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The plant microbiota can complement host functioning, leading to improved growth and health under unfavorable conditions. Microbiome engineering could therefore become a transformative technique for crop production. Microbiome genes, abbreviated as M genes, provide valuable targets for shaping plant-associated microbial communities. Plant genotype is a major driver of the structure and function of plant-associated microbial communities. In this Perspective, the author discusses targeted microbiome engineering through identification and selection of Microbiome genes within crops genomes.

Background One promise of the recently presented microbiome definition suggested that, in combination with unifying concepts and standards, microbiome research could be important for solving new challenges associated with anthropogenic-driven changes in various microbiota. With this commentary we want to further elaborate this suggestion, because we noticed specific signatures in microbiota affected by the Anthropocene. Results Here, we discuss this based on a review of available literature and our own research targeting exemplarily the plant microbiome. It is not only crucial for plants themselves but also linked to planetary health. We suggest that different human activities are commonly linked to a shift of diversity and evenness of the plant microbiota, which is also characterized by a decrease of host specificity, and an increase of r-strategic microbes, pathogens, and hypermutators. The resistome, anchored in the microbiome, follows this shift by an increase of specific antimicrobial resistance (AMR) mechanisms as well as an increase of plasmid-associated resistance genes. This typical microbiome signature of the Anthropocene is often associated with dysbiosis and loss of resilience, and leads to frequent pathogen outbreaks. Although several of these observations are already confirmed by meta-studies, this issue requires more attention in upcoming microbiome studies. Conclusions Our commentary aims to inspire holistic studies for the development of solutions to restore and save microbial diversity for ecosystem functioning as well as the closely connected planetary health. ETPSa4FGwVwF5mWJYnX5UR Video abstract

Mutualistic interactions within microbial assemblages provide a survival strategy under extreme conditions; however, little is known about the complexity of interaction networks in multipartite, free-living communities. In the present study, the interplay within algae-dominated microbial communities exposed to harsh environmental influences in the Austrian Alps was assessed in order to reveal the interconnectivity of eukaryotic and prokaryotic inhabitants. All analyzed snowfields harbored distinct microbial communities. Network analyses revealed that mutual exclusion prevailed among microalgae in the alpine environment, while bacteria were mainly positively embedded in the interaction networks. Especially members of Proteobacteria , with a high prevalence of Oxalobacteraceae , Pseudomonadaceae , and Sphingomonadaceae showed genus-specific co-occurrences with distinct microalgae. Co-cultivation experiments with algal and bacterial isolates confirmed beneficial interactions that were predicted based on the bioinformatic analyses; they resulted in up to 2.6-fold more biomass for the industrially relevant microalga Chlorella vulgaris , and up to 4.6-fold increase in biomass for the cryophilic Chloromonas typhlos . Our findings support the initial hypothesis that microbial communities exposed to adverse environmental conditions in alpine systems harbor inter-kingdom supportive capacities. The insights into mutualistic inter-kingdom interactions and the ecology of microalgae within complex microbial communities provide explanations for the prevalence and resilience of such assemblages in alpine environments.

In terrestrial ecosystems, plant leaves provide the largest biological habitat for highly diverse microbial communities, known as the phyllosphere microbiota. However, the underlying mechanisms of host-driven assembly of these ubiquitous communities remain largely elusive. Here, we conduct a large-scale and in-depth assessment of the rice phyllosphere microbiome aimed at identifying specific host-microbe links. A genome-wide association study reveals a strong association between the plant genotype and members of four bacterial orders, Pseudomonadales, Burkholderiales, Enterobacterales and Xanthomonadales. Some of the associations are specific to a distinct host genomic locus, pathway or even gene. The compound 4-hydroxycinnamic acid (4-HCA) is identified as the main driver for enrichment of bacteria belonging to Pseudomonadales. 4-HCA can be synthesized by the host plant’s OsPAL02 from the phenylpropanoid biosynthesis pathway. A knockout mutant of OsPAL02 results in reduced Pseudomonadales abundance, dysbiosis of the phyllosphere microbiota and consequently higher susceptibility of rice plants to disease. Our study provides a direct link between a specific plant metabolite and rice phyllosphere homeostasis opening possibilities for new breeding strategies. The underlying mechanisms of host-driven assembly of phyllosphere microbiota remain largely unknown. Here, 4-hydroxycinnamic acid synthesized by the rice plant’s PAL02 in the phenylpropanoid biosynthesis pathway is shown to be the main driver for enrichment of Pseudomonadales bacteria.

Cereal crop production is severely affected by seed-borne bacterial diseases across the world. Locally occurring disease resistance in various crops remains elusive. Here, we have observed that rice plants of the same cultivar can be differentiated into disease-resistant and susceptible phenotypes under the same pathogen pressure. Following the identification of a seed-endophytic bacterium as the resistance-conferring agent, integration of high-throughput data, gene mutagenesis and molecular interaction assays facilitated the discovery of the underlying mode of action. Sphingomonas melonis that is accumulated and transmitted across generations in disease-resistant rice seeds confers resistance to disease-susceptible phenotypes by producing anthranilic acid. Without affecting cell growth, anthranilic acid interferes with the sigma factor RpoS of the seed-borne pathogen Burkholderia plantarii , probably leading to impairment of upstream cascades that are required for virulence factor biosynthesis. The overall findings highlight the hidden role of seed endophytes in the phytopathology paradigm of ‘disease triangles’, which encompass the plant, pathogens and environmental conditions. These insights are potentially exploitable for modern crop cultivation threatened by globally widespread bacterial diseases. In rice, one endophyte ( Sphingomonas melonis ) colonizes seeds and produces anthranilic acid, which confers resistance to a bacterial pathogen ( Burkholderia plantarii ) in the plant.

The expanding antibiotic resistance crisis calls for a more in depth understanding of the importance of antimicrobial resistance genes (ARGs) in pristine environments. We, therefore, studied the microbiome associated with Sphagnum moss forming the main vegetation in undomesticated, evolutionary old bog ecosystems. In our complementary analysis of culture collections, metagenomic data and a fosmid library from different geographic sites in Europe, we identified a low abundant but highly diverse pool of resistance determinants, which targets an unexpectedly broad range of 29 antibiotics including natural and synthetic compounds. This derives both, from the extraordinarily high abundance of efflux pumps (up to 96%), and the unexpectedly versatile set of ARGs underlying all major resistance mechanisms. Multi-resistance was frequently observed among bacterial isolates, e.g. in Serratia , Rouxiella, Pandoraea, Paraburkholderia and Pseudomonas . In a search for novel ARGs, we identified the new class A β-lactamase Mm3. The native Sphagnum resistome comprising a highly diversified and partially novel set of ARGs contributes to the bog ecosystem´s plasticity. Our results reinforce the ecological link between natural and clinically relevant resistomes and thereby shed light onto this link from the aspect of pristine plants. Moreover, they underline that diverse resistomes are an intrinsic characteristic of plant-associated microbial communities, they naturally harbour many resistances including genes with potential clinical relevance.

Background The plant microbiota is crucial for plant health and growth. Recently, vertical transmission of a beneficial core microbiota was identified for crop seeds, but for native plants, complementary mechanisms are almost completely unknown. Methods We studied the seeds of eight native plant species growing together for centuries under the same environmental conditions in Alpine meadows (Austria) by qPCR, FISH-CLSM, and amplicon sequencing targeting bacteria, archaea, and fungi. Results Bacteria and fungi were determined with approx. 10 10 gene copy numbers g −1 seed as abundant inhabitants. Archaea, which were newly discovered as seed endophytes, are less and represent only 1.1% of the signatures. The seed microbiome was highly diversified, and all seeds showed a species-specific, highly unique microbial signature, sharing an exceptionally small core microbiome. The plant genotype (species) was clearly identified as the main driver, while different life cycles (annual/perennial) had less impact on the microbiota composition, and fruit morphology (capsule/achene) had no significant impact. A network analysis revealed significant co-occurrence patterns for bacteria and archaea, contrasting with an independent fungal network that was dominated by mutual exclusions. Conclusions These novel insights into the native seed microbiome contribute to a deeper understanding of seed microbial diversity and phytopathological processes for plant health, and beyond that for ecosystem plasticity and diversification within plant-specific microbiota.

Background Bogs are unique ecosystems inhabited by distinctive, coevolved assemblages of organisms, which play a global role for carbon storage, climate stability, water quality and biodiversity. To understand ecology and plant–microbe co-occurrence in bogs, we selected 12 representative species of bryophytes and vascular plants and subjected them to a shotgun metagenomic sequencing approach. We explored specific plant–microbe associations as well as functional implications of the respective communities on their host plants and the bog ecosystem. Results Microbial communities were shown to be functionally adapted to their plant hosts; a higher colonization specificity was found for vascular plants. Bryophytes that commonly constitute the predominant Sphagnum layer in bogs were characterized by a higher bacterial richness and diversity. Each plant group showed an enrichment of distinct phylogenetic and functional bacterial lineages. Detailed analyses of the metabolic potential of 28 metagenome-assembled genomes (MAGs) supported the observed functional specification of prevalent bacteria. We found that novel lineages of Betaproteobacteria and Actinobacteria in the bog environment harboured genes required for carbon fixation via RuBisCo. Interestingly, several of the highly abundant bacteria in both plant types harboured pathogenicity potential and carried similar virulence factors as found with corresponding human pathogens. Conclusions The unexpectedly high specificity of the plant microbiota reflects intimate plant–microbe interactions and coevolution in bog environments. We assume that the detected pathogenicity factors might be involved in coevolution processes, but the finding also reinforces the role of the natural plant microbiota as a potential reservoir for human pathogens. Overall, the study demonstrates how plant–microbe assemblages can ensure stability, functioning and ecosystem health in bogs. It also highlights the role of bog ecosystems as a playground for plant–microbe coevolution. CSBTkEkudLxGFKgcLKq6BM Video abstract

The plant microbiota fulfils various crucial functions related to host health, fitness, and productivity. Over the past years, the number of plant microbiome studies continued to steadily increase. Technological advancements not only allow us to produce constantly increasing datasets, but also to extract more information from them in order to advance our understanding of plant-microbe interactions. The growing knowledge base has an enormous potential to improve microbiome-based, sustainable agricultural practices, which are currently poorly understood and have yet to be further developed. Cereal plants are staple foods for a large proportion of the world’s population and are therefore often implemented in microbiome studies. In the present review, we conducted extensive literature research to reflect the current state of knowledge in terms of the microbiome of the four most commonly cultivated cereal plants. We found that currently the majority of available studies are targeting the wheat microbiome, which is closely followed by studies on maize and rice. There is a substantial gap, in terms of published studies, addressing the barley microbiome. Overall, the focus of most microbiome studies on cereal plants is on the below-ground microbial communities, and there is more research on bacteria than on fungi and archaea. A meta-analysis conducted in the frame of this review highlights microbiome similarities across different cereal plants. Our review also provides an outlook on how the plant microbiota could be harnessed to improve sustainability of cereal crop production.