Red imported fire ant (Solenopsis invicta) nesting enriches soil biodiversity but simplifies nutrient cycling functional genes

Abstract

The invasion of the red imported fire ant (Solenopsis invicta Buren) is a typical case of soil animal invasion. It has been listed as key invasive species in China, posing a serious threat to soil health, human safety, and ecosystem stability. Yet, how this invasion reshapes soil communities and,critically, their functional capabilities in agricultural ecosystems, remains akey unknown. To bridge this knowledge gap, we used amplicon methods to investigate soil biodiversity (bacteria, fungi, protists, nematodes), and used metagenomic methods to assess the diversity of functional genes related to carbon, nitrogen, phosphorus and sulfur cycling in S. invicta nests and non-nest soils in farmlands. Our results showed that the diversity of bacteria, nematodes, and certain protists and fungal groups increased in nest soils. However, this increase in biodiversity did not lead to a corresponding increase in functional gene diversity. Instead, the diversity of most functional genes associated with nutrient cycling declined in ant nests, except for carbon decomposition and phosphorus cycling genes, which were significantly enhanced. Path analysis revealed that the negative impacts of ant nesting on functional gene diversity were mainly mediated by increased bacterial diversity. These findings demonstrate that S. invicta invasion can restructure soil biotic communities while simplifying key functional genetic potential, with implications for soil nutrient turnover and long-term agricultural sustainability. This study provides critical insights for assessing the ecological risks posed by invasive ants to agroecosystems and supports the development of integrated management strategies.

Graphical abstract

Keywords

invasive species / microbial community / soil fauna / biogeochemical cycles / metagenomics

Highlight

	● An integrated environmental DNA and metagenomic approach was used to characterize soil communities and nutrient-cycling functional genes in red imported fire ant nests and non-nests soils.
	● Red imported fire ant invasion increases soil biodiversity but reduces functional gene diversity for nutrient cycling.
	● The negative impact on soil functional gene diversity is primarily mediated through increased bacterial diversity.

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