Wetland soil microbial responses to upland agricultural intensification and snail invasion

Abstract

Wetland soils harbor diverse microorganisms including bacteria, archaea, and fungi, all of which play significant roles in maintaining soil health and ecosystem functions but are susceptible to influences from multiple environmental changes. Agricultural intensification and biological invasion are two fundamental drivers of environmental change for wetlands, but their interactive effects on soil microbial communities remain less well understood, particularly for seasonal subtropical wetlands. Yet such understanding is vital for wetland conservation and management. In this study, we conducted a 14-week field mesocosm experiment to investigate how agricultural intensification and invasive apple snail (Pomacea maculata) – an emerging and increasingly concerning threat to natural and agricultural systems in southeastern U.S. – altered wetland soil microbial communities and structures. We found that invasive P. maculata showed selective effects on relative abundance of specific microbial taxa (e.g., Proteobacteria, Nitrospirota), and interactive effects with upland intensification on Spirochaetota and Mortierellomycota. Upland agricultural intensification also exerted significant and consistent effects on microbial composition and diversity across microbial domains. Changes in microbial composition were partly manifested through modifications in water chemistry, such as dissolved oxygen, which acted as environmental regulators. In addition, upland intensification led to more complex but sparsely connected microbial networks, while invasive snail presence decreased network complexity and resulted in greater modularity, less edge density, and longer path length, indicative of lower molecular information exchange efficiency. Our research emphasizes the need for a comprehensive evaluation of microbial responses (i.e., composition, diversity, and co-occurrence patterns) to better understand multi-stressor impacts from human activities on wetland belowground microbial communities. By holistically characterizing microbial responses, our findings show how global change drivers may impact wetland microorganisms in subtropical biomes and infer their functional consequences. Our results have important implications for sustainable landscape management and conservation of wetlands that are experiencing escalating human-induced environmental changes.