Dataset Information

Biological soil crusts on agricultural soils of mesic regions promote microbial cross-kingdom co-occurrences and nutrient retention.

ABSTRACT:

Introduction

Biological soil crusts (biocrusts) are known as biological hotspots on undisturbed, nutrient-poor bare soil surfaces and until now, are mostly observed in (semi-) arid regions but are currently poorly understood in agricultural systems. This is a crucial knowledge gap because managed sites of mesic regions can quickly cover large areas. Thus, we addressed the questions (i) if biocrusts from agricultural sites of mesic regions also increase nutrients and microbial biomass as their (semi-) arid counterparts, and (ii) how microbial community assemblage in those biocrusts is influenced by disturbances like different fertilization and tillage regimes.

Methods

We compared phototrophic biomass, nutrient concentrations as well as the abundance, diversity and co-occurrence of Archaea, Bacteria, and Fungi in biocrusts and bare soils at a site with low agricultural soil quality.

Results and discussion

Biocrusts built up significant quantities of phototrophic and microbial biomass and stored more nutrients compared to bare soils independent of the fertilizer applied and the tillage management. Surprisingly, particularly low abundant Actinobacteria were highly connected in the networks of biocrusts. In contrast, Cyanobacteria were rarely connected, which indicates reduced importance within the microbial community of the biocrusts. However, in bare soil networks, Cyanobacteria were the most connected bacterial group and, hence, might play a role in early biocrust formation due to their ability to, e.g., fix nitrogen and thus induce hotspot-like properties. The microbial community composition differed and network complexity was reduced by conventional tillage. Mineral and organic fertilizers led to networks that are more complex with a higher percentage of positive correlations favoring microbe-microbe interactions. Our study demonstrates that biocrusts represent a microbial hotspot on soil surfaces under agricultural use, which may have important implications for sustainable management of such soils in the future.

SUBMITTER: Kurth JK

PROVIDER: S-EPMC10382179 | biostudies-literature | 2023

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Biological soil crusts on agricultural soils of mesic regions promote microbial cross-kingdom co-occurrences and nutrient retention.

Kurth Julia Katharina JK Albrecht Martin M Glaser Karin K Karsten Ulf U Vestergaard Gisle G Armbruster Martin M Kublik Susanne S Schmid Christoph A O CAO Schloter Michael M Schulz Stefanie S

Frontiers in microbiology 20230714

<h4>Introduction</h4>Biological soil crusts (biocrusts) are known as biological hotspots on undisturbed, nutrient-poor bare soil surfaces and until now, are mostly observed in (semi-) arid regions but are currently poorly understood in agricultural systems. This is a crucial knowledge gap because managed sites of mesic regions can quickly cover large areas. Thus, we addressed the questions (i) if biocrusts from agricultural sites of mesic regions also increase nutrients and microbial biomass as ...[more]

PMID: 37520365

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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:BackgroundCover cropping is an agricultural practice that uses secondary crops to support the growth of primary crops through various mechanisms including erosion control, weed suppression, nutrient management, and enhanced biodiversity. Cover crops may elicit some of these ecosystem services through chemical interactions with the soil microbiome via root exudation, or the release of plant metabolites from roots. Phytohormones are one metabolite type exuded by plants that activate the rhizosphere microbiome, yet managing this chemical interaction remains an untapped mechanism for optimizing plant-soil-microbiome interactions. Currently, there is limited understanding on the diversity of cover crop phytohormone root exudation patterns and our aim was to understand how phytochemical signals selectively enrich specific microbial taxa and functionalities in agricultural soils.ResultsHere, we link variability in cover crop root exudate composition to changes in soil microbiome functionality. Exudate chemical profiles from 4 cover crop species (Sorghum bicolor, Vicia villosa, Brassica napus, and Secale cereal) were used as the chemical inputs to decipher microbial responses. These distinct exudate profiles, along with a no exudate control, were amended to agricultural soil microcosms with microbial responses tracked over time using metabolomes and genome-resolved metatranscriptomes. Our findings illustrated microbial metabolic patterns were unique in response to cover crop exudate inputs over time, particularly by sorghum and cereal rye amended microcosms. In these microcosms, we identify novel microbial members (at the genera and family level) who produced IAA and GA4 over time. Additionally, we identified cover crop exudates exclusively enriched for bacterial nitrite oxidizers, while control microcosms were discriminated for nitrogen transport, mineralization, and assimilation, highlighting distinct changes in microbial nitrogen cycling in response to chemical inputs.ConclusionsWe highlight that root exudate amendments alter microbial community function (i.e., N cycling) and microbial phytohormone metabolisms, particularly in response to root exudates isolated from cereal rye and sorghum plants. Additionally, we constructed a soil microbial genomic catalog of microorganisms responding to commonly used cover crops, a public resource for agriculturally relevant microbes. Many of our exudate-stimulated microorganisms are representatives from poorly characterized or novel taxa, revealing the yet to be discovered metabolic reservoir harbored in agricultural soils. Our findings emphasize the tractability of high-resolution multi-omics approaches to investigate processes relevant for agricultural soils, opening the possibility of targeting specific soil biogeochemical outcomes through biological precision agricultural practices that use cover crops and the microbiome as levers for enhanced crop production. Video Abstract.

Project description:BackgroundCover cropping is an agricultural practice that uses secondary crops to support the growth of primary crops through various mechanisms including erosion control, weed suppression, nutrient management, and enhanced biodiversity. Cover crops may elicit some of these ecosystem services through chemical interactions with the soil microbiome via root exudation, or the release of plant metabolites from roots. Phytohormones are one metabolite type exuded by plants that activate the rhizosphere microbiome, yet managing this chemical interaction remains an untapped mechanism for optimizing plant-soil microbiome interactions. Currently, there is limited understanding on the diversity of cover crop phytohormone root exudation patterns and how these chemical messages selectively enrich specific microbial taxa and functionalities in agricultural soils.ResultsHere, we link variability in cover crop root exudate composition to changes in soil microbiome functionality. Exudate chemical profiles from 4 cover crop species (Sorghum bicolor, Vicia villosa, Brassica napus, and Secale cereal) were used as the chemical inputs to decipher microbial responses. These distinct exudate profiles, along with a no exudate control, were amended to agricultural soil microcosms with microbial responses tracked over time using metabolomes and genome-resolved metatranscriptomes. Our findings illustrated microbial metabolic patterns were unique in response to cover crop exudate inputs over time, particularly by sorghum and cereal rye amended microcosms where we identify novel microbial members (at the genera and family level) who produced IAA and GA4 over time. We also identify broad changes in microbial nitrogen cycling in response chemical inputs.ConclusionsWe highlight that root exudate amendments alter microbial community function and phytohormone metabolisms, particularly in response to root exudates isolated from cereal rye and sorghum plants. Additionally, we constructed a soil microbial genomic catalog of microorganisms responding to commonly used cover crops, a public resource for agriculturally-relevant microbes. Many of our exudate-stimulated microorganisms are representatives from poorly characterized or novel taxa, highlighting the yet to be discovered metabolic reservoir harbored in agricultural soils. Our findings emphasize the tractability of high-resolution multiomics approaches to investigate processes relevant for agricultural soils, opening the possibility of targeting specific soil biogeochemical outcomes through biological precision agricultural practices that use cover crops and the microbiome as levers for enhanced crop production.

Dataset Information

Biological soil crusts on agricultural soils of mesic regions promote microbial cross-kingdom co-occurrences and nutrient retention.

Introduction

Methods

Results and discussion

Publications

Biological soil crusts on agricultural soils of mesic regions promote microbial cross-kingdom co-occurrences and nutrient retention.

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