Functional phases define the response of the soil microbiome to environmental change.

A major challenge in microbiome research is understanding how natural communities respond to environmental change. The ecological, spatial, and chemical complexity of soils makes understanding the metabolic response of these communities to perturbations particularly challenging. Here we measure the dynamics of respiratory nitrate utilization in >1,500 soil microcosms from 20 soil samples subjected to pH perturbations. Despite the complexity of the soil microbiome a minimal mathematical model with two parameters, the quantity of active biomass and the availability of a limiting nutrient, quantifies observed nitrate utilization dynamics across soils and pH perturbations. Across environmental perturbations, the model reveals the existence of three functional phases each with distinct qualitative dynamics of nitrate utilization over time: a phase where acidic perturbations induce cell death that limits metabolic activity, a nutrient-limiting phase where nitrate uptake is performed by dominant taxa that utilize nutrients released from the soil matrix, and a resurgent growth phase in basic conditions, where nutrients are in excess and rare taxa rapidly outgrow dominant populations. The underlying mechanism of each phase is predicted by our interpretable model and tested via amendment experiments, nutrient measurements, and sequencing. Finally, our data suggest that how soils transition between functional phases depends on the long-term history of environmental variation in the wild. Therefore, quantitative measurements and a minimal mathematical formalism reveal the existence of qualitative phases that capture the mechanisms and dynamics of a community responding to environmental change.

The potato rhizosphere microbiota correlated to the yield of three different regions in Korea.

We examined potato rhizosphere bacterial and fungal communities across three regions: Cheongju, Pyeongchang, and Gangneung. These regions have varying soil and climate conditions, resulting in different yields. We found that precipitation was the main limiting factor in our study while soil physiochemical factors affect bacterial and fungal microbiota in correlation with yield. Both bacterial and fungal microbiota showed distinct patterns according to the regions. ASVs positively correlated with yield were predominantly found in the Pyeongchang region which also produced the highest yields, while ASVs negatively correlated with yield were associated with Gangneung where the lowest yields were observed. The greatest bacterial and fungal diversity was detected in Pyeongchang consisting of Propionibacteriales, Burkholderiales, and Vicinamibacteriales. Gangneung, on the other hand primarily belong to Sordariales, Mortierellales, Cystofilobasidiales, and Tremellales. The putative yield-negative ASVs detected in Gangneung may have been influenced by drought stress. This work has highlighted key bacterial and fungal taxa as well as core taxa that may potentially be associated with high and low yields of potato in relation to metadata which includes soil chemical and physical parameters as well as weather data. Taken together we suggest that this information can be used to assess site suitability for potato production.

High-quality genome resource of a basidiomycetous yeast, Moesziomyces antarcticus isolate RS1, isolated from rice seed.

Moesziomyces antarcticus (anamorph: Pseudozyma antarctica) is a basidiomycetous yeast in the Ustilaginaceae family and is a core member of the rice seed microbiome. M. antarcticus RS1 was isolated from surface-sterilized rice seeds. This 18.287 Mb draft genome of M. antarcticus RS1 is comprised of a 60.8% GC content and 6,817 protein-coding genes.

Global patterns in gene content of soil microbiomes emerge from microbial interactions.

Microbial metabolism sustains life on Earth. Sequencing surveys of communities in hosts, oceans, and soils have revealed ubiquitous patterns linking the microbes present, the genes they possess, and local environmental conditions. One prominent explanation for these patterns is environmental filtering: local conditions select strains with particular traits. However, filtering assumes ecological interactions do not influence patterns, despite the fact that interactions can and do play an important role in structuring communities. Here, we demonstrate the insufficiency of the environmental filtering hypothesis for explaining global patterns in topsoil microbiomes. Using denitrification as a model system, we find that the abundances of two characteristic genotypes trade-off with pH; nar gene abundances increase while nap abundances decrease with declining pH. Contradicting the filtering hypothesis, we show that strains possessing the Nar genotype are enriched in low pH conditions but fail to grow alone. Instead, the dominance of Nar genotypes at low pH arises from an ecological interaction with Nap genotypes that alleviates nitrite toxicity. Our study provides a roadmap for dissecting how global associations between environmental variables and gene abundances arise from environmentally modulated community interactions.

Dysbiotic but nonpathogenic shift in the fecal mycobiota of patients with rheumatoid arthritis.

Rheumatoid arthritis (RA) is closely associated with the oral and gut microbiomes. Fungal cell wall components initiate inflammatory arthritis in mouse models. However, little is known regarding the role of the fungal community in the pathogenesis of RA. To evaluate the association between RA and the gut microbiome, investigations of bacterial and fungal communities in patients with RA are necessary. Therefore, we investigated the compositions and associations of fecal bacterial and fungal communities in 30 healthy controls and 99 patients with RA. The relative abundances of Bifidobacterium and Blautia decreased, whereas the relative abundance of Streptococcus increased, in patients with RA. The relative abundance of Candida in the fecal fungal community was higher in patients with RA than in healthy controls, while the relative abundance of Aspergillus was higher in healthy controls than in patients with RA. Candida species-specific gene amplification showed that C. albicans was the most abundant species of Candida. Ordination analysis and random forest classification models supported the findings of structural changes in bacterial and fungal communities. Aspergillus was the core fecal fungal genus in healthy controls, although Saccharomyces spp. are typically predominant in Western cohorts. In addition, bacterial-fungal association analyses showed that the hub node had shifted from fungi to bacteria in patients with RA. The finding of fungal dysbiosis in patients with RA suggests that fungi play critical roles in the fecal microbial communities and pathogenesis of RA.

Cross-kingdom co-occurrence networks in the plant microbiome: Importance and ecological interpretations.

Microbial co-occurrence network analysis is being widely used for data exploration in plant microbiome research. Still, challenges lie in how well these microbial networks represent natural microbial communities and how well we can interpret and extract eco-evolutionary insights from the networks. Although many technical solutions have been proposed, in this perspective, we touch on the grave problem of kingdom-level bias in network representation and interpretation. We underscore the eco-evolutionary significance of using cross-kingdom (bacterial-fungal) co-occurrence networks to increase the network's representability of natural communities. To do so, we demonstrate how ecosystem-level interpretation of plant microbiome evolution changes with and without multi-kingdom analysis. Then, to overcome oversimplified interpretation of the networks stemming from the stereotypical dichotomy between bacteria and fungi, we recommend three avenues for ecological interpretation: (1) understanding dynamics and mechanisms of co-occurrence networks through generalized Lotka-Volterra and consumer-resource models, (2) finding alternative ecological explanations for individual negative and positive fungal-bacterial edges, and (3) connecting cross-kingdom networks to abiotic and biotic (host) environments.

Compositional Shift of Bacterial, Archaeal, and Fungal Communities Is Dependent on Trophic Lifestyles in Rice Paddy Soil.

The soil environment determines plants' health and performance during their life cycle. Therefore, ecological understanding on variations in soil environments, including physical, chemical, and biological properties, is crucial for managing agricultural fields. Here, we present a comprehensive and extensive blueprint of the bacterial, archaeal, and fungal communities in rice paddy soils with differing soil types and chemical properties. We discovered that natural variations of soil nutrients are important factors shaping microbial diversity. The responses of microbial diversity to soil nutrients were related to the distribution of microbial trophic lifestyles (oligotrophy and copiotrophy) in each community. The compositional changes of bacterial and archaeal communities in response to soil nutrients were mainly governed by oligotrophs, whereas copiotrophs were mainly involved in fungal compositional changes. Compositional shift of microbial communities by fertilization is linked to switching of microbial trophic lifestyles. Random forest models demonstrated that depletion of prokaryotic oligotrophs and enrichment of fungal copiotrophs are the dominant responses to fertilization in low-nutrient conditions, whereas enrichment of putative copiotrophs was important in high-nutrient conditions. Network inference also revealed that trophic lifestyle switching appertains to decreases in intra- and inter-kingdom microbial associations, diminished network connectivity, and switching of hub nodes from oligotrophs to copiotrophs. Our work provides ecological insight into how soil nutrient-driven variations in microbial communities affect soil health in modern agricultural systems.

The DME demethylase regulates sporophyte gene expression, cell proliferation, differentiation, and meristem resurrection.

The flowering plant life cycle consists of alternating haploid (gametophyte) and diploid (sporophyte) generations, where the sporophytic generation begins with fertilization of haploid gametes. In Arabidopsis, genome-wide DNA demethylation is required for normal development, catalyzed by the DEMETER (DME) DNA demethylase in the gamete companion cells of male and female gametophytes. In the sporophyte, postembryonic growth and development are largely dependent on the activity of numerous stem cell niches, or meristems. Analyzing Arabidopsis plants homozygous for a loss-of-function dme-2 allele, we show that DME influences many aspects of sporophytic growth and development. dme-2 mutants exhibited delayed seed germination, variable root hair growth, aberrant cellular proliferation and differentiation followed by enhanced de novo shoot formation, dysregulation of root quiescence and stomatal precursor cells, and inflorescence meristem (IM) resurrection. We also show that sporophytic DME activity exerts a profound effect on the transcriptome of developing Arabidopsis plants, including discrete groups of regulatory genes that are misregulated in dme-2 mutant tissues, allowing us to potentially link phenotypes to changes in specific gene expression pathways. These results show that DME plays a key role in sporophytic development and suggest that DME-mediated active DNA demethylation may be involved in the maintenance of stem cell activities during the sporophytic life cycle in Arabidopsis.

Domestication of Oryza species eco-evolutionarily shapes bacterial and fungal communities in rice seed.

BACKGROUND: Plant-associated microbiomes, which are shaped by host and environmental factors, support their hosts by providing nutrients and attenuating abiotic and biotic stresses. Although host genetic factors involved in plant growth and immunity are known to shape compositions of microbial communities, the effects of host evolution on microbial communities are not well understood. RESULTS: We show evidence that both host speciation and domestication shape seed bacterial and fungal community structures. Genome types of rice contributed to compositional variations of both communities, showing a significant phylosymbiosis with microbial composition. Following the domestication, abundance inequality of bacterial and fungal communities also commonly increased. However, composition of bacterial community was relatively conserved, whereas fungal membership was dramatically changed. These domestication effects were further corroborated when analyzed by a random forest model. With these changes, hub taxa of inter-kingdom networks were also shifted from fungi to bacteria by domestication. Furthermore, maternal inheritance of microbiota was revealed as a major path of microbial transmission across generations. CONCLUSIONS: Our findings show that evolutionary processes stochastically affect overall composition of microbial communities, whereas dramatic changes in environments during domestication contribute to assembly of microbiotas in deterministic ways in rice seed. This study further provides new insights on host evolution and microbiome, the starting point of the holobiome of plants, microbial communities, and surrounding environments.