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Bacterial Rhizoplane Colonization Patterns of Buchloe dactyloides Growing in Metalliferous Mine Tailings Reflect Plant Status and Biogeochemical Conditions

Abstract

Plant establishment during phytostabilization of legacy mine tailings in semiarid regions is challenging due to low pH, low organic carbon, low nutrients, and high toxic metal(loid) concentrations. Plant-associated bacterial communities are particularly important under these harsh conditions because of their beneficial services to plants. We hypothesize that bacterial colonization profiles on rhizoplane surfaces reflect deterministic processes that are governed by plant health and the root environment. The aim of this study was to identify associations between bacterial colonization patterns on buffalo grass (Buchloe dactyloides) rhizoplanes and both plant status (leaf chlorophyll and plant cover) and substrate biogeochemistry (pH, electrical conductivity, total organic carbon, total nitrogen, and rhizosphere microbial community). Buffalo grass plants from mesocosm- and field-scale phytostabilization trials conducted with tailings from the Iron King Mine and Humboldt Smelter Superfund Site in Dewey-Humboldt, Arizona, were analyzed. These tailings are extremely acidic and have arsenic and lead concentrations of 2–4 g kg−1 substrate. Bacterial communities on rhizoplanes and in rhizosphere-associated substrate were characterized using fluorescence in situ hybridization and 16S rRNA gene amplicon sequencing, respectively. The results indicated that the metabolic status of rhizoplane bacterial colonizers is significantly related to plant health. Principal component analysis revealed that root-surface Alphaproteobacteria relative abundance was associated most strongly with substrate pH and Gammaproteobacteria relative abundance associated strongly with substrate pH and plant cover. These factors also affected the phylogenetic profiles of the associated rhizosphere communities. In summary, rhizoplane bacterial colonization patterns are plant specific and influenced by plant status and rhizosphere biogeochemical conditions.

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Acknowledgements

We thank Scott White for his work in designing and implementing the IKMHSS field study. We thank Steven Schuchardt, president of North American Industries, for providing access to the IKMHSS site and help with irrigation. We thank all volunteer students from Environmental Microbiology, Environmental Biochemistry, and Contaminant Transport Labs for their help during field implementation and sampling trips, and especially Corin Hammond for her dedicated work in helping to organize as well as participate in these sampling trips. We also thank Alexis Valentín-Vargas for collecting and fixing buffalo grass root samples from the mesocosm study that were used in the current study. This work was supported by the National Institute of Environmental and Health Sciences (NIEHS) Superfund Research Program (SRP) grant P42 ES004940 and R01 ES01709 and the National Science Foundation Graduate Research Fellowhip Program (NSF GRFP) grant DGE-1143953.

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Correspondence to Julia W. Neilson.

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Honeker, L.K., Neilson, J.W., Root, R.A. et al. Bacterial Rhizoplane Colonization Patterns of Buchloe dactyloides Growing in Metalliferous Mine Tailings Reflect Plant Status and Biogeochemical Conditions. Microb Ecol 74, 853–867 (2017). https://doi.org/10.1007/s00248-017-0998-7

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Keywords

  • Phytostabilization
  • Rhizosphere
  • Rhizoplane
  • Plant-microbe associations
  • FISH
  • 16S rRNA gene amplicon sequencing