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Agaves are plants native to North America that sustain life in arid and semiarid ecosystems. Previous studies revealed that cultivated plants of Agave tequilana had lower microbial diversity and functionality than wild Agave species. Here, we tested if synthetic communities (syncoms), based on microbial hubs or taxa with enriched microbial functions, could increase microbial diversity, plant health, and productivity in A. tequilana. We applied 10 syncoms to the phyllospheres of 6-month-old plants of A. tequilana in the field and monitored their development for 2 years. Amplicon sequencing of 16S-rRNA-V4 and ITS2 revealed that the inoculated syncoms played a negligible or minor role in the assembly of the prokaryotic and eukaryotic phyllospheric communities associated with A. tequilana, respectively. However, syncoms based on microbial hubs, particularly those observed in the phyllosphere associated with wild A. salmiana (PFCS), promoted microbial communities with higher alpha diversity. Some of these syncom-derived phyllospheric communities consumed a greater variety of carbon sources; had more complex co-occurrence networks; and increased the content of sugars (oBrix, a measure of productivity in agaves) in the stem and changed the leaf metabolome. Our work demonstrates that the application of syncoms formulated based on predicted microbe–microbe interactions and metagenomic analyses of microbial communities in cultivated and wild plant species represents an effective tool to improve the sustainability and productivity of crops in arid ecosystems. [Graphic: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Microbial symbionts account for survival, development, fitness and evolution of eukaryotic hosts. These microorganisms together with their host form a biological unit known as holobiont. Recent studies have revealed that the holobiont of agaves and cacti comprises a diverse and structured microbiome, which might be important for its adaptation to drylands. Here, we investigated the functional signatures of the prokaryotic communities of the soil and the episphere, that includes the rhizosphere and phyllosphere, associated with the cultivated Agave tequilana and the native and sympatric Agave salmiana, Opuntia robusta and Myrtillocactus geometrizans by mining shotgun metagenomic data. Consistent with previous phylogenetic profiling, we found that Proteobacteria, Actinobacteria and Firmicutes were the main represented phyla in the episphere of agaves and cacti, and that clustering of metagenomes correlated with the plant compartment. In native plants, genes related to aerobic anoxygenic phototrophy and photosynthesis were enriched in the phyllosphere and soil, while genes coding for biofilm formation and quorum sensing were enriched in both epiphytic communities. In the episphere of cultivated A. tequilana fewer genes were identified, but they belonged to similar pathways than those found in native plants. A. tequilana showed a depletion in several genes belonging to carbon metabolism, secondary metabolite biosynthesis and xenobiotic degradation suggesting that its lower microbial diversity might be linked to functional losses. However, this species also showed an enrichment in biofilm and quorum sensing in the epiphytic compartments, and evidence for nitrogen fixation in the rhizosphere. Aerobic anoxygenic phototrophic markers were represented by Rhizobiales (Methylobacterium) and Rhodospirillales (Belnapia) in the phyllosphere, while photosystem genes were widespread in Bacillales and Cyanobacteria. Nitrogen fixation and biofilm formation genes were mostly related to Proteobacteria. These analyses support the idea of niche differentiation in the rhizosphere and phyllosphere of agaves and cacti and shed light on the potential mechanisms by which epiphytic microbial communities survive and colonize plants of arid and semiarid ecosystems. This study establishes a guideline for testing the relevance of the identified functional traits on the microbial community and the plant fitness.

Abstract When a pathogen invades a plant, it encounters a diverse microbiota with some members contributing to the health and growth of the plant host. So far, the relevance of interactions between pathogens and the plant microbiota are poorly understood; however, new lines of evidence suggest that pathogens play an important role in shaping the microbiome of their host during invasion. This review aims to summarize recent findings that document changes in microbial community composition during the invasion of filamentous pathogens in plant tissues. We explore the known mechanisms of interaction between plant pathogens and the host microbiota that underlie these changes, particularly the pathogen-encoded traits that are produced to target specific microbes. Moreover, we discuss the limitations of current strategies and shed light on new perspectives to study the complex interaction networks between filamentous pathogens and the plant microbiome.