Water Management Impacts on Arsenic Speciation and Iron-Reducing

Relative proportions of Archaea and iron-reducing bacteria (FeRB) were .... Arsenic species concentrations in rhizosphere soil, pore-water, root-plaqu...
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Water Management Impacts on Arsenic Speciation and Iron-Reducing Bacteria in Contrasting Rice-Rhizosphere Compartments Anil C. Somenahally,†,* Emily B. Hollister,† Wengui Yan,‡ Terry J. Gentry,† and Richard H. Loeppert† † ‡

Department of Soil and Crop Sciences, Texas A&M University, College Station, Texas, 77843-2474, United States USDA-ARS, Dale Bumpers National Rice Research Center, Stuttgart, Arkansas 72160, United States

bS Supporting Information ABSTRACT: Rice cultivated on arsenic (As) contaminated-soils will accumulate variable grain-As concentrations, as impacted by varietal differences, soil variables, and crop management. A field-scale experiment was conducted to study the impact of intermittent and continuous flooding on As speciation and microbial populations in rice rhizosphere compartments of soils that were either historically amended with As pesticide or unamended with As. Rhizosphere-soil, root-plaque, pore-water and grain As were quantified and speciated, and microbial populations in rhizosphere soil and root-plaque were characterized. Total-As concentrations in rhizosphere and grain were significantly lower in intermittently flooded compared to the continuously flooded plots (86% lower in pore-water, 55% lower in rootplaque and 41% lower in grain samples). iAsV, iAsIII, and DMAsV were the predominant As species detected in rhizosphere-soil and root-plaque, porewater and grain samples, respectively. Relative proportions of Archaea and iron-reducing bacteria (FeRB) were higher in rhizosphere soil compared to root-plaque. In rhizosphere soil, the relative abundance of FeRB was lower in intermittently flooded compared to continuously flooded plots, but there were no differences between root-plaque samples. This study has demonstrated that reductions in dissolved As concentrations in the rhizosphere and subsequent decreases in grain-As concentration can be attained through water management.

’ INTRODUCTION Arsenic (As) is a toxic metalloid known to cause cancer in humans. More than 50 million people worldwide ingest higher levels of As from drinking water, than the recommended World Health Organization maximum allowable level (20 μg day 1).1 Another potential dietary source of As is rice,2 which is extensively cultivated on As-impacted soils throughout the world.3 Several Ascontaining defoliants and pesticides have been extensively used in cotton production in south-central U.S., which has resulted in widespread As-contamination of many soils in the region.4 Rice is currently grown on many of these soils, and moderate to high residual soil-As concentrations can result in high As concentrations in rice originating from this region.5 High grain-As concentrations can be exacerbated by the practice of continuous flooding on As-contaminated soils, compared to a more aerobic rice cultivation as reported in recent pot-scale studies.6,7 However, few studies have evaluated alternative water management strategies to reduce grain-As concentration at the field scale. Rice roots can absorb inorganic [arsenite (iAsIII) and arsenate (iAsV)] and organic [monomethylarsonous acid (MMAsIII), monomethylarsonic acid (MMAsV), dimethylarsinous acid (DMAsIII) and dimethylarsinic acid (DMAsV)] species of As.8 Studies have documented that more oxic conditions (e.g., intermittent vs continuous flooding) can alter the speciation of inorganic As in soil.6,7 Howr 2011 American Chemical Society

ever, little is known about the impact of intermittent flooding on the concentration of soil organic-As species, such as DMAsV which has been detected at much higher concentrations than inorganic As in rice grains originating from south-central U.S.9 Under continuous flooding, the bulk soil becomes anaerobic over the growing season; however, the surfaces of physiologically active rice roots stay relatively oxic because of radial oxygen diffusion from the root-aerenchyma structure.10 Dissolved Fe2+ that is transported by diffusion from the anaerobic bulk soil can be oxidized to Fe3+, and subsequently precipitated as iron oxide as it encounters the more highly oxidized root surface. The rice rhizosphere can, thus, be compartmentalized into two distinct zones, that is, (i) the zone of iron-oxide precipitation and plaque development directly at the root surface and (ii) the adjacent rhizosphere soil that is impacted by both more highly oxic plant root and the more highly reduced bulk soil. Each zone has unique biogeochemical properties. Numerous studies have recognized that the root plaque comprises a unique environment that can adsorb significant amounts of As, impacting the amount of As taken up by rice plants.11 13 Received: April 12, 2011 Accepted: August 26, 2011 Revised: June 6, 2011 Published: August 26, 2011 8328

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Environmental Science & Technology However, not much is known about the speciation of As in the rootplaque under different water management practices or the microbial populations inhabiting rice-root plaque. Localized conditions in the rhizosphere compartments can impact the various microbial groups and thus the microbially facilitated processes including As-reduction, -oxidation, -methylation, and demethylation that impact As speciation.14 Iron-reducing bacteria can increase dissimilatory iron-oxide reduction and result in the release of associated As.15 However, the specific impacts of different water-management practices on As speciation and microbial communities, including iron-reducing bacteria in different rhizosphere compartments, are not fully understood. The objective of this study was to compare the impacts of continuous vs intermittent flooding on the speciation of As and the relative abundances of various microbial groups in contrasting rice-rhizosphere compartments.

’ MATERIAL AND METHODS Experimental Site and Treatments. Field experiments were conducted in research plots at the U.S. Department of Agriculture, Agriculture Research Service, Dale Bumpers National Rice Research Center, Stuttgart, AR, in 2008. One of the experimental plots has been continuously amended with monosodium methane-arsonate (MSMA) in alternate years for more than 20 years,16 where it has been used to screen rice cultivars for MSMA tolerance. In 2008, MSMA was applied to the surface soil immediately before planting, at the rate of 6.7 kg ha 1yr 1 (equivalent to 3.1 kg As ha 1yr 1). The adjacent unamended soil had not received any As-containing products for at least the last 20 years. The water treatments that were superimposed on the unamended- and MSMA-soil treatments, included intermittent and continuous flooding. Under intermittent flooding the plots were initially flooded, then allowed to dry until small, surface cracks were evident, at which point the plots were reflooded. For the continuous-flood treatment, water was consistently maintained at approximately 10 cm depth during the entire season until one week before harvest. The treatment groups used in this study were (1) MSMA-continuous flood (M-CF), (2) MSMAintermittent flood (M-IF), (3) unamended-continuous flood (U-CF), and (4) unamended-intermittent flood (U-IF). The treatment plots were arranged using a split-plot design with soilAs as the main plot and water treatment as the subplot. Subplot replicates were arranged in a completely randomized design within each main plot. Each treatment was replicated three times. The cultivar used in our study was ‘Cocodrie’, a commonly grown cultivar in Arkansas that is susceptible to As toxicity.16 All other management practices for weeds, fertilization, etc. were followed as previously described.16 The chemical characterization of the soil samples from the experimental plots is presented in Table S1 and S2 of the Supporting Information. Sampling. Approximately three months after the first flood and three weeks before the rice was harvested (120 days after planting), the rhizosphere soil, pore-water, root-plaque, and grain samples were collected. To minimize the effects of soil water content on rhizosphere soil and pore-water sampling between the two water treatments, samples were obtained when the rhizosphere of both water treatments were completely saturated. Additional details on rhizosphere soil and root-plaque sampling details are provided in the Supporting Information. The root-plaque and rhizosphere-soil samples were each split into subsamples for subsequent chemical and microbial analyses. Samples for chemical analysis were transported on ice from the

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field and were subsequently processed in the lab. Samples for microbial analysis were frozen over dry ice in the field and were subsequently stored at 80 °C. Rhizosphere soil samples were airdried in the lab, ground to 7.25 Root-plaque can act as a barrier and reduce the bioavailability of several As species to plants, as suggested by previous studies;11,12 however, whether root-plaque is a sink or a source of As for plants might depend on other localized soil conditions, for example, localized microbial activity that impacts the dissolution/precipitation of iron oxide and speciation of As.26 Lower grain-As concentrations in IF compared to that with the CF treatments in the current field study is attributable mainly to lower dissolved As concentrations in the rhizosphere and is comparable to the results of previous pot-scale experiments.6,7 The total grain As, iAsIII and DMAsV concentrations from unamended soils were similar to concentrations reported by Pillai et al.;27 however the concentrations from MSMA-amended plots were considerably higher than the concentrations from unamended soils and several market-basket surveys.5,28 The results of the current study indicate that the high grain-DMAsV concentrations in rice plants from MSMA-amended plots could be attributable to the direct absorption of DMAsV from the rhizosphere pore water and subsequent translocation to the grain. Several studies have reported that DMAsV is readily taken up by rice plants,29 and that rice roots can absorb DMAsV through the aquaporin channel.8 However, it is not clear why rice grain from the M-IF plots accumulated considerably higher DMAsV concentrations than that from the U-CF plots that had much higher pore water AsIII and DMAsV concentrations. The results of the current study imply that soil-As speciation, specifically the occurrence of methyl-As species in the rhizosphere soil and root plaque, had a greater impact than water management on grain-DMAsV concentration. These results indicate a possibility that the high proportion of DMAsV frequently observed in rice grains produced in south-central U.S. 5,30 could also be at least partially due to trace residual methyl As from decades of application of MSMA as a cotton defoliant. However, the DMAsV concentration range observed in grain from the unamended plots indicate that other factors such as microbial methylation could contribute to organicAs accumulation. Further studies are needed to investigate the complex roles of soil variability, water management, As concentration and speciation, microbial interaction, and plant genetics in impacting grain-As concentration and speciation. As Biogeochemistry and Microbial Communities. The relative abundance of microbial groups varied noticeably between

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the rhizosphere compartments, that is, rhizosphere soil vs rootplaque Previous studies have reported that rhizosphere and nonrhizosphere communities varied greatly,31 33 but none of the studies looked at the differences between rice-rhizosphere compartments. The higher relative abundance of Archaea and FeRB in rhizosphere soil compared to the root-plaque is likely due to the relatively more highly reduced conditions in the former compared to the surface of an actively metabolizing root. This trend is in contrast to a previous study that reported much higher FeRB activity on the surface of roots than in the rhizosphere soil of several submerged macrophytes.31 However, the occurrence of FeRB and SRB on root-plaque suggests that localized anaerobic microsites that are conducive to the growth of anaerobic heterotrophs likely occur on the root surface.34,35 The higher concentration of dissolved As in the rhizosphere soil of the CF plots correspond with the greater relative abundances of FeRB in these plots. Dissimilatory reduction of FeIII oxyhydroxides, as a result of FeRB activity,36 would result in the dissolution of iron oxide and the subsequent release of surfacebound As.15 This phenomenon is likely a significant factor that contributes to the relatively high pore-water As concentrations observed in CF plots. FeRB prefer poorly crystalline iron-oxide phases such as ferrihydrite, that are predominant in the rootplaque over well crystalline phases such as goethite,37 which suggests that dissimilatory Fe(III) reduction and subsequent release of associated As could also be occurring on root-plaque, given appropriate localized redox conditions. FeRB are commonly found in rice paddies,38,39 and studies have detected dissimilatory iron reduction on the rice-root surface.26,35 This study is the first report illustrating correlations between the population dynamics of key microbial groups and the abundance of various As species in multiple rhizosphere compartments under different water management practices used in rice cultivation. The results of the current study demonstrate that microbial populations differ significantly between the rhizosphere-soil and root-plaque compartments. Water management had a much greater impact on rhizosphere soil microbial communities, especially populations of Archaea and FeRB, than on that of the root plaque that is strongly impacted by radial O2 diffusion from the rice root. The effect of water management is reflected in pore-water As concentrations that are impacted primarily by the microbially induced reduction of FeIII. Microbial processes would also strongly impact the bioavailability of As through the reduction iAsV and methyl AsV species to more soluble and mobile AsIII species. These results also support previous observations that water management that results in a more highly oxidized rooting zone are viable management options to reduce soluble As concentrations in the rhizosphere and also reduce rice-grain As concentrations.

’ ASSOCIATED CONTENT

bS

Supporting Information. Details on rhizosphere-soil and root-plaque sampling, As species extraction, 16S rRNA sequence analysis, chemical characterization of experimental plot soil, instrumentation details, as well as neighbor-joining phylogenetic trees for most abundant OTUs representing Anaeromyxobacter and Geobacteraceae populations in rhizosphere-soil and rootplaque samples. This material is available free of charge via the Internet at http://pubs.acs.org.

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’ AUTHOR INFORMATION Corresponding Author

*Phone: 1-979-845-5322; fax: 1-979-845-0456; e-mail: [email protected].

’ ACKNOWLEDGMENT We thank the research team of the germplasm lab at USDAARS, Dale Bumpers National Rice Research Center, Stuttgart, Arkansas for their help with the field experiment. We also thank Dr. Dennis James in the Department of Chemistry, Texas A&M University for his help with the HPLC-ICP-MS analyses. ’ REFERENCES (1) Duxbury, J. M.; Mayer, A. B.; Lauren, J. G.; Hassan, N. Food chain aspects of arsenic contamination in Bangladesh: Effects on quality and productivity of rice. J. Environ. Sci. Health, Part A: Environ. Sci. Eng. 2003, 38 (1), 61–69. (2) Mondal, D.; Polya, D. A. Rice is a major exposure route for arsenic in Chakdaha block, Nadia district, West Bengal, India: A probabilistic risk assessment. App. Geochem. 2008, 23 (11), 2987–2998. (3) Meharg, A. A.; Rahman, M. Arsenic contamination of Bangladesh paddy field soils: implications for rice contribution to arsenic consumption. Environ. Sci. Technol. 2003, 37 (2), 229–234. (4) Woolson, E. A. Fate of arsenicals in different environmental substrates. Environ. Health Perspect. 1977, 19, 73–81. (5) Williams, P. N.; Raab, A.; Feldmann, J.; Meharg, A. A. Market basket survey shows elevated levels of as in South Central U.S. processed rice compared to California: consequences for human dietary exposure. Environ. Sci. Technol. 2007, 41 (7), 2178–2183. (6) Li, R. Y.; Stroud, J. L.; Ma, J. F.; McGrath, S. P.; Zhao, F. J. Mitigation of arsenic accumulation in rice with water management and silicon fertilization. Environ. Sci. Technol. 2009, 43 (10), 3778–3783. (7) Xu, X. Y.; McGrath, S. P.; Meharg, A. A.; Zhao, F. J. Growing rice aerobically markedly decreases arsenic accumulation. Environ. Sci. Technol. 2008, 42 (15), 5574–5579. (8) Li, R. Y.; Ago, Y.; Liu, W. J.; Mitani, N.; Feldmann, J.; McGrath, S. P.; Ma, J. F.; Zhao, F. J. The rice aquaporin Lsi1 mediates uptake of methylated arsenic species. Plant Physiol. 2009, 150 (4), 2071–2080. (9) Meharg, A. A.; Williams, P. N.; Adomako, E.; Lawgali, Y. Y.; Deacon, C.; Villada, A.; Cambell, R. C. J.; Sun, G.; Zhu, Y. G.; Feldmann, J.; Raab, A.; Zhao, F. J.; Islam, R.; Hossain, S.; Yanai, J. Geographical variation in total and inorganic arsenic content of polished (white) rice. Environ. Sci. Technol. 2009, 43 (5), 1612–1617. (10) Colmer, T. D. Long-distance transport of gases in plants: A perspective on internal aeration and radial oxygen loss from roots. Plant, Cell Environ. 2003, 26 (1), 17–36. (11) Hossain, M. B.; Jahiruddin, M.; Loeppert, R. H.; Panaullah, G. M.; Islam, M. R.; Duxbury, J. M. The effects of iron plaque and phosphorus on yield and arsenic accumulation in rice. Plant Soil 2009, 317 (1 2), 167–176. (12) Liu, W. J.; Zhu, Y. G.; Smith, F. A.; Smith, S. E. Do phosphorus nutrition and iron plaque alter arsenate (As) uptake by rice seedlings in hydroponic culture? New Phytol. 2004, 162 (2), 481–488. (13) Seyfferth, A. L.; Webb, S. M.; Andrews, J. C.; Fendorf, S. Arsenic localization, speciation, and co-occurrence with iron on rice (Oryza sativa) roots having variable Fe coatings. Environ. Sci. Technol. 2010, 44 (21), 8108–8113. (14) Oremland, R. S.; Stolz, J. F. The ecology of arsenic. Science 2003, 300 (5621), 939–944. (15) Cummings, D. E.; Caccavo, F.; Fendorf, S.; Rosenzweig, R. F. Arsenic mobilization by the dissimilatory Fe(III)-reducing bacterium Shewanella alga BrY. Environ. Sci. Technol. 1999, 33 (5), 723–729. (16) Yan, W. G.; Dilday, R. H.; Tai, T. H.; Gibbons, J. W.; McNew, R. W.; Rutger, J. N. Differential response of rice germplasm to straighthead induced by arsenic. Crop Sci. 2005, 45 (4), 1223–1228.

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