Background
Phytoremediation is a potentially cost-effective way to remediate highly contaminated mine tailing sites. However, nutrient limitations, especially the deficiency of nitrogen (N), can hinder the growth of plants and impair the phytoremediation of mine tailings. Nevertheless, pioneer plants can successfully colonize mine tailings and exhibit potential for tailing phytoremediation. Diazotrophs, especially diazotrophic endophytes, can promote the growth of their host plants. This was tested in a mine-tailing habitat by a combination of field sampling, DNA-stable isotope probing (SIP) analysis, and pot experiments.
Results
Bacteria belonging to the genera Herbaspirillum, Rhizobium, Devosia, Pseudomonas, Microbacterium, and Delftia are crucial endophytes for Chinese silvergrass (Miscanthus sinensis) grown in the tailing, the model pioneer plant selected in this study. Further, DNA-SIP using 15N2 identified Pseudomonas, Rhizobium, and Exiguobacterium as putative diazotrophic endophytes of M. sinensis. Metagenomic-binning suggested that these bacteria contained essential genes for nitrogen fixation and plant growth promotion. Finally, two diazotrophic endophytes Rhizobium sp. G-14 and Pseudomonas sp. Y-5 were isolated from M. sinensis. Inoculation of another pioneer plant in mine tailings, Bidens pilosa, with diazotrophic endophytes resulted in successful plant colonization, significantly increased nitrogen fixation activity, and promotion of plant growth.
Conclusions
This study indicated that diazotrophic endophytes have the potential to promote the growth of pioneer plant B. pilosa in mine tailings.
Biological nitrogen fixation (BNF) has important environmental implications in tailings by providing bioavailable nitrogen to these habitats and sustaining ecosystem functions. Previously, chemolithotrophic diazotrophs that dominate in mine tailings were shown to use reduced sulfur (S) as the electron donor. Tailings often contain high concentrations of As(III) that might function as an alternative electron donor to fuel BNF. Here, we tested this hypothesis and report on BNF fueled by As(III) oxidation as a novel biogeochemical process in addition to BNF fueled by S. Arsenic (As)-dependent BNF was detected in cultures inoculated from As-rich tailing samples derived from the Xikuangshan mining area in China, as suggested by nitrogenase activity assays, quantitative polymerase chain reaction, and 15 N 2 enrichment incubations. As-dependent BNF was also active in eight other As-contaminated tailings and soils, suggesting that the potential for As-dependent BNF may be widespread in As-rich habitats. DNAstable isotope probing identified Serratia spp. as the bacteria responsible for Asdependent BNF. Metagenomic binning indicated that the essential genes for As-dependent BNF [i.e., nitrogen fixation, As(III) oxidation, and carbon fixation] were present in Serratia-associated metagenome-assembled genomes. Over 20 Serratia genomes obtained from NCBI also contained essential genes for both As(III) oxidation and BNF (i.e., aioA and nif H), suggesting that Asdependent BNF may be a widespread metabolic trait in Serratia spp.
Primary succession in mine tailings is a prerequisite for tailing vegetation. Microorganisms, including bacteria, fungi, and protists, play an important role in this process in the driving force for improving the nutritional status. Compared to bacteria and fungi, protist populations have rarely been investigated regarding their role in mine tailings, especially for those inhabiting tailings associated with primary succession. Protists are the primary consumers of fungi and bacteria, and their predatory actions promote the release of nutrients immobilized in the microbial biomass, as well as the uptake and turnover of nutrients, affecting the functions of the wider ecosystems. In this study, three different types of mine tailings associated with three successional stages (original tailings, biological crusts, and Miscanthus sinensis grasslands) were selected to characterize the protistan community diversity, structure, and function during primary succession. Some members classified as consumers dominated the network of microbial communities in the tailings, especially in the original bare land tailings. The keystone phototrophs of Chlorophyceae and Trebouxiophyceae showed the highest relative abundance in the biological crusts and grassland rhizosphere, respectively. In addition, the co-occurrences between protist and bacterial taxa demonstrated that the proportion of protistan phototrophs gradually increased during primary succession. Further, the metagenomic analysis of protistan metabolic potential showed that abundances of many functional genes associated with photosynthesis increased during the primary succession of tailings. Overall, these results suggest that the primary succession of mine tailings drives the changes observed in the protistan community, and in turn, the protistan phototrophs facilitate the primary succession of tailings. This research offers an initial insight into the changes in biodiversity, structure, and function of the protistan community during ecological succession on tailings.
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