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

Pteris vittata (PV) and Pteris quadriaurita (PQ) are reported to hyperaccumulate arsenic (As) when grown in Asrich 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 (As(III)), arsenate (As(V)), phosphorus (P), manganese (Mn), iron (Fe) and oxygen (O(2)), we found localized patterns of As(III)/As(V) redox transformations in the PV rhizosphere (As(III)/As(V) ratio of 0.57) compared to bulk soil (As(III)/As(V) 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 As(V) reduction and As(III) root efflux, leading to As(III) accumulation and re-oxidation to As(V) in the rhizosphere porewater. This As cycling mechanism is linked to the reduction of O2 and Mn(III/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 As(V) depletion in the PQ rhizosphere, and no As(III) 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.