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Habitat fragmentation is a leading cause of biodiversity and ecosystem function loss in the Anthropocene. Despite the importance of plant-microbiome interactions to ecosystem productivity, we have limited knowledge of how fragmentation affects microbiomes and even less knowledge of its consequences for microbial interactions with plants.Combining field surveys, microbiome sequencing, manipulative experiments, and random forest models, we investigated fragmentation legacy effects on soil microbiomes in imperiled pine rocklands, tested how compositional shifts across 14 fragmentation-altered soil microbiomes affected performance and resource allocation of three native plant species, and identified fragmentation-responding microbial families underpinning plant performance.Legacies of habitat fragmentation were associated with significant changes in microbial diversity and composition (across three of four community axes). Experiments showed plants often strongly benefited from the microbiome's presence, but fragmentation-associated changes in microbiome composition also significantly affected plant performance and resource allocation across all seven metrics examined. Finally, random forest models identified ten fungal and six bacterial families important for plant performance that changed significantly with fragmentation.Our findings not only support the existence of significant fragmentation effects on natural microbiomes, but also demonstrate for the first time that fragmentation-associated changes in microbiomes can have meaningful consequences for native plant performance and investment.

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1. Anthropogenic habitat fragmentation – the breaking up of natural landscapes – is a pervasive threat to biodiversity and ecosystem function worldwide. Fragmentation results in a mosaic of remnant native habitat patches embedded in human-modified habitat known as the “matrix”. By introducing novel environmental conditions in matrix habitats and reducing connectivity of native habitats, fragmentation can dramatically change how organisms experience their environment. The effects of fragmentation can be especially important in urban landscapes, which are expanding across the globe. Despite this surging threat and the importance of microbiomes for ecosystem services, we know very little about how fragmentation affects microbiomes and even less about their consequences for plant-microbe interactions in urban landscapes. 2. By combining field surveys, microbiome sequencing, and experimental mesocosms, we (1) investigated how microbial community diversity, composition, and functional profiles differed between 15 native pine rockland fragments and the adjacent urban matrix habitat, (2) identified habitat attributes that explained significant variation in microbial diversity of native core habitat compared to urban matrix, and (3) tested how changes in urbanized and low connectivity microbiomes affected plant community productivity. 3. We found urban and native microbiomes differed substantively in diversity, composition, and functional profiles, including symbiotic fungi decreasing 81% and pathogens increasing 327% in the urban matrix compared to native habitat. Further, fungal diversity rapidly declined as native habitats became increasingly isolated, with ~50% of variation across the landscape explained by habitat connectivity alone. Interestingly, microbiomes from native habitats increased plant productivity by ~300% while urban matrix microbiomes had no effect, suggesting that urbanization may decouple beneficial plant-microbe interactions. In addition, microbial diversity within native habitats explained significant variation in plant community productivity, with higher productivity linked to more diverse microbiomes from more connected, larger fragments. 4. Synthesis. Taken together, our study not only documents significant changes in microbial diversity, composition, and functions in the urban matrix, but also supports that two aspects of habitat fragmentation — the introduction of a novel urban matrix and reduced habitat connectivity — disrupt microbial effects on plant community productivity, highlighting preservation of native microbiomes as critical for productivity in remnant fragments.