The earthworm microbiome is resilient to exposure to biocidal metal nanoparticles

Abstract

Environmental pollution can disrupt the interactions between animals and their symbiotic bacteria, which can lead to adverse effects on the host even in the absence of direct chemical toxicity. It is therefore crucial to understand how environmental pollutants affect animal microbiomes, especially for those chemicals that are designed to target microbes. Here, we study the effects of two biocidal nanoparticles (NPs) (Ag and CuO) on the soil bacterial community and the resident gut microbiome of the earthworm Eisenia fetida over a 28-day period using metabarcoding techniques. Exposures to NPs were conducted following OECD test guidelines and effects on earthworm reproduction and juvenile biomass were additionally recorded in order to compare effects on the host to effects on microbiomes. By employing a full concentration series, we were able to link pollutants to microbiome effects in high resolution. Multivariate analysis, differential abundance analysis and species sensitivity distribution analysis showed that Ag-NPs are more toxic to soil bacteria than CuO-NPs. In contrast to the strong effects of CuO-NPs and Ag-NPs on the soil bacterial community, the earthworm gut microbiome is largely resilient to exposure to biocidal NPs. Despite this buffering effect, CuO-NPs did negatively affect the relative abundance of some earthworm symbionts, including 'Candidatus Lumbricincola'. Changes in the soil bacterial community and the earthworm microbiome occur at total copper concentrations often found or modelled to occur in agricultural fields, demonstrating that soil bacterial communities and individual taxa in the earthworm microbiome may be at risk from environmental copper exposure including in nanomaterial form.

Keywords: Earthworms; Eisenia fetida; Metals; Microbiome; Nanoparticles.