Plant-microbe-metal interactions during phytostabilization

My interest in microbial ecology as it pertains to soil health and the rhizosphere began in graduate school, where I worked with Raina Maier and Julie Neilson in the Dept. of Environmental Science at the University of Arizona. In my dissertation, titled, “Rhizosphere bacteria and phytostabilization success: The association between bacteria, plant establishment and metal(loid) immobilization in metalliferous mine tailings”, I identified microbial indicators of plant and soil health and developed a technique for probing microscale interactions between bacteria and metals on the plant root surface (Honeker et al., 2016, Journal of Microbiological Methods, https://doi.org/10.1016/j.mimet.2016.09.018.

Establishing a plant cover in metal-contaminated mine tailings in a semi-arid climate is extremely challenging, and microbes play a key role in the success or failure. Our field site was located in Iron King Mine and Humboldt Smelter Superfund Site in Dewey Humboldt, AZ where we conducted a phytostabilization experiment testing the efficacy of direct planting into the mine tailings.

Iron King Mine and Humboldt Smelter Superfund Site- Mine tailings pile
Phytostabilization – Buffalo Grass and Quailbush planted directly into mine tailings with compost amendment

To assist plant survival in the extremely harsh conditions, a compost-amendment was added to buffer the highly acidic tailings (pH 2-4) and provide a heterotrophic bacterial inoculum containing plant-growth-promoting bacteria (PGPB) to offset the acid-generating bacteria (AGB) including Fe/S-oxidizers resident in the bare mine tailings. I assessed the microbial communities on the root surface, rhizosphere, and bulk soil of buffalo grass plants used in the experiment. On the root surface, I found that the microbial activity and relative abundance of Gammaproteobacteria (%) was associated with plant health and establishment (leaf chlorophyll and plant cover [%]), while Alphaproteobacteria (%) was associated with pH (Honeker et al., 2017, Microbial Ecology, https://doi.org/10.1007/s00248-017-0998-7).

My other key findings were that the addition of compost amendment alleviated the plant-growth inhibiting characteristics of the mine tailings, with the rhizosphere and bulk substrate containing a diverse community with PGPB. Over time, the acid-generating potential of the mine tailings overpowered the neutralizing capacity of the compost, and re-acidification began. This was associated with an increased divergence between rhizosphere and bulk alpha diversity, with the rhizosphere maintaining high diversity and presence of PGPB, while the bulk dropped in diversity and became dominated by AGB, a demonstration of the ‘fertility island’ effect and the reduced capacity for the mine tailings to sustain plant establishment (Honeker et al., 2019, Frontiers in Microbiology, https://doi.org/10.3389/fmicb.2019.01209). Other indicators of decreased soil health included increased activity of Fe/S oxidizers and decreased nifH gene abundance in the bulk soil, which tended to occur when the pH reached ~4, below which a final indication of suppressed plant establishment occurred when these patterns extended into the rhizosphere as well. In conclusion, I identified key indicators of phytostabilization success in terms of microbial colonization patterns on the root surface, and rhizosphere and bulk substrate.

Theoretical framework for management of phytostabilization in acidic mine tailings. R, rhizosphere; B, bulk; AGB, acid generating bacteria; PGBP, plant-growth-supporting bacteria