Soil redox status governs within-field spatial variation in microbial arsenic methylation and rice straighthead disease.

Microbial arsenic (As) methylation in paddy soil produces mainly dimethylarsenate (DMA), which can cause physiological straighthead disease in rice. The disease is often highly patchy in the field, but the reasons remain unknown. We investigated within-field spatial variations in straighthead disease severity, As species in rice husks and in soil porewater, microbial composition and abundance of arsM gene encoding arsenite S-adenosylmethionine methyltransferase in two paddy fields. The spatial pattern of disease severity matched those of soil redox potential, arsM gene abundance, porewater DMA concentration, and husk DMA concentration in both fields. Structural equation modelling identified soil redox potential as the key factor affecting arsM gene abundance, consequently impacting porewater DMA and husk DMA concentrations. Core amplicon variants that correlated positively with husk DMA concentration belonged mainly to the phyla of Chloroflexi, Bacillota, Acidobacteriota, Actinobacteriota, and Myxococcota. Meta-omics analyses of soil samples from the disease and non-disease patches identified 5129 arsM gene sequences, with 71% being transcribed. The arsM-carrying hosts were diverse and dominated by anaerobic bacteria. Between 96 and 115 arsM sequences were significantly more expressed in the soil samples from the disease than from the non-disease patch, which were distributed across 18 phyla, especially Acidobacteriota, Bacteroidota, Verrucomicrobiota, Chloroflexota, Pseudomonadota, and Actinomycetota. This study demonstrates that even a small variation in soil redox potential within the anoxic range can cause a large variation in the abundance of As-methylating microorganisms, thus resulting in within-field variation in rice straighthead disease. Raising soil redox potential could be an effective way to prevent straighthead disease.

Widespread Occurrence of the Highly Toxic Dimethylated Monothioarsenate (DMMTA) in Rice Globally.

Arsenic (As) accumulation in rice is of global concern for human health and international trade. Rice is typically reported to contain inorganic As (iAs) and dimethylated arsenate (DMA), with current food guidelines limiting toxic iAs but not less-toxic DMA. Here, we show that the highly toxic dimethylated monothioarsenate (DMMTA) is also found in rice worldwide and has been unknowingly determined as less-toxic DMA by previous routine analytical methods. Using enzymatic extraction followed by high-performance liquid chromatography-inductively coupled plasma-mass spectrometry (HPLC-ICP-MS) analysis with a C18 column, DMMTA was detected in rice grains (n = 103) from a field survey from China and in polished rice grains (n = 140) from a global market-basket survey. Concentration ranged from <0.20 to 34.8 µg/kg (median 10.3 µg/kg), accounting for 0 to 21% of total As. A strong linear correlation was observed in all rice samples between DMA and DMMTA (being 30 ± 8% of DMA) concentrations. This robust relationship allows an estimation of DMMTA in rice grains from the DMA data reported in previous market-basket surveys, showing a general global geographical pattern with DMMTA concentration increasing from the equator toward high-latitude regions. Based on the global occurrence and potential high toxicity, DMMTA in rice should be considered in health risk assessments and for setting food regulations.

Dynamics of Dimethylated Monothioarsenate (DMMTA) in Paddy Soils and Its Accumulation in Rice Grains.

Arsenic species transformation in paddy soils has important implications for arsenic accumulation in rice grains and its safety to the consumers. Methylated thioarsenates including highly toxic dimethylated monothioarsenate (DMMTA) have been detected in paddy soils, but their production and dynamics remain poorly understood. In the present study, we first optimized a HPLC-ICP-MS method to quantify methylated thioarsenate species. Using this method together with 10 mM diethylenetriamine pentaacetate (DTPA) to preserve As speciation, we investigated methylated thioarsenate species in porewaters of seven As-contaminated soils incubated under flooded conditions and of two paddy fields. DMMTA was the main methylated thioarsenate species in the porewaters in both incubated soils and paddy fields, with concentrations ranging from 0.2 to 36.2 µg/L and representing ca. 58% of its precursor dimethylarsenate (DMA). The temporal production and dynamics of DMMTA were linked with the DMA concentrations. When soils were drained, DMMTA was converted to DMA. In the two paddy fields, DMMTA concentrations in rice grains were 0.4-10.1 µg/kg. Addition of sulfur fertilizer and rice straw incorporation increased grain DMMTA by 9-28%. These results suggest that DMMTA is an important As species in paddy soils and can accumulate in rice grains, presenting a risk to food safety and human health.

How Could Agronomic Biofortification of Rice Be an Alternative Strategy with Higher Cost-Effectiveness for Human Iron and Zinc Deficiency in China?

BACKGROUND: Iron and zinc deficiencies affect human health globally, especially in developing countries. Agronomic biofortification, as a strategy for alleviating these issues, has been focused on small-scale field studies, and not widely applied while lacking of cost-effectiveness analysis (CEA). OBJECTIVE: We conducted the CEA of agronomic biofortification, expressed as USD per disability-adjusted life years (DALYs) saved, to recommend a cost-effectiveness strategy that can be widely applied. METHODS: The DALYs were applied to quantify the health burden due to Fe and/or Zn deficiency and health cost of agronomic biofortification via a single, dual, or triple foliar spray of Fe, Zn, and/or pesticide in 4 (northeast, central China, southeast, and southwest) major Chinese rice-based regions. RESULTS: The current health burden by Fe or Zn malnutrition was 0.45 to 1.45 or 0.14 to 0.84 million DALYs for these 4 regions. Compared to traditional rice diets, the daily Fe and/or Zn intake from Fe and/or Zn-biofortified rice increased, and the health burden of Fe and/or Zn deficiency decreased by 28% and 48%, respectively. The cost of saving 1 DALYs ranged from US$376 to US$4989, US$194 to US$2730, and US$37.6 to US$530.1 for the single, dual, and triple foliar Fe, Zn, and/or pesticide application, respectively, due to a substantial decrease in labor costs by the latter 2 applications. CONCLUSIONS: Agronomic biofortification of rice with the triple foliar spray of Fe, Zn, and pesticide is a rapidly effective and cost-effectiveness pathway to alleviate Fe and Zn deficiency for rice-based dietary populations.