Fragmentation disrupts microbial effects on native plant community productivity

Abstract

Abstract Anthropogenic habitat fragmentation—the breaking up of natural landscapes—is a pervasive threat to biodiversity and ecosystem function world‐wide. 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. 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. 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. Furthermore, 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. 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.