Microbiome differentiation between micro-sympatric maize and teosinte reveals domestication-driven functional erosion of the microbiome across plant compartments

Introduction. Crop domestication has fundamentally transformed plant phenotypes through artificial selection, yet the consequences of domestication for plant-associated microbial communities across the plant-soil continuum remain poorly understood. Gap Statement. While recent studies suggest that domestication impacts microbiome structures, the magnitude, mechanisms, and functional implications of such impacts have not been systematically quantified using controlled experimental designs that eliminate environmental confounding factors. Aim. To characterize and quantify the effects of crop domestication on microbial community structure and function by comparing maize (Zea mays subsp. mays) and its wild ancestor Balsas teosinte (Zea mays subsp. parviglumis) across multiple plant compartments in an unmanipulated field setting in Mexico, maize's domestication center. Methodology. We applied a micro-sympatric design in a natural setting to compare microbial communities between maize and Balsas teosinte across five plant compartments: bulk soil, rhizosphere, mucilage, leaves, and seeds. Full-length 16S rRNA gene sequencing was used for taxonomic characterization, Functional Annotation of Prokaryotic Taxa (FAPROTAX) and PICRUSt 2.0 were used to predict functional profiles, and network analysis was used to assess functional connectivity. Results. Compartment identity explained 72.2% of variation in community structure, with consistent host effects across all niches (9.0%). Teosinte maintained significantly higher microbial diversity than maize across all compartments, with pronounced differences in seeds (32.0 vs 9.3 species, P < 0.01) and rhizosphere (60.3 vs 33.8 species, P < 0.01). Eighty-nine percent of predicted metabolic functions showed significant changes associated with domestication, with teosinte exhibiting enhanced nitrogen fixation (0.89 vs 0.44 in maize mucilage), siderophore production, and pathogen suppression. Network analysis revealed functional fragmentation in maize, with reduced connections (80 to 49) and lower clustering coefficients (0.62 vs 0.25, P < 0.001). Conclusion. Balsas teosinte domestication fundamentally eroded microbial diversity and functional capacity in maize leading to a "domestication gap" that encompasses taxonomic loss, functional simplification, and network fragmentation, and replaced mutualistic plant-microbe partnerships with simplified microbial assemblages that may compromise crop resilience vis-a-vis a changing climate.