Soil rare microorganisms mediated the plant cadmium uptake: The central role of protists

Abstract

Plants and microorganisms symbiotically mediate and/or catalyse the turnover of elements in rhizosphere soils, thus directly influencing the effectiveness of phytoremediation in addressing heavy metal contamination. Soil rare microbial communities are diverse but not well understood in terms of their importance for phytoremediation. In this study, we simulated the loss of rare microorganisms through dilution-to-extinction approach, and investigated the effects on integrated rhizosphere microbiome with soil microcosm experiments, including bacteria, fungi, protists, and microfauna. Additionally, we explored the implications for ryegrass (Lolium multiflorum Lam.) growth and its uptake of Cd (cadmium). Compared with the undiluted group, ryegrass exhibited a significant decrease in Cd uptake ranging from 52.34 % to 73.71 % in the rare species-loss soils, indicating a lack of functional redundancy in rhizosphere soil microbial community following rare species loss. Interestingly, these soils displayed a remarkable 1.79-fold increase in plant biomass and a 41.02 % increase in plant height. By sequencing the 16S, 18S, and ITS rRNA gene amplicons of rhizosphere microbes, we found that soil rare species loss decreased the rhizosphere microbial α-diversity, changed the community structures, and shifted the functional potential. Protists were particularly affected. Through the analysis of species co-occurrence networks, along with the partial least squares path modeling, we found that the diversity of protists and bacteria and the co-occurring network connectivity of protists and fungi contributed most to plant Cd uptake and growth. These results highlighted the potential significance of rare microorganisms, particularly protists, in phytoextraction of Cd-contaminated soils, owing to their central role in the microbial food web.