Showing papers by "Janet K. Jansson published in 2022"

Trends in Microbial Community Composition and Function by Soil Depth

Abstract: Microbial communities play important roles in soil health, contributing to processes such as the turnover of organic matter and nutrient cycling. As soil edaphic properties such as chemical composition and physical structure change from surface layers to deeper ones, the soil microbiome similarly exhibits substantial variability with depth, with respect to both community composition and functional profiles. However, soil microbiome studies often neglect deeper soils, instead focusing on the top layer of soil. Here, we provide a synthesis on how the soil and its resident microbiome change with depth. We touch upon soil physicochemical properties, microbial diversity, composition, and functional profiles, with a special emphasis on carbon cycling. In doing so, we seek to highlight the importance of incorporating analyses of deeper soils in soil studies.

Standardized multi-omics of Earth’s microbiomes reveals microbial and metabolite diversity

Abstract: Despite advances in sequencing, lack of standardization makes comparisons across studies challenging and hampers insights into the structure and function of microbial communities across multiple habitats on a planetary scale. Here we present a multi-omics analysis of a diverse set of 880 microbial community samples collected for the Earth Microbiome Project. We include amplicon (16S, 18S, ITS) and shotgun metagenomic sequence data, and untargeted metabolomics data (liquid chromatography-tandem mass spectrometry and gas chromatography mass spectrometry). We used standardized protocols and analytical methods to characterize microbial communities, focusing on relationships and co-occurrences of microbially related metabolites and microbial taxa across environments, thus allowing us to explore diversity at extraordinary scale. In addition to a reference database for metagenomic and metabolomic data, we provide a framework for incorporating additional studies, enabling the expansion of existing knowledge in the form of an evolving community resource. We demonstrate the utility of this database by testing the hypothesis that every microbe and metabolite is everywhere but the environment selects. Our results show that metabolite diversity exhibits turnover and nestedness related to both microbial communities and the environment, whereas the relative abundances of microbially related metabolites vary and co-occur with specific microbial consortia in a habitat-specific manner. We additionally show the power of certain chemistry, in particular terpenoids, in distinguishing Earth's environments (for example, terrestrial plant surfaces and soils, freshwater and marine animal stool), as well as that of certain microbes including Conexibacter woesei (terrestrial soils), Haloquadratum walsbyi (marine deposits) and Pantoea dispersa (terrestrial plant detritus). This Resource provides insight into the taxa and metabolites within microbial communities from diverse habitats across Earth, informing both microbial and chemical ecology, and provides a foundation and methods for multi-omics microbiome studies of hosts and the environment.

Permafrost as a potential pathogen reservoir

Abstract:

Summary

The Arctic is currently warming at unprecedented rates because of global climate change, resulting in thawing of large tracts of permafrost soil. A great challenge is understanding the implications of permafrost thaw on human health and the environment. Permafrost is a reservoir of mostly uncharacterized microorganisms and viruses, many of which could be viable. Given our limited knowledge of permafrost-resident microbes, we also lack the basis to judge whether they pose risks to humans, animals, and plants. Here we delve into features of permafrost as a microbial habitat and discuss what is known about the potential for microbial pathogens to emerge in a warming climate as permafrost thaws. This review has broader implications for human health and ecosystem sustainability in the new Arctic environment that will emerge from a thawed permafrost landscape.

Structural characterization of a soil viral auxiliary metabolic gene product – a functional chitosanase

Abstract: Abstract Metagenomics is unearthing the previously hidden world of soil viruses. Many soil viral sequences in metagenomes contain putative auxiliary metabolic genes (AMGs) that are not associated with viral replication. Here, we establish that AMGs on soil viruses actually produce functional, active proteins. We focus on AMGs that potentially encode chitosanase enzymes that metabolize chitin – a common carbon polymer. We express and functionally screen several chitosanase genes identified from environmental metagenomes. One expressed protein showing endo-chitosanase activity (V-Csn) is crystalized and structurally characterized at ultra-high resolution, thus representing the structure of a soil viral AMG product. This structure provides details about the active site, and together with structure models determined using AlphaFold, facilitates understanding of substrate specificity and enzyme mechanism. Our findings support the hypothesis that soil viruses contribute auxiliary functions to their hosts.

Metadata harmonization–Standards are the key for a better usage of omics data for integrative microbiome analysis

Abstract: Tremendous amounts of data generated from microbiome research studies during the last decades require not only standards for sampling and preparation of omics data but also clear concepts of how the metadata is prepared to ensure re-use for integrative and interdisciplinary microbiome analysis.In this Commentary, we present our views on the key issues related to the current system for metadata submission in omics research, and propose the development of a global metadata system. Such a system should be easy to use, clearly structured in a hierarchical way, and should be compatible with all existing microbiome data repositories, following common standards for minimal required information and common ontology. Although minimum metadata requirements are essential for microbiome datasets, the immense technological progress requires a flexible system, which will have to be constantly improved and re-thought. While FAIR principles (Findable, Accessible, Interoperable, and Reusable) are already considered, international legal issues on genetic resource and sequence sharing provided by the Convention on Biological Diversity need more awareness and engagement of the scientific community.The suggested approach for metadata entries would strongly improve retrieving and re-using data as demonstrated in several representative use cases. These integrative analyses, in turn, would further advance the potential of microbiome research for novel scientific discoveries and the development of microbiome-derived products.

Interaction Networks Are Driven by Community-Responsive Phenotypes in a Chitin-Degrading Consortium of Soil Microbes

Abstract: The soil microbiome performs many functions that are key to ecology, agriculture, and nutrient cycling. However, because of the complexity of this ecosystem we do not know the molecular details of the interactions between microbial species that lead to these important functions. ABSTRACT Soil microorganisms provide key ecological functions that often rely on metabolic interactions between individual populations of the soil microbiome. To better understand these interactions and community processes, we used chitin, a major carbon and nitrogen source in soil, as a test substrate to investigate microbial interactions during its decomposition. Chitin was applied to a model soil consortium that we developed, “model soil consortium-2” (MSC-2), consisting of eight members of diverse phyla and including both chitin degraders and nondegraders. A multiomics approach revealed how MSC-2 community-level processes during chitin decomposition differ from monocultures of the constituent species. Emergent properties of both species and the community were found, including changes in the chitin degradation potential of Streptomyces species and organization of all species into distinct roles in the chitin degradation process. The members of MSC-2 were further evaluated via metatranscriptomics and community metabolomics. Intriguingly, the most abundant members of MSC-2 were not those that were able to metabolize chitin itself, but rather those that were able to take full advantage of interspecies interactions to grow on chitin decomposition products. Using a model soil consortium greatly increased our knowledge of how carbon is decomposed and metabolized in a community setting, showing that niche size, rather than species metabolic capacity, can drive success and that certain species become active carbon degraders only in the context of their surrounding community. These conclusions fill important knowledge gaps that are key to our understanding of community interactions that support carbon and nitrogen cycling in soil. IMPORTANCE The soil microbiome performs many functions that are key to ecology, agriculture, and nutrient cycling. However, because of the complexity of this ecosystem we do not know the molecular details of the interactions between microbial species that lead to these important functions. Here, we use a representative but simplified model community of bacteria to understand the details of these interactions. We show that certain species act as primary degraders of carbon sources and that the most successful species are likely those that can take the most advantage of breakdown products, not necessarily the primary degraders. We also show that a species phenotype, including whether it is a primary degrader or not, is driven in large part by the membership of the community it resides in. These conclusions are critical to a better understanding of the soil microbial interaction network and how these interactions drive central soil microbiome functions.

RNA Viruses Linked to Eukaryotic Hosts in Thawed Permafrost

Abstract: Permafrost is thawing at a rapid pace in the Arctic with largely unknown consequences on ecological processes that are fundamental to Arctic ecosystems. This is the first study to determine the composition of RNA viruses in thawed permafrost. ABSTRACT Arctic permafrost is thawing due to global warming, with unknown consequences on the microbial inhabitants or associated viruses. DNA viruses have previously been shown to be abundant and active in thawing permafrost, but little is known about RNA viruses in these systems. To address this knowledge gap, we assessed the composition of RNA viruses in thawed permafrost samples that were incubated for 97 days at 4°C to simulate thaw conditions. A diverse RNA viral community was assembled from metatranscriptome data including double-stranded RNA viruses, dominated by Reoviridae and Hypoviridae, and negative and positive single-stranded RNA viruses, with relatively high representations of Rhabdoviridae and Leviviridae, respectively. Sequences corresponding to potential plant and human pathogens were also detected. The detected RNA viruses primarily targeted dominant eukaryotic taxa in the samples (e.g., fungi, Metazoa and Viridiplantae) and the viral community structures were significantly associated with predicted host populations. These results indicate that RNA viruses are linked to eukaryotic host dynamics. Several of the RNA viral sequences contained auxiliary metabolic genes encoding proteins involved in carbon utilization (e.g., polygalacturosase), implying their potential roles in carbon cycling in thawed permafrost. IMPORTANCE Permafrost is thawing at a rapid pace in the Arctic with largely unknown consequences on ecological processes that are fundamental to Arctic ecosystems. This is the first study to determine the composition of RNA viruses in thawed permafrost. Other recent studies have characterized DNA viruses in thawing permafrost, but the majority of DNA viruses are bacteriophages that target bacterial hosts. By contrast RNA viruses primarily target eukaryotic hosts and thus represent potential pathogenic threats to humans, animals, and plants. Here, we find that RNA viruses in permafrost are novel and distinct from those in other habitats studied to date. The COVID-19 pandemic has heightened awareness of the importance of potential environmental reservoirs of emerging RNA viral pathogens. We demonstrate that some potential pathogens were detected after an experimental thawing regime. These results are important for understanding critical viral-host interactions and provide a better understanding of the ecological roles that RNA viruses play as permafrost thaws.

A Mineral-Doped Micromodel Platform Demonstrates Fungal Bridging of Carbon Hot Spots and Hyphal Transport of Mineral-Derived Nutrients

Abstract: Fungal species are foundational members of soil microbiomes, where their contributions in accessing and transporting vital nutrients is key for community resilience. To date, the molecular mechanisms underlying fungal mineral weathering and nutrient translocation in low-nutrient environments remain poorly resolved due to the lack of a platform for spatial analysis of biotic weathering processes. ABSTRACT Soil fungi facilitate the translocation of inorganic nutrients from soil minerals to other microorganisms and plants. This ability is particularly advantageous in impoverished soils because fungal mycelial networks can bridge otherwise spatially disconnected and inaccessible nutrient hot spots. However, the molecular mechanisms underlying fungal mineral weathering and transport through soil remains poorly understood primarily due to the lack of a platform for spatially resolved analysis of biotic-driven mineral weathering. Here, we addressed this knowledge gap by demonstrating a mineral-doped soil micromodel platform where mineral weathering mechanisms can be studied. We directly visualize acquisition and transport of inorganic nutrients from minerals through fungal hyphae in the micromodel using a multimodal imaging approach. We found that Fusarium sp. strain DS 682, a representative of common saprotrophic soil fungus, exhibited a mechanosensory response (thigmotropism) around obstacles and through pore spaces (~12 μm) in the presence of minerals. The fungus incorporated and translocated potassium (K) from K-rich mineral interfaces, as evidenced by visualization of mineral-derived nutrient transport and unique K chemical moieties following fungus-induced mineral weathering. Specific membrane transport proteins were expressed in the fungus in the presence of minerals, including those involved in oxidative phosphorylation pathways and the transmembrane transport of small-molecular-weight organic acids. This study establishes the significance of a spatial visualization platform for investigating microbial induced mineral weathering at microbially relevant scales. Moreover, we demonstrate the importance of fungal biology and nutrient translocation in maintaining fungal growth under water and carbon limitations in a reduced-complexity soil-like microenvironment. IMPORTANCE Fungal species are foundational members of soil microbiomes, where their contributions in accessing and transporting vital nutrients is key for community resilience. To date, the molecular mechanisms underlying fungal mineral weathering and nutrient translocation in low-nutrient environments remain poorly resolved due to the lack of a platform for spatial analysis of biotic weathering processes. Here, we addressed this knowledge gap by developing a mineral-doped soil micromodel platform. We demonstrate the function of this platform by directly probing fungal growth using spatially resolved optical and chemical imaging methodologies. We found the presence of minerals was required for fungal thigmotropism around obstacles and through soil-like pore spaces, and this was related to fungal transport of potassium (K) and corresponding K speciation from K-rich minerals. These findings provide new evidence and visualization into hyphal transport of mineral-derived nutrients under nutrient and water stresses.

Mass spectral imaging showing the plant growth-promoting rhizobacteria's effect on the Brachypodium awn.

Abstract: The plant growth-promoting rhizobacteria (PGPR) on the host plant surface play a key role in biological control and pathogenic response in plant functions and growth. However, it is difficult to elucidate the PGPR effect on plants. Such information is important in biomass production and conversion. Brachypodium distachyon (Brachypodium), a genomics model for bioenergy and native grasses, was selected as a C3 plant model; and the Gram-negative Pseudomonas fluorescens SBW25 (P.) and Gram-positive Arthrobacter chlorophenolicus A6 (A.) were chosen as representative PGPR strains. The PGPRs were introduced to the Brachypodium seed's awn prior to germination, and their possible effects on the seeding and growth were studied using different modes of time-of-flight secondary ion mass spectrometry (ToF-SIMS) measurements, including a high mass-resolution spectral collection and delayed image extraction. We observed key plant metabolic products and biomarkers, such as flavonoids, phenolic compounds, fatty acids, and auxin indole-3-acetic acid in the Brachypodium awns. Furthermore, principal component analysis and two-dimensional imaging analysis reveal that the Brachypodium awns are sensitive to the PGPR, leading to chemical composition and morphology changes on the awn surface. Our results show that ToF-SIMS can be an effective tool to probe cell-to-cell interactions at the biointerface. This work provides a new approach to studying the PGPR effects on awn and shows its potential for the research of plant growth in the future.

Metagenomes from Arctic Soil Microbial Communities from the Barrow Environmental Observatory, Utqiaġvik, AK, USA

Abstract: Here, we report 36 active-layer and 17 permafrost metagenomes from Utqiaġvik, AK, USA. Samples were collected from different topographical features and depths to study Arctic tundra microbiomes. ABSTRACT Here, we report 36 active-layer and 17 permafrost metagenomes from Utqiaġvik, AK, USA. Samples were collected from different topographical features and depths to study Arctic tundra microbiomes.