Arsenic redox transformations and cycling in the rhizosphere of Pteris vittata and Pteris quadriaurita

Stefan Wagner,Christoph Hoefer,Markus Puschenreiter,Walter W Wenzel,Eva Oburger,Stephan Hann,Brett Robinson,Ruben Kretzschmar,Jakob Santner

doi:10.1016/j.envexpbot.2020.104122

Abstract

Pteris vittata (PV) and Pteris quadriaurita (PQ) are reported to hyperaccumulate arsenic (As) when grown in As-rich soil. Yet, little is known about the impact of their unique As accumulation mechanisms on As transformations and cycling at the soil-root interface. Using a combined approach of two-dimensional (2D), sub-mm scale solute imaging of arsenite (AsIII), arsenate (AsV), phosphorus (P), manganese (Mn), iron (Fe) and oxygen (O2), we found localized patterns of AsIII/AsV redox transformations in the PV rhizosphere (AsIII/AsV ratio of 0.57) compared to bulk soil (AsIII/AsV ratio of ≤0.04). Our data indicate that the high As root uptake, translocation and accumulation from the As-rich experimental soil (2080 mg kg−1) to PV fronds (6986 mg kg−1) induced As detoxification via AsV reduction and AsIII root efflux, leading to AsIII accumulation and re-oxidation to AsV in the rhizosphere porewater. This As cycling mechanism is linked to the reduction of O2 and MnIII/IV (oxyhydr)oxides resulting in decreased O2 levels and increased Mn solubilization along roots. Compared to PV, we found 4-fold lower As translocation to PQ fronds (1611 mg kg−1), 2-fold lower AsV depletion in the PQ rhizosphere, and no AsIII efflux from PQ roots, suggesting that PQ efficiently controls As uptake to avoid toxic As levels in roots. Analysis of root exudates obtained from soil-grown PV showed that As acquisition by PV roots was not associated with phytic acid release. Our study demonstrates that two closely-related As-accumulating ferns have distinct mechanisms for As uptake modulating As cycling in As-rich environments.

Highlights

Arsenic (As) is a widespread and persistent metalloid contaminant in natural soil environments
Reproducible patterns in the rhizospheric AsIII/AsV distribution and total As accumulation in fern tissues revealed differential As uptake mechanisms and biotransformation pathways in Pteris vittata (PV) and Pteris quadriaurita (PQ)
We conclude that the high As uptake, translocation and accumulation from As-rich soil in PV fronds induced the need for root As detoxification via AsV reduction and AsIII efflux leading to AsIII accumulation and re-oxidation to AsV in the rhizosphere porewater

Summary

Introduction

Arsenic (As) is a widespread and persistent metalloid contaminant in natural soil environments. Terrestrial plants generally restrict As uptake in roots and translocation to shoots to survive As stress (Fitz and Wenzel, 2006). 13 species from the Pteris genus of ferns, including Pteris vittata (PV) and Pteris quadriaurita (PQ), are known to hyperaccumulate As (Chen et al., 2018; Claveria et al, 2019), showing efficient As root uptake and translocation from As-rich soil to aboveground tissues (i.e. fronds) (Ma et al, 2001; Zhao et al, 2002; Meharg, 2003; Srivastava et al, 2006), which is used for the plant-based remediation (i.e. phytoremediation) of As-contaminated environments (Tu et al, 2004a; Wang and Ma, 2015; da Silva et al, 2018).

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