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 m 2 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 cm 2 .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.
Biological soil crusts (biocrust) are microbial communities that develop at the soil surface of drylands and play an important role in erosion control and fertility. Soil surface disturbance from a broad range of natural and human processes (e.g. fire, livestock grazing, off-road traffic) cause significant losses in biocrust cover and associated ecosystems services. Hence, biocrust restoration is emerging as an important intervention strategy to rehabilitate degraded dryland soils. In a multistep process, we designed protocols for the establishment of "microbial nurseries" to produce photosynthetic cyanobacterial inoculum for biocrust seeding at scale. We first report on the strategy for isolation, directly from the target site, of a large culture collection of cyanobacteria that included multiple representatives of the five most common biocrust taxa. After genetic pedigreeing of these isolates, we could select those that best matched field populations genetically for scale-up cultivation. We then developed protocols for effective cyanobacterial biomass production to obtain sufficient inoculum. This was followed by conditioning treatments (hardening off) to preacclimate this inoculum to the stressful conditions expected in the field. Finally, we show that the inoculum obtained was fit to thrive in its original soil under natural outdoor conditions if sufficient water was available. We repeated this process successfully for four sites, two in the hot Chihuanuan desert and two in the cooler Great Basin Desert, and on two textural types of soils in each. The cyanobacterial biocrust nursery approach represents a versatile, viable, and safe tool for the rehabilitation of dryland soils.
Microcoleus vaginatus plays a prominent role as both primary producer and pioneer in biocrust communities from dryland soils. And yet, it cannot fix dinitrogen, essential in often nitrogen-limited drylands. But a diazotroph-rich “cyanosphere” has been described in M. vaginatus, hinting that there exists a C for N exchange between the photoautotroph and heterotrophic diazotrophs. We provide evidence for this by establishing such a symbiosis in culture and by showing that it is selective and dependent on nitrogen availability. In natural populations, provision of nitrogen resulted in loss of diazotrophs from the cyanosphere of M. vaginatus compared to controls, but provision of phosphorus did not. Co-culturing of pedigreed cyanosphere diazotroph isolates with axenic M. vaginatus resulted in copious growth in C and N-free medium, but co-culture with non-cyanosphere diazotrophs or other heterotrophs did not. Unexpectedly, bundle formation in M. vaginatus, diacritical to the genus but not seen in axenic culture, was restored in vitro by imposed nitrogen limitation or, even more strongly, by co-culture with diazotrophic partners, implicating this trait in the symbiosis. Our findings provide direct evidence for a symbiotic relationship between M. vaginatus and its cyanosphere and help explain how it can be a global pioneer in spite of its genetic shortcomings.
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.
Biological soil crusts are complex communities of organisms that develop on the top layer of dryland soils where they enhance important ecosystem services, including soil fertility and protection from erosion. Regrettably, a range of human activities such as cattle grazing, off‐road driving, hiking, and global warming result in significant deterioration of biocrust cover and their associated services. This scenario has prompted efforts to develop effective biocrust restoration strategies, which often involve the production of biocrust inoculum, both in greenhouse and in laboratory settings. Sometimes this inoculum is preconditioned in a process of “hardening” at considerable expense and effort in order to improve its fitness under harsh field conditions. But the positive effects of such hardening procedures have yet to be rigorously demonstrated. Here, we compared the growth performance of 20 cultured strains of biocrust cyanobacteria in outdoor tests on native soils as a function of preconditioning regimes consisting of increasingly high exposure to solar radiation, temperature and illumination daily variability, and recurrent wet‐dry cycles. Preconditioning improved performance in 13 out of 20 strains, particularly among pioneer crust‐forming Microcoleus spp. (eight out of eight). Improvements were variable among heterocystous strains (three out of four Scytonema spp., two out of four Tolypothrix spp., and none out of four Nostoc spp.). Based on these results, we recommend the inclusion of preconditioning treatments to increase inoculum survival rate and speed of cyanobacterial biocrust recovery in restoration of dryland soils.
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