Microbial diversity and keystone species drive soil nutrient cycling and multifunctionality following mangrove restoration

Abstract

Vegetation restoration exerts transformative effects on nutrient cycling, microbial communities, and ecosystem functions. While extensive research has been conducted on the significance of mangroves and their restoration efforts, the effectiveness of mangrove restoration in enhancing soil multifunctionality in degraded coastal wetlands remains unclear. Herein, we carried out a field experiment to explore the impacts of mangrove restoration and its chronosequence on soil microbial communities, keystone species, and soil multifunctionality, using unrestored aquaculture ponds as controls. The results revealed that mangrove restoration enhanced soil multifunctionality, with these positive effects progressively amplifying over the restoration chronosequence. Furthermore, mangrove restoration led to a substantial increase in microbial diversity and a reshaping of microbial community composition, increasing the relative abundance of dominant phyla such as Nitrospirae, Deferribacteres, and Fusobacteria. Soil multifunctionality exhibited positive correlations with microbial diversity, suggesting a link between variations in microbial diversity and soil multifunctionality. Metagenomic screening demonstrated that mangrove restoration resulted in a simultaneous increase in the abundance of nitrogen (N) related genes, such as N fixation (nirD/H/K), nitrification (pmoA-amoA/B/C), and denitrification (nirK, norB/C, narG/H, napA/B), as well as phosphorus (P)-related genes, including organic P mineralization (phnX/W, phoA/D/G, phnJ/N/P), inorganic P solubilization (gcd, ppx-gppA), and transporters (phnC/D/E, pstA/B/C/S)). The relationship between the abundance of keystone species (such as phnC/D/E) and restoration-induced changes in soil multifunctionality indicates that mangrove restoration enhances soil multifunctionality through an increase in the abundance of keystone species associated with N and P cycles. Additionally, it was observed that changes in microbial community and multifunctionality were largely associated with shifts in soil salinity. These findings demonstrate that mangrove restoration positively influences soil multifunctionality and shapes nutrient dynamics, microbial communities, and overall ecosystem resilience. As global efforts continue to focus on ecosystem restoration, understanding the complexity of mangrove-soil interactions is critical for effective nutrient management and mangrove conservation.