Hidden drivers of restoration: Persistent divergence in soil microbiome functional capacity post-habitat reconstruction

Abstract

Ecosystems today are facing unprecedented environmental stress, leading to large-scale losses of habitat and ecosystem services. To address this, reconstructive efforts aim to restore habitat features and their natural complexity, biodiversity, and function. However, many reconstructive efforts fail to consider microbial communities, even though they play key roles in decomposition, nutrient cycling, and plant and animal health. Here, we use shotgun metagenomic sequencing to compare the structure and functional capacity of soil microbial communities from natural Everglades tree islands and islands constructed within a landscape-scale experimental Everglades restoration effort, followed by a manipulative greenhouse experiment to link tree sapling traits with microbiome functional genetic divergence. We found that constructed and natural island microbiomes exhibited strong, robust, and persistent divergence in both taxonomic and functional composition, with natural island microbial communities having greater functional genetic diversity and redundancy. Furthermore, we identified enrichment in functional pathways in constructed island microbiomes such as those involved in pollutant degradation that may reflect continued disturbance leading to shifts in microbiome functional profiles. Despite their capacity for functions such as nitrogen cycling we found to be important for supporting sapling growth, constructed island microbiomes displayed reduced functional genetic diversity and redundancy and were enriched in pathways associated with environmental disturbance, suggesting a potentially diminished capacity for long-term resilience. Overall, our assessment of soil microbial communities in reconstructed and natural habitats emphasizes how reconstructive restoration can impact microbial functional repertoires and highlights the importance of these hidden players in management and restoration of ecosystem health.