Climate change and physical disturbance manipulations result in distinct biological soil crust communities.
ABSTRACT: Biological soil crusts (biocrusts) colonize plant interspaces in many drylands and are critical to soil nutrient cycling. Multiple climate change and land use factors have been shown to detrimentally impact biocrusts on a macroscopic (i.e., visual) scale. However, the impact of these perturbations on the bacterial components of the biocrusts remains poorly understood. We employed multiple long-term field experiments to assess the impacts of chronic physical (foot trampling) and climatic changes (2°C soil warming, altered summer precipitation [wetting], and combined warming and wetting) on biocrust bacterial biomass, composition, and metabolic profile. The biocrust bacterial communities adopted distinct states based on the mechanism of disturbance. Chronic trampling decreased biomass and caused small community compositional changes. Soil warming had little effect on biocrust biomass or composition, while wetting resulted in an increase in the cyanobacterial biomass and altered bacterial composition. Warming combined with wetting dramatically altered bacterial composition and decreased Cyanobacteria abundance. Shotgun metagenomic sequencing identified four functional gene categories that differed in relative abundance among the manipulations, suggesting that climate and land use changes affected soil bacterial functional potential. This study illustrates that different types of biocrust disturbance damage biocrusts in macroscopically similar ways, but they differentially impact the resident soil bacterial communities, and the communities' functional profiles can differ depending on the disturbance type. Therefore, the nature of the perturbation and the microbial response are important considerations for management and restoration of drylands.
Project description:Biological soil crusts (biocrusts) are microbial communities that are a feature of arid surface soils worldwide. In drylands where precipitation is pulsed and ephemeral, the ability of biocrust microbiota to rapidly initiate metabolic activity is critical to their survival. Community gene expression was compared after a short duration (1 h) wetting pulse in both intact and soils disturbed by chronic foot trampling. Across the metatranscriptomes the majority of transcripts were cyanobacterial in origin, suggesting that cyanobacteria accounted for the bulk of the transcriptionally active cells. Chronic trampling substantially altered the functional profile of the metatranscriptomes, specifically resulting in a significant decrease in transcripts for nitrogen fixation. Soil depth (biocrust and below crust) was a relatively small factor in differentiating the metatranscriptomes, suggesting that the metabolically active bacteria were similar between shallow soil horizons. The dry samples were consistently enriched for hydrogenase genes, indicating that molecular hydrogen may serve as an energy source for the desiccated soil communities. The water pulse was associated with a restructuring of the metatranscriptome, particularly for the biocrusts. Biocrusts increased transcripts for photosynthesis and carbon fixation, suggesting a rapid resuscitation upon wetting. In contrast, the trampled surface soils showed a much smaller response to wetting, indicating that trampling altered the metabolic response of the community. Finally, several biogeochemical cycling genes in carbon and nitrogen cycling were assessed for their change in abundance due to wetting in the biocrusts. Different transcripts encoding the same gene product did not show a consensus response, with some more abundant in dry or wet biocrusts, highlighting the challenges in relating transcript abundance to biogeochemical cycling rates. These observations demonstrate that metatranscriptome sequencing was able to distinguish alterations in the function of arid soil microbial communities at two varying temporal scales, a long-term ecosystems disturbance through foot trampling, and a short term wetting pulse. Thus, community metatranscriptomes have the potential to inform studies on the response and resilience of biocrusts to various environmental perturbations.
Project description:Soil surface communities dominated by mosses, lichens and cyanobacteria (biocrusts) are common between vegetation patches in drylands worldwide, and are known to affect soil wetting and drying after rainfall events. While ongoing climate change is already warming and changing rainfall patterns of drylands in many regions, little is known on how these changes may affect the hydrological behaviour of biocrust-covered soils. We used eight years of continuous soil moisture and rainfall data from a climate change experiment in central Spain to explore how biocrusts modify soil water gains and losses after rainfall events under simulated changes in temperature (2.5°C warming) and rainfall (33% reduction). Both rainfall amount and biocrust cover increased soil water gains after rainfall events, whereas experimental warming, rainfall intensity and initial soil moisture decreased them. Initial moisture, maximum temperature and biocrust cover, by means of enhancing potential evapotranspiration or by soil darkening, increased the drying rates and enhanced the exponential behaviour of the drying events. Meanwhile, warming reduced their exponential behaviour. The effects of climate change treatments on soil water gains and losses changed through time, with important differences between the first two years of the experiment and five years after its setup. These effects were mainly driven by the important reductions in biocrust cover and diversity observed under warming. Our results highlight the importance of long-term studies to understand soil moisture responses to ongoing climate change in drylands.
Project description:Soil surface communities composed of cyanobacteria, algae, mosses, liverworts, fungi, bacteria and lichens (biocrusts) largely affect soil respiration in dryland ecosystems. Climate change is expected to have large effects on biocrusts and associated ecosystem processes. However, few studies so far have experimentally assessed how expected changes in temperature and rainfall will affect soil respiration in biocrust-dominated ecosystems. We evaluated the impacts of biocrust development, increased air temperature and decreased precipitation on soil respiration dynamics during dry (2009) and wet (2010) years, and investigated the relative importance of soil temperature and moisture as environmental drivers of soil respiration, in a semiarid grassland from central Spain. Soil respiration rates were significantly lower in the dry than during the wet year, regardless of biocrust cover. Warming increased soil respiration rates, but this response was only significant in biocrust-dominated areas (> 50% biocrust cover). Warming also increased the temperature sensitivity (Q10 values) of soil respiration in biocrust-dominated areas, particularly during the wet year. The combination of warming and rainfall exclusion had similar effects in low biocrust cover areas. Our results highlight the importance of biocrusts as a modulator of soil respiration responses to both warming and rainfall exclusion, and indicate that they must be explicitly considered when evaluating soil respiration responses to climate change in drylands.
Project description:Soil communities dominated by lichens and mosses (biocrusts) play key roles in maintaining ecosystem structure and functioning in drylands worldwide. However, few studies have explicitly evaluated how climate change-induced impacts on biocrusts affect associated soil microbial communities. We report results from a field experiment conducted in a semiarid Pinus halepensis plantation, where we setup an experiment with two factors: cover of biocrusts (low [<15%] versus high [>50%]), and warming (control versus a ?2°C temperature increase). Warming reduced the richness and cover (?45%) of high biocrust cover areas 53 months after the onset of the experiment. This treatment did not change the ratios between the major microbial groups, as measured by phospholipid fatty acid analysis. Warming increased the physiological stress of the Gram negative bacterial community, as indicated by the cy17:0/16:1?7 ratio. This response was modulated by the initial biocrust cover, as the increase in this ratio with warming was higher in areas with low cover. Our findings suggest that biocrusts can slow down the negative effects of warming on the physiological status of the Gram negative bacterial community. However, as warming will likely reduce the cover and diversity of biocrusts, these positive effects will be reduced under climate change.
Project description:Dryland ecosystems account for ca. 27% of global soil organic carbon (C) reserves, yet it is largely unknown how climate change will impact C cycling and storage in these areas. In drylands, soil C concentrates at the surface, making it particularly sensitive to the activity of organisms inhabiting the soil uppermost levels, such as communities dominated by lichens, mosses, bacteria and fungi (biocrusts). We conducted a full factorial warming and rainfall exclusion experiment at two semiarid sites in Spain to show how an average increase of air temperature of 2-3 °C promoted a drastic reduction in biocrust cover (ca. 44% in 4 years). Warming significantly increased soil CO2 efflux, and reduced soil net CO2 uptake, in biocrust-dominated microsites. Losses of biocrust cover with warming through time were paralleled by increases in recalcitrant C sources, such as aromatic compounds, and in the abundance of fungi relative to bacteria. The dramatic reduction in biocrust cover with warming will lessen the capacity of drylands to sequester atmospheric CO2 . This decrease may act synergistically with other warming-induced effects, such as the increase in soil CO2 efflux and the changes in microbial communities to alter C cycling in drylands, and to reduce soil C stocks in the mid to long term.
Project description:The impact of 10 years of annual foot trampling on soil biocrusts was examined in replicated field experiments at three cold desert sites of the Colorado Plateau, USA. Trampling detrimentally impacted lichens and mosses, and the keystone cyanobacterium, Microcoleus vaginatus, resulting in increased soil erosion and reduced C and N concentrations in surface soils. Trampled biocrusts contained approximately half as much extractable DNA and 20-52% less chlorophyll a when compared with intact biocrusts at each site. Two of the three sites also showed a decline in scytonemin-containing, diazotrophic cyanobacteria in trampled biocrusts. 16S rRNA gene sequence and terminal restriction fragment length polymorphism (T-RFLP) analyses of soil bacteria from untrampled and trampled biocrusts demonstrated a reduced proportion (23-65% reduction) of M. vaginatus and other Cyanobacteria in trampled plots. In parallel, other soil bacterial species that are natural residents of biocrusts, specifically members of the Actinobacteria, Chloroflexi and Bacteroidetes, became more readily detected in trampled than in untrampled biocrusts. Replicate 16S rRNA T-RFLP profiles from trampled biocrusts at all three sites contained significantly more fragments (n = 17) than those of untrampled biocrusts (n≤6) and exhibited much higher variability among field replicates, indicating transition to an unstable disturbed state. Despite the dramatic negative impacts of trampling on biocrust physical structure and composition, M. vaginatus could still be detected in surface soils after 10 years of annual trampling, suggesting the potential for biocrust re-formation over time. Physical damage of biocrusts, in concert with changing temperature and precipitation patterns, has potential to alter performance of dryland ecosystems for decades.
Project description:Biocrusts cover ~30% of global drylands with a prominent role in the biogeochemical cycles. Theoretically, biocrusts, vascular plants, and bare soil can represent multiple stable states in drylands. However, no empirical evidence for the existence of a biocrust stable state has been reported. Here, using a global drylands dataset, we found that biocrusts form an alternative stable state (biocrust cover, ~80%; vascular cover, ?10%) besides bare soil (both biocrust and vascular cover, ?10%) and vascular plants (vascular cover, >50%; biocrust cover, ~5%). The pattern of multiple stable states associated with biocrusts differs from the classic fold bifurcation, and values of the aridity index in the range of 0 to 0.6 define a bistable region where multiple stable states coexist. This study empirically demonstrates the existence and thresholds of multiple stable states associated with biocrusts along climatic gradients and thus may greatly contribute to conservation and restoration of global drylands.
Project description:Biological soil crusts (biocrusts) are topsoil communities formed by cyanobacteria or other microbial primary producers and are typical of arid and semiarid environments. Biocrusts promote a range of ecosystem services, such as erosion resistance and soil fertility, but their degradation by often anthropogenic disturbance brings about the loss of these services. This has prompted interest in developing restoration techniques. One approach is to source biocrust remnants from the area of interest for scale-up cultivation in a microbial "nursery" that produces large quantities of high-quality inoculum for field deployment. However, growth dynamics and the ability to reuse the produced inoculum for continued production have not been assessed. To optimize production, we followed nursery growth dynamics of biocrusts from cold (Great Basin) and hot (Chihuahuan) deserts. Peak phototrophic biomass was attained between 3 and 7?weeks in cold desert biocrusts and at 12?weeks in those from hot deserts. We also reused the resultant biocrust inoculum to seed successive incubations, tracking both phototroph biomass and cyanobacterial community structure using 16S rRNA gene amplicon sequencing. Hot desert biocrusts showed little to no viability upon reinoculation, while cold desert biocrusts continued to grow, but at the expense of progressive shifts in species composition. This leads us to discourage the reuse of nursery-grown inoculum. Surprisingly, growth was highly variable among replicates, and overall yields were low, a fact that we attribute to the demonstrable presence of virulent and stochastically distributed but hitherto unknown cyanobacterial pathogens. We provide recommendations to avoid pathogen incidence in the process.IMPORTANCE Biocrust communities provide important ecosystem services for arid land soils, such as soil surface stabilization promoting erosion resistance and contributing to overall soil fertility. Anthropogenic degradation to biocrust communities (through livestock grazing, agriculture, urban sprawl, and trampling) is common and significant, resulting in a loss of those ecosystem services. Losses impact both the health of the native ecosystem and the public health of local populations due to enhanced dust emissions. Because of this, approaches for biocrust restoration are being developed worldwide. Here, we present optimization of a nursery-based approach to scaling up the production of biocrust inoculum for field restoration with respect to temporal dynamics and reuse of biological materials. Unexpectedly, we also report on complex population dynamics, significant spatial variability, and lower than expected yields that we ascribe to the demonstrable presence of cyanobacterial pathogens, the spread of which may be enhanced by some of the nursery production standard practices.
Project description:Biological soil crusts (biocrusts) account for a substantial portion of primary production in dryland ecosystems. They successionally mature to deliver a suite of ecosystem services, such as carbon sequestration, water retention and nutrient cycling, and climate regulation. Biocrust assemblages are extremely well adapted to survive desiccation and to rapidly take advantage of the periodic precipitation events typical of arid ecosystems. Here we focus on the wetting response of incipient cyanobacterial crusts as they mature from "light" to "dark." We sampled a cyanobacterial biocrust chronosequence before (dry) and temporally following a controlled wetting event and used high-throughput 16S rRNA and rRNA gene sequencing to monitor the dynamics of microbial response. Overall, shorter-term changes in phylogenetic beta diversity attributable to periodic wetting were as large as those attributable to biocrust successional stage. Notably, more mature crusts showed significantly higher resistance to precipitation disturbance. A large bloom of a few taxa within the Firmicutes, primarily in the order Bacillales, emerged 18 h after wetting, while filamentous crust-forming cyanobacteria showed variable responses to wet-up across the successional gradient, with populations collapsing in less-developed light crusts but increasing in later-successional-stage dark crusts. Overall, the consistent Bacillales bloom accompanied by the variable collapse of pioneer cyanobacteria of the Oscillatoriales order across the successional gradient suggests that the strong response of few organisms to a hydration pulse with the mortality of the autotroph might have important implications for carbon (C) balance in semiarid ecosystems.IMPORTANCE Desert biological soil crusts are terrestrial topsoil microbial communities common to arid regions that comprise 40% of Earth's terrestrial surface. They successionally develop over years to decades to deliver a suite of ecosystem services of local and global significance. Ecosystem succession toward maturity has been associated with both resistance and resilience to disturbance. Recent work has shown that the impacts of both climate change and physical disturbance on biocrusts increase the potential for successional resetting. A larger proportion of biocrusts are expected to be at an early developmental stage, hence increasing susceptibility to changes in precipitation frequencies. Therefore, it is essential to characterize how biocrusts respond to wetting across early developmental stages. In this study, we document the wetting response of microbial communities from a biocrust chronosequence. Overall, our results suggest that the cumulative effects of altered precipitation frequencies on the stability of biocrusts will depend on biocrust maturity.
Project description:Biological soil crusts (biocrusts) are slow-growing, phototroph-based microbial assemblages that develop on the topsoils of drylands. Biocrusts help maintain soil fertility and reduce erosion. Because their loss through human activities has negative ecological and environmental health consequences, biocrust restoration is of interest. Active soil inoculation with biocrust microorganisms can be an important tool in this endeavor. We present a culture-independent, two-step process to grow multispecies biocrusts in open greenhouse nursery facilities, based on the inoculation of local soils with local biocrust remnants and incubation under seminatural conditions that maintain the essence of the habitat but lessen its harshness. In each of four U.S. Southwest sites, we tested and deployed combinations of factors that maximized growth (gauged as chlorophyll a content) while minimizing microbial community shifts (assessed by 16S rRNA sequencing and bioinformatics), particularly for crust-forming cyanobacteria. Generally, doubling the frequency of natural wetting events, a 60% reduction in sunlight, and inoculation by slurry were optimal. Nutrient addition effects were site specific. In 4 months, our approach yielded crusts of high inoculum quality reared on local soil exposed to locally matched climates, acclimated to desiccation, and containing communities minimally shifted in composition from local ones. Our inoculum contained abundant crust-forming cyanobacteria and no significant numbers of allochthonous phototrophs, and it was sufficient to treat ca. 6,000 m2 of degraded dryland soils at 1 to 5% of the typical crust biomass concentration, having started from a natural crust remnant as small as 6 to 30 cm2 IMPORTANCE: Soil surface crusts can protect dryland soils from erosion, but they are often negatively impacted by human activities. Their degradation causes a loss of fertility, increased production of fugitive dust and intensity of dust storms with associated traffic problems, and provokes general public health hazards. Our results constitute an advance in the quest to actively restore biological soil covers by providing a means to obtain high-quality inoculum within a reasonable time (a few months), thereby allowing land managers to recover essential, but damaged, ecosystem services in a sustainable, self-perpetuating way as provided by biocrust communities.