Dataset Information

Distribution of Mixotrophy and Desiccation Survival Mechanisms across Microbial Genomes in an Arid Biological Soil Crust Community.

ABSTRACT: Desert surface soils devoid of plant cover are populated by a variety of microorganisms, many with yet unresolved physiologies and lifestyles. Nevertheless, a common feature vital for these microorganisms inhabiting arid soils is their ability to survive long drought periods and reactivate rapidly in rare incidents of rain. Chemolithotrophic processes such as oxidation of atmospheric hydrogen and carbon monoxide are suggested to be a widespread energy source to support dormancy and resuscitation in desert soil microorganisms. Here, we assessed the distribution of chemolithotrophic, phototrophic, and desiccation-related metabolic potential among microbial populations in arid biological soil crusts (BSCs) from the Negev Desert, Israel, via population-resolved metagenomic analysis. While the potential to utilize light and atmospheric hydrogen as additional energy sources was widespread, carbon monoxide oxidation was less common than expected. The ability to utilize continuously available energy sources might decrease the dependency of mixotrophic populations on organic storage compounds and carbon provided by the BSC-founding cyanobacteria. Several populations from five different phyla besides the cyanobacteria encoded CO₂ fixation potential, indicating further potential independence from photoautotrophs. However, we also found population genomes with a strictly heterotrophic genetic repertoire. The highly abundant Rubrobacteraceae (Actinobacteriota) genomes showed particular specialization for this extreme habitat, different from their closest cultured relatives. Besides the ability to use light and hydrogen as energy sources, they encoded extensive O₂ stress protection and unique DNA repair potential. The uncovered differences in metabolic potential between individual, co-occurring microbial populations enable predictions of their ecological niches and generation of hypotheses on the dynamics and interactions among them.IMPORTANCE This study represents a comprehensive community-wide genome-centered metagenome analysis of biological soil crust (BSC) communities in arid environments, providing insights into the distribution of genes encoding different energy generation mechanisms, as well as survival strategies, among populations in an arid soil ecosystem. It reveals the metabolic potential of several uncultured and previously unsequenced microbial genera, families, and orders, as well as differences in the metabolic potential between the most abundant BSC populations and their cultured relatives, highlighting once more the danger of inferring function on the basis of taxonomy. Assigning functional potential to individual populations allows for the generation of hypotheses on trophic interactions and activity patterns in arid soil microbial communities and represents the basis for future resuscitation and activity studies of the system, e.g., involving metatranscriptomics.

SUBMITTER: Meier DV

PROVIDER: S-EPMC7901476 | biostudies-literature |

REPOSITORIES: biostudies-literature

ACCESS DATA

Similar Datasets

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.

Project description:Biological soil crusts (biocrusts) are photosynthetic "hot spots" in deserts and cover ∼12% of the Earth's terrestrial surface, and yet they face an uncertain future given expected shifts in rainfall events. Laboratory wetting of biocrust communities is known to cause a bloom of Firmicutes which rapidly become dominant community members within 2 days after emerging from a sporulated state. We hypothesized that their bacteriophages (phages) would respond to such a dramatic increase in their host's abundance. In our experiment, wetting caused Firmicutes to bloom and triggered a significant depletion of cyanobacterial diversity. We used genome-resolved metagenomics to link phage to their hosts and found that the bloom of the genus Bacillus correlated with a dramatic increase in the number of Caudovirales phages targeting these diverse spore-formers (r = 0.762). After 2 days, we observed dramatic reductions in the relative abundances of Bacillus, while the number of Bacillus phages continued to increase, suggestive of a predator-prey relationship. We found predicted auxiliary metabolic genes (AMGs) associated with sporulation in several Caudovirales genomes, suggesting that phages may influence and even benefit from sporulation dynamics in biocrusts. Prophage elements and CRISPR-Cas repeats in Firmicutes metagenome-assembled genomes (MAGs) provide evidence of recent infection events by phages, which were corroborated by mapping viral contigs to their host MAGs. Combined, these findings suggest that the blooming Firmicutes become primary targets for biocrust Caudovirales phages, consistent with the classical "kill-the-winner" hypothesis.IMPORTANCE This work forms part of an overarching research theme studying the effects of a changing climate on biological soil crust (biocrust) in the Southwestern United States. To our knowledge, this study was the first to characterize bacteriophages in biocrust and offers a view into the ecology of phages in response to a laboratory wetting experiment. The phages identified here represent lineages of Caudovirales, and we found that the dynamics of their interactions with their Firmicutes hosts explain the collapse of a bacterial bloom that was induced by wetting. Moreover, we show that phages carried host-altering metabolic genes and found evidence of proviral infection and CRISPR-Cas repeats within host genomes. Our results suggest that phages exert controls on population density by lysing dominant bacterial hosts and that they further impact biocrust by acquiring host genes for sporulation. Future research should explore how dominant these phages are in other biocrust communities and quantify how much the control and lysis of blooming populations contributes to nutrient cycling in biocrusts.

Project description:Exploring the structural characteristics of arid soil microbial communities and their assembly mechanisms is important for understanding the ecological characteristics of arid zone soils and promoting ecological restoration. In this study, we used Illumina high-throughput sequencing technology to study soils in the arid zone of the Lake Ebinur basin, determined the differences among soil microbial community structures in the study area under different water-salt gradients, and investigated the effects of environmental factors on microbial community structure and assembly mechanisms. The results show the following: the microbial community alpha diversity exhibited a significantly higher low water-salt gradient (L) than high water-salt gradient (H) and medium water-salt gradient (M). The pH was most strongly correlated with soil microbial community structure, where the alpha diversity indices of the bacterial community and fungal community were significantly negatively correlated with pH, and the Bray-Curtis distance of bacterial community was significantly positively correlated with pH (p < 0.05). The complexity of bacterial community co-occurrence networks showed a significantly higher L than H and M, and the complexity of fungal community co-occurrence network showed a significantly lower L than H and M. The cooperative relationship of H and M in the co-occurrence networks was stronger than that of the L, and the key species of the microbial co-occurrence network were different under different water-salt gradients. Stochastic processes dominated the assembly mechanism of the microbial community structure of soil, and the explanation rates of deterministic and stochastic processes were different under different water-salt gradients, with the highest explanation rate of stochastic processes on the L accounting for more than 90%. In summary, the soil microbial community structure and assembly mechanisms significantly differed across water-salt gradients, and these findings can help provide a reference for further research on soil microbiology in arid zones.

Project description:The N cycle of arid ecosystems is influenced by low soil organic matter, high soil pH, and extremes in water potential and temperature that lead to open canopies and development of biological soil crusts (biocrusts). We investigated the effects of N amendment on soil microbial dynamics in a Larrea tridentata-Ambrosia dumosa shrubland site in southern Nevada USA. Sites were fertilized with a NO3-NH4 mix at 0, 7, and 15 kg N ha(-1) y(-1) from March 2012 to March 2013. In March 2013, biocrust (0-0.5 cm) and bulk soils (0-10 cm) were collected beneath Ambrosia canopies and in the interspaces between plants. Biomass responses were assessed as bacterial and fungal SSU rRNA gene copy number and chlorophyll a concentration. Metabolic responses were measured by five ecoenzyme activities and rates of N transformation. By most measures, nutrient availability, microbial biomass, and process rates were greater in soils beneath the shrub canopy compared to the interspace between plants, and greater in the surface biocrust horizon compared to the deeper 10 cm soil profile. Most measures responded positively to experimental N addition. Effect sizes were generally greater for bulk soil than biocrust. Results were incorporated into a meta-analysis of arid ecosystem responses to N amendment that included data from 14 other studies. Effect sizes were calculated for biomass and metabolic responses. Regressions of effect sizes, calculated for biomass, and metabolic responses, showed similar trends in relation to N application rate and N load (rate × duration). The critical points separating positive from negative treatment effects were 88 kg ha(-1) y(-1) and 159 kg ha(-1), respectively, for biomass, and 70 kg ha(-1) y(-1) and 114 kg ha(-1), respectively, for metabolism. These critical values are comparable to those for microbial biomass, decomposition rates and respiration reported in broader meta-analyses of N amendment effects in mesic ecosystems. However, large effect sizes at low N addition rates indicate that arid ecosystems are sensitive to modest increments in anthropogenic N deposition.

Dataset Information

Distribution of Mixotrophy and Desiccation Survival Mechanisms across Microbial Genomes in an Arid Biological Soil Crust Community.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets