Introduction In dryland systems, biological soil crusts (biocrusts) can occupy large areas of plant interspaces, where they fix carbon following rain. Although distinct biocrust types contain different dominant photoautotrophs, few studies to date have documented carbon exchange over time from various biocrust types. This is especially true for gypsum soils. Our objective was to assess the carbon exchange of biocrust types established at the world’s largest gypsum dune field at White Sands National Park. Methods We sampled five different biocrust types from a sand sheet location in three different years and seasons (summer 2020, fall 2021, and winter 2022) for carbon exchange measurements in controlled lab conditions. Biocrusts were rehydrated to full saturation and light incubated for 30 min, 2, 6, 12, 24, and 36 h. Samples were then subject to a 12-point light regime with a LI-6400XT photosynthesis system to determine carbon exchange. Results Biocrust carbon exchange values differed by biocrust type, by incubation time since wetting, and by date of field sampling. Lichens and mosses had higher gross and net carbon fixation rates than dark and light cyanobacterial crusts. High respiration rates were found after 0.5 h and 2 h incubation times as communities recovered from desiccation, leveling off after 6 h incubation. Net carbon fixation of all types increased with longer incubation time, primarily as a result of decreasing respiration, which suggests rapid recovery of biocrust photosynthesis across types. However, net carbon fixation rates varied from year to year, likely as a product of time since the last rain event and environmental conditions preceding collection, with moss crusts being most sensitive to environmental stress at our study sites. Discussion Given the complexity of patterns discovered in our study, it is especially important to consider a multitude of factors when comparing biocrust carbon exchange rates across studies. Understanding the dynamics of biocrust carbon fixation in distinct crust types will enable greater precision of carbon cycling models and improved forecasting of impacts of global climate change on dryland carbon cycling and ecosystem functioning.
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Adaptation to Environmental Extremes Structures Functional Traits in Biological Soil Crust and Hypolithic Microbial Communities
ABSTRACT Biological soil crusts (biocrusts) are widespread in drylands and deserts. At the microhabitat scale, they also host hypolithic communities that live under semitranslucent stones. Both environmental niches experience exposure to extreme conditions such as high UV radiation, desiccation, temperature fluctuations, and resource limitation. However, hypolithic communities are somewhat protected from extremes relative to biocrust communities. Conditions are otherwise similar, so comparing them can answer outstanding questions regarding adaptations to environmental extremes. Using metagenomic sequencing, we assessed the functional potential of dryland soil communities and identified the functional underpinnings of ecological niche differentiation in biocrusts versus hypoliths. We also determined the effect of the anchoring photoautotroph (moss or cyanobacteria). Genes and pathways differing in abundance between biocrusts and hypoliths indicate that biocrust communities adapt to the higher levels of UV radiation, desiccation, and temperature extremes through an increased ability to repair damaged DNA, sense and respond to environmental stimuli, and interact with other community members and the environment. Intracellular competition appears to be crucial to both communities, with biocrust communities using the Type VI Secretion System (T6SS) and hypoliths favoring a diversity of antibiotics. The dominant primary producer had a reduced effect on community functional potential compared with niche, but an abundance of genes related to monosaccharide, amino acid, and osmoprotectant uptake in moss-dominated communities indicates reliance on resources provided to heterotrophs by mosses. Our findings indicate that functional traits in dryland communities are driven by adaptations to extremes and we identify strategies that likely enable survival in dryland ecosystems. IMPORTANCE Biocrusts serve as a keystone element of desert and dryland ecosystems, stabilizing soils, retaining moisture, and serving as a carbon and nitrogen source in oligotrophic environments. Biocrusts cover approximately 12% of the Earth’s terrestrial surface but are threatened by climate change and anthropogenic disturbance. Given their keystone role in ecosystem functioning, loss will have wide-spread consequences. Biocrust microbial constituents must withstand polyextreme environmental conditions including high UV exposure, desiccation, oligotrophic conditions, and temperature fluctuations over short time scales. By comparing biocrust communities with co-occurring hypolithic communities (which inhabit the ventral sides of semitranslucent stones and are buffered from environmental extremes), we identified traits that are likely key adaptations to extreme conditions. These include DNA damage repair, environmental sensing and response, and intracellular competition. Comparison of the two niches, which differ primarily in exposure levels to extreme conditions, makes this system ideal for understanding how functional traits are structured by the environment.
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- Award ID(s):
- 1638996
- NSF-PAR ID:
- 10380875
- Editor(s):
- Gilbert, Jack A.
- Date Published:
- Journal Name:
- mSystems
- Volume:
- 7
- Issue:
- 4
- ISSN:
- 2379-5077
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Understanding the importance of biotic interactions in driving the distribution and abundance of species is a central goal of plant ecology. Early vascular plants likely colonized land occupied by biocrusts — photoautotrophic, surface‐dwelling soil communities comprised of cyanobacteria, bryophytes, lichens and fungi — suggesting biotic interactions between biocrusts and plants have been at play for some 2,000 million years. Today, biocrusts coexist with plants in dryland ecosystems worldwide, and have been shown to both facilitate or inhibit plant species performance depending on ecological context. Yet, the factors that drive the direction and magnitude of these effects remain largely unknown.
We conducted a meta‐analysis of plant responses to biocrusts using a global dataset encompassing 1,004 studies from six continents.
Meta‐analysis revealed there is no simple positive or negative effect of biocrusts on plants. Rather, plant responses differ by biocrust composition and plant species traits and vary across plant ontogeny. Moss‐dominated biocrusts facilitated, while lichen‐dominated biocrusts inhibited overall plant performance. Plant responses also varied among plant functional groups: C4grasses received greater benefits from biocrusts compared to C3grasses, and plants without N‐fixing symbionts responded more positively to biocrusts than plants with N‐fixing symbionts. Biocrusts decreased germination but facilitated growth of non‐native plant species.
Synthesis . Results suggest that interspecific variation in plant responses to biocrusts, contingent on biocrust type, plant traits, and ontogeny can have strong impacts on plant species performance. These findings have important implications for understanding biocrust contributions to plant productivity and community assembly processes in ecosystems worldwide. -
Stams, Alfons J. (Ed.)ABSTRACT Biological soil crusts (biocrusts) are communities of microbes that inhabit the surface of arid soils and provide essential services to dryland ecosystems. While resistant to extreme environmental conditions, biocrusts are susceptible to anthropogenic disturbances that can deprive ecosystems of these valuable services for decades. Until recently, culture-based efforts to produce inoculum for cyanobacterial biocrust restoration in the southwestern United States focused on producing and inoculating the most abundant primary producers and biocrust pioneers, Microcoleus vaginatus and members of the family Coleofasciculaceae (also called Microcoleus steenstrupii complex). The discovery that a unique microbial community characterized by diazotrophs, known as the cyanosphere, is intimately associated with M. vaginatus suggests a symbiotic division of labor in which nutrients are traded between phototrophs and heterotrophs. To probe the potential use of such cyanosphere members in the restoration of biocrusts, we performed coinoculations of soil substrates with cyanosphere constituents. This resulted in cyanobacterial growth that was more rapid than that seen for inoculations with the cyanobacterium alone. Additionally, we found that the mere addition of beneficial heterotrophs enhanced the formation of a cohesive biocrust without the need for additional phototrophic biomass within native soils that contain trace amounts of biocrust cyanobacteria. Our findings support the hitherto-unknown role of beneficial heterotrophic bacteria in the establishment and growth of biocrusts and allow us to make recommendations concerning biocrust restoration efforts based on the presence of remnant biocrust communities in disturbed areas. Future biocrust restoration efforts should consider cyanobacteria and their beneficial heterotrophic community as inoculants. IMPORTANCE The advancement of biocrust restoration methods for cyanobacterial biocrusts has been largely achieved through trial and error. Successes and failures could not always be traced back to particular factors. The investigation and application of foundational microbial interactions existing within biocrust communities constitute a crucial step toward informed and repeatable biocrust restoration methods.more » « less
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Dietz, Karl-Josef (Ed.)Abstract Plants in dryland ecosystems experience extreme daily and seasonal fluctuations in light, temperature, and water availability. We used an in situ field experiment to uncover the effects of natural and reduced levels of ultraviolet radiation (UV) on maximum PSII quantum efficiency (Fv/Fm), relative abundance of photosynthetic pigments and antioxidants, and the transcriptome in the desiccation-tolerant desert moss Syntrichia caninervis. We tested the hypotheses that: (i) S. caninervis plants undergo sustained thermal quenching of light [non-photochemical quenching (NPQ)] while desiccated and after rehydration; (ii) a reduction of UV will result in improved recovery of Fv/Fm; but (iii) 1 year of UV removal will de-harden plants and increase vulnerability to UV damage, indicated by a reduction in Fv/Fm. All field-collected plants had extremely low Fv/Fm after initial rehydration but recovered over 8 d in lab-simulated winter conditions. UV-filtered plants had lower Fv/Fm during recovery, higher concentrations of photoprotective pigments and antioxidants such as zeaxanthin and tocopherols, and lower concentrations of neoxanthin and Chl b than plants exposed to near natural UV levels. Field-grown S. caninervis underwent sustained NPQ that took days to relax and for efficient photosynthesis to resume. Reduction of solar UV radiation adversely affected recovery of Fv/Fm following rehydration.more » « less
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Centaurea stoebe .We surveyed
Centaurea and biocrust cover and evaluated how interactions amongCentaurea , biocrusts and water pulses influenced plant biomass and soil nitrogen in a field experiment.Centaurea seedling and biocrust interactions were also compared in a greenhouse experiment to evaluate differences related to life stage.In field surveys,
Centaurea and biocrusts were positively associated. Across water pulse treatments, biocrust biomass decreased whenCentaurea was removed, indicating thatCentaurea facilitated biocrusts. Biocrusts did not affect adultCentaurea in the field, butCentaurea seedling biomass was greater when grown with biocrusts in the greenhouse. Water pulses did not affect plant biomass, but interactions betweenCentaurea and biocrusts corresponded with variation in the effect of water pulses on soil nitrogen which were not evident whenCentaurea or biocrusts were grown alone. Twenty‐four hours after large water pulses were added, soilwas nine times higher in plots where biocrusts and Centaurea co‐occurred compared with small water pulse plots. In these same plots, soiltended to be lower at the end of the experiment. These results highlight positive interactions between an invasive exotic forb and native moss biocrust. Water pulses influenced soil nitrogen availability when both plants co‐occurred, but did not affect plant biomass, suggesting that resource pulses and species interactions can interact to affect ecosystem processes.
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1128/msystems.01419-21
