentration on the use of organic matter: An experimental study using an infiltration sediment tank

Water flowing through hyporheic river sediments or artificial recharge facilities promotes the development of microbial communities with sediment depth. We performed an 83-day mesocosm infiltration experment, to study howmicrobial functions (e.g., extracellular enzyme activities and carbon substrate utilization) are affected by sediment depth (up to 50 cm) and different oxygen concentrations. Results indicated that surface sediment layers were mainly colonized bymicroorganisms capable of using awide range of substrates (although they preferred to degrade carbon polymeric compounds, as indicated by the higher ß-glucosidase activity). In contrast, at a depth of 50 cm, the microbial community became specialized in using fewer carbon substrates, showing decreased functional richness and diversity. At this depth, microorganisms picked nitrogenous compounds, including amino acids and carboxyl acids. After the 83-day experiment, the sediment at the bottomof the tank became anoxic, inhibiting phosphatase activity. Coexistence of aerobic and anaerobic communities, promoted by greater physicochemical heterogeneity, was also observed in deeper sediments. The presence of specific metabolic fingerprints under oxic and anoxic conditions indicated that the microbial community was adapted to use organic matter under different oxygen conditions. Overall the heterogeneity of oxygen concentrations with depth and in time would influence organic matter metabolism in the sediment tan