Influence of manganese abundances on iron and arsenic solubility in rice paddy soils

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Abstract

Arsenic (As) mobilization in rice paddy soils under fluctuating redox conditions is influenced by the biogeochemical cycling of redox sensitive elements such as iron (Fe) and manganese (Mn). Arsenic mobility in paddy soils is highly variable, and the influence of Mn abundances and Mn/Fe ratios on As mobility in these soils have received little attention. In this contribution, we developed a complementary set of field and laboratory experiments designed to evaluate the impact of Mn on interconnected Fe and As solubilization in rice paddy soils experiencing wetting-drying cycles through controlled irrigation. Porewater monitoring and synchrotron-based imaging and spectroscopy of thin sections prepared from an Arkansas paddy soil confirmed that As release was primarily governed by reductive dissolution of Fe (oxy)hydroxide phases. Experiments with laboratory soil microcosms amended with the synthetic nanocrystalline Mn oxide, δ-MnO2, showed that higher initial Mn/Fe inhibited Fe and As mobilization into porewater relative to unamended soil by up to 95% and 45%, respectively. Geochemical modeling suggests that pH increases driven by microbial MnO2 reduction, in conjunction with microbial Fe- and sulfate-reduction in carbonate-rich porewater, enhanced the precipitation of siderite (FeCO3(s)), mackinawite (FeS(s)), and potentially a Mn(II) arsenate phase. These secondary mineral phases likely played a greater role in controlling As solubilization than the role of Mn as a redox buffer regulating the redox conditions in the flooded soils. Field and laboratory experiments showed that alternate wetting and drying approaches with a single dry-down can be effective at reducing dissolved As concentrations in porewater through the oxidation of Fe. Differences in soil Mn/Fe ratios had no clear impact on the effectiveness of dry-downs as a strategy to reduce As mobilization.

Introduction

Arsenic (As) is a naturally-occurring toxic metalloid that is widespread in terrestrial and aquatic environments. Elevated As concentrations in the deltaic aquifers of South and Southeast Asia, many of which are heavily exploited for drinking water and irrigation, have motivated substantial research on the hydrological and biogeochemical processes governing arsenic mobility in subsurface environments (Polizzotto et al., 2008, Fendorf et al., 2010, Postma et al., 2012, Gillispie et al., 2019). There has also been growing concern over human exposure to inorganic arsenic, a non-threshold human carcinogen, through consumption of rice (Meharg and Rahman, 2003, Zhao et al., 2010). A number of alternative methods for paddy soil management have been shown to influence As uptake by rice (Linquist et al., 2015, Xu et al., 2017, Limmer et al., 2018), but there remain significant knowledge gaps around the underlying mechanisms through which paddy soil management practices regulate As mobility and uptake by plants. The fact that rice serves as a dietary staple for approximately three billion people (Zhao et al., 2010) underscores the need for process-based knowledge regarding the biogeochemical processes that limit As bioavailability in rice paddy soils.

Rice efficiently assimilates As from the soil solution due to its growth in flooded, anaerobic soil conditions which favor As solubilization. Arsenic mobilization in flooded soils is typically linked to the microbial reductive dissolution of As-bearing iron (Fe) (oxyhydr)oxide phases, and the subsequent release of As to the soil solution (Masscheleyn et al., 1991, Smedley and Kinniburgh, 2002, Blodau et al., 2008). Manganese (Mn) oxides are ubiquitous redox-active minerals that co-exist with Fe oxy(hydroxide) phases in soils and sediments, and that have direct and indirect influence on As sorption and redox processes (Lafferty et al., 2010, Ying et al., 2012, Suda and Makino, 2016). Recently a number of studies have suggested that soils that are naturally high in Mn or that have been amended with Mn, either in the form of synthetic Mn oxide minerals, Mn-impregnated biochar, or Mn nanotubes, show reduced As mobilization and/or uptake into rice plants and grains (Ehlert et al., 2016, Xu et al., 2017, Simmler et al., 2017, Yu et al., 2017, Lin et al., 2017, Li et al., 2019). While aspects of the biogeochemical interactions among As, Mn, and Fe have been explored in prior investigations, it is not clear which of these processes are responsible for diminished As solubility in soils that are elevated in Mn.

An important direct coupling between Mn and As cycling involves the role of Mn(III/IV) oxides as strong oxidants of As(III) to As(V), which can then adsorb onto surface edge sites of poorly crystalline Mn oxides (Manning et al., 2002, Villalobos, 2015, Yu et al., 2017). The extent of As release from aquifer sediments has recently been linked to extractable Mn, suggesting a role for Mn in the sequestration of As on aquifer sediments (Gillispie et al., 2016). Microbial and/or abiotic reductive dissolution of Mn oxide minerals associated with As may then act as an important mechanism releasing As into porewater. Manganese can also control the solubility of As through the precipitation of phases such as Mn3(AsO4)2 (Tournassat et al., 2002). The precipitation of this mixed As-Mn phase has been suggested in As-contaminated soils in reducing conditions (Masscheleyn et al., 1991) but its role in controlling As solubility in rice paddy environments is unclear. Alternatively, Mn oxides can exert indirect control on As release through the oxidation of Fe(II) to form Fe(III) (oxy)hydroxide minerals that can readily sorb As(III) and As(V) (Dixit and Hering, 2003, Ehlert et al., 2014), or via a redox buffering mechanism that renders the reductive dissolution of Fe(III) phases unfavorable. Since Mn oxides are more thermodynamically favorable terminal electron acceptors than Fe oxy(hydroxides), reduction of Mn oxides is expected to precede Fe (oxy)hydroxide reduction. Reduction half reactions for MnO2 and Fe(OH)3 are (25 °C; pH 7; 1 µM Mn2+ and Fe2+) (Morel and Hering, 1993):12MnO2+2H++e-12Mn2++H2OEH=+578mVFeOH3+3H++e-Fe2++3H2OEH=+59mV

Coupling these reactions to lactate as a representative electron donor gives overall oxidation-reduction reactions (Morel and Hering, 1993):12MnO2+112lactate+1.08H+12Mn2++14CO2+34H2OFeOH3+112lactate+2.08H+Fe2++14CO2+114H2O

As more thermodynamically favorable terminal electron acceptors, Mn oxides can delay the onset of Fe reductive dissolution and, in electron donor-limited systems, may reduce the overall extent of Fe reduction. When coupled to lactate oxidation, microbial reduction of Mn oxides also consumes 2.16 protons for each mol of Mn reduced (Eq. (3)), so greater utilization of Mn oxides as terminal electron acceptors may also impact soil solution pH with implications for speciation of metal(loids) and complexing ligands.

The Mn/Fe ratios in rice paddy soils around the world vary widely as a function of geology, land use, and other factors (Table 1). The impact of Mn abundance and hence Mn/Fe ratios on the timing and extent of Fe reduction, and coupled As release, has scarcely been studied (Ehlert et al., 2016, Xu et al., 2017). These biogeochemical processes are driven by changes in the saturation state of the paddy soils. In particular, alternate wetting and drying (AWD) techniques for irrigation management are growing in popularity as an approach for reducing methane emissions and water use in rice paddy fields as well as mitigating As uptake into rice (Somenahally et al., 2011, Linquist et al., 2015, Runkle et al., 2018, Carrijo et al., 2019), but little is known about time-resolved effects of AWD on cycling of redox-active elements in paddy soils.

In this contribution, we combine complementary field and laboratory experiments to elucidate the direct and indirect effects of Mn on As dynamics in rice paddy soils. Field experiments were conducted in rice paddy fields in Arkansas, which produces over half of the USA’s rice crop. The mean native Mn/Fe ratio (w/w) in the paddy fields examined here was 0.05, which is towards the upper end of reported Mn/Fe ratios in paddy soils and thus allowed us to assess the influence of relatively high Mn abundances on As release into porewaters. The role of the Mn/Fe ratio was further evaluated through laboratory microcosm experiments with the same Arkansas paddy soils amended with the synthetic nanocrystalline Mn oxide, δ-MnO2, to achieve Mn/Fe ratios (w/w) from 0.05 to 0.35. The interactions of Mn, Fe, and As in the rice paddy soil were determined through a combination of synchrotron-based micro X-ray fluorescence (µXRF) imaging and micro X-ray absorption near edge structure (µXANES) spectroscopy, monitoring of porewater chemistry and soil physical-chemical properties, and geochemical modeling. This approach allowed us to test two hypothesized mechanisms for Mn regulation of As solubility and plant-availability. The first hypothesized mechanism is that reductive dissolution of Mn oxides directly releases As into porewater, due to the role of Mn oxides in arsenite oxidation and subsequent adsorption onto Mn oxide surfaces. The second hypothesized mechanism is that Mn oxide reduction serves as a sink for electrons and protons and thus indirectly influences As solubilization via effects on Fe(III) (oxy)hydroxide reductive dissolution and/or pH-dependent precipitation of secondary mineral phases that sequester As.

Section snippets

Field experimental design

Field experiments were conducted in three adjacent rice paddy fields (40 m × 6 m) at the United States Department of Agriculture’s (USDA) Dale Bumpers National Rice Research Center (DBNRRC) in Stuttgart, Arkansas, USA. The soil texture is characterized as a Dewitt silt loam (fine, smectitic, thermic, Typic Albaqualfs) (5% sand, 78% silt, 17% clay) and the fields have been under rice-soybean crop rotation for over 20 years. Every other year, when under rice cultivation, the paddy soils were

Bulk and micro-scale elemental composition of paddy soil

Mean total arsenic concentrations in the soils of the experimental site were 19.7 mg kg−1 in the upper 12 cm of the soil column and decreased to 8.5 mg kg−1 in the 24–36 cm depth range (Table 2). 6 mg kg−1 As is often considered the threshold between a contaminated and non-contaminated rice paddy soil (Zavala and Duxbury, 2008). Total Mn concentrations changed significantly as a function of depth, with relatively high concentrations of 1100–1200 mg kg−1 in the upper 24 cm of the soil column and

The role of Mn on As distributions and mobilization in rice paddy soils

µXRF mapping of elemental distributions in rice paddy soil both before and after flooding suggested that Mn oxides played at most a minor role as a sorbent for arsenic. This finding is consistent with laboratory experiments with goethite and birnessite which showed that birnessite principally serves as an oxidant of As(III) and temporary sorbent of As(V), and that over time As(V) is redistributed onto goethite surfaces (Ying et al., 2012). A µXRF analysis of soils influenced by rhizosphere

Conclusion

While the importance of Fe (oxy)hydroxides in controlling the solubilization of As is well-established, there has been relatively little attention to the role of ubiquitous and redox-active Mn oxide minerals in regulating As mobility, particularly in the context of rice paddy environments. We performed complementary field and laboratory experiments with an Mn-rich paddy soil from a major commercial rice production area in Arkansas to explore the impacts of Mn on biogeochemical processes

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgment

The authors thank T. Sookaserm and L. Sells for field assistance at Dale Bumpers National Rice Research Center, N. Butkevich for assistance with DNA extraction and qPCR, and Dr. Thierry Adatte and Y. Sang for assistance with XRD. The authors also thank the three reviewers whose careful comments significantly improved the quality of this manuscript. This research was funded by NSF Award number EAR-1625317. Elemental analysis of field porewater samples was performed at the Dartmouth Trace Element

References (73)

  • L. Lin et al.

    Reduced arsenic accumulation in indica rice (Oryza sativa L.) cultivar with ferromanganese oxide impregnated biochar composites amendments

    Environ. Pollut.

    (2017)
  • L. Ou et al.

    Impact of soil organic carbon on monosodium methyl arsenate (MSMA) sorption and species transformation

    Chemosphere

    (2017)
  • D. Rickard

    Kinetics of FeS precipitation: Part 1. Competing reaction mechanisms

    Geochim. Cosmochim. Acta

    (1995)
  • A.A. Simanova et al.

    Probing the sorption reactivity of the edge surfaces in birnessite nanoparticles using nickel (II)

    Geochim. Cosmochim. Acta

    (2015)
  • M. Simmler et al.

    Reductive solubilization of arsenic in a mining-impacted river floodplain: Influence of soil properties and temperature

    Environ. Pollut.

    (2017)
  • P.L. Smedley et al.

    A review of the source, behaviour and distribution of arsenic in natural waters

    Appl. Geochem.

    (2002)
  • S. Stubner

    Enumeration of 16S rDNA of Desulfotomaculum lineage 1 in rice field soil by real-time PCR with SybrGreen™ detection

    J. Microbiol. Methods

    (2002)
  • A. Suda et al.

    Functional effects of manganese and iron oxides on the dynamics of trace elements in soils with a special focus on arsenic and cadmium: a review

    Geoderma

    (2016)
  • E. Viollier et al.

    The ferrozine method revisited: Fe (II)/Fe (III) determination in natural waters

    Appl. Geochem.

    (2000)
  • M. Wolthers et al.

    Surface chemistry of disordered mackinawite (FeS)

    Geochim. Cosmochim. Acta

    (2005)
  • M. Wolthers et al.

    Arsenic mobility in the ambient sulfidic environment: Sorption of arsenic (V) and arsenic (III) onto disordered mackinawite

    Geochim. Cosmochim. Acta

    (2005)
  • X. Xu et al.

    Control of arsenic mobilization in paddy soils by manganese and iron oxides

    Environ. Pollut.

    (2017)
  • X. Xu et al.

    Microbial sulfate reduction decreases arsenic mobilization in flooded paddy soils with high potential for microbial Fe reduction

    Environ. Pollut.

    (2019)
  • S.C. Ying et al.

    Oxidation and competitive retention of arsenic between iron-and manganese oxides

    Geochim. Cosmochim. Acta

    (2012)
  • Z. Yu et al.

    Effects of manganese oxide-modified biochar composites on arsenic speciation and accumulation in an indica rice (Oryza sativa L.) cultivar

    Chemosphere

    (2017)
  • Donald Langmuir et al.

    Solubility products of amorphous ferric arsenate and crystalline scorodite (FeAsO4· 2H2O) and their application to arsenic behavior in buried mine tailings

    Geochimica et Cosmochimica Acta

    (2006)
  • A. Bednar et al.

    Presence of organoarsenicals used in cotton production in agricultural water and soil of the southern United States

    J. Agric. Food. Chem.

    (2002)
  • E.D. Burton et al.

    Arsenic mobility during flooding of contaminated soil: the effect of microbial sulfate reduction

    Environ. Sci. Technol.

    (2014)
  • E.D. Burton et al.

    Sulfate availability drives divergent evolution of arsenic speciation during microbially mediated reductive transformation of schwertmannite

    Environ. Sci. Technol.

    (2013)
  • C. Chen et al.

    Sulfate–reducing bacteria and methanogens are involved in arsenic methylation and demethylation in paddy soils

    The ISME J.

    (2019)
  • S. Dixit et al.

    Comparison of arsenic (V) and arsenic (III) sorption onto iron oxide minerals: implications for arsenic mobility

    Environ. Sci. Technol.

    (2003)
  • T. Dolenec et al.

    Major and trace elements in paddy soil contaminated by Pb–Zn mining: a case study of Kočani Field, Macedonia

    Environ. Geochem. Health

    (2007)
  • M.F. Dong et al.

    Inoculation of Fe/Mn-oxidizing bacteria enhances Fe/Mn plaque formation and reduces Cd and As accumulation in Rice Plant tissues

    Plant Soil

    (2016)
  • K. Ehlert et al.

    Impact of birnessite on arsenic and iron speciation during microbial reduction of arsenic-bearing ferrihydrite

    Environ. Sci. Technol.

    (2014)
  • K. Ehlert et al.

    Effects of manganese oxide on arsenic reduction and leaching from contaminated floodplain soil

    Environ. Sci. Technol.

    (2016)
  • M.L. Farquhar et al.

    Mechanisms of arsenic uptake from aqueous solution by interaction with goethite, lepidocrocite, mackinawite, and pyrite: An X-ray absorption spectroscopy study

    Environ. Sci. Technol.

    (2002)
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