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Niche Differentiation of Arsenic-Transforming Microbial Groups in the Rice Rhizosphere Compartments as Impacted by Water Management and Soil-Arsenic Concentrations.

ABSTRACT: Arsenic (As) bioavailability in the rice rhizosphere is influenced by many microbial interactions, particularly by metal-transforming functional groups at the root-soil interface. This study was conducted to examine As-transforming microbes and As-speciation in the rice rhizosphere compartments, in response to two different water management practices (continuous and intermittently flooded), established on fields with high to low soil-As concentration. Microbial functional gene composition in the rhizosphere and root-plaque compartments were characterized using the GeoChip 4.0 microarray. Arsenic speciation and concentrations were analyzed in the rhizosphere soil, root-plaque, pore water, and grain samples. Results confirmed several As-biotransformation processes in the rice rhizosphere compartments, and distinct assemblage of As-reducing and methylating bacteria was observed between the root-plaque and rhizosphere. Results confirmed higher potential for microbial As-reduction and As-methylation in continuously flooded, long term As-contaminated fields, which accumulated highest concentrations of As^III and methyl-As concentrations in pore water and rice grains. Water management treatment significantly altered As-speciation in the rhizosphere, and intermittent flooding reduced methyl-As and As^III concentrations in the pore water, root-plaque and rice grain. Ordination and taxonomic analysis of detected gene-probes indicated that root-plaque and rhizosphere assembled significantly different microbial functional groups demonstrating niche separation. Taxonomic non-redundancy was evident, suggesting that As-reduction, -oxidation and -methylation processes were performed by different microbial functional groups. It was also evident that As transformation was coupled to different biogeochemical cycling processes (nutrient assimilation, carbon metabolism etc.) in the compartments and between treatments, revealing functional non-redundancy of rice-rhizosphere microbiome in response to local biogeochemical conditions and As contamination. This study provided novel insights on As-biotransformation processes and their implications on As-chemistry at the root-soil interface and their responses to water management, which could be applied for mitigating As-bioavailability and accumulation in rice grains.

SUBMITTER: Somenahally AC

PROVIDER: S-EPMC8602891 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Background:In parts of Cambodia, irrigation with groundwater results in arsenic accumulation in soils and rice, leading to health concerns associated with rice consumption. A high concentration of iron in groundwater can precipitate arsenic and reduce its bioavailability, however high concentrations of arsenic and iron can also reduce rice production. Furthermore, concerns have been raised about chemical contamination from inorganic fertilizers used to grow rice. The relationship between soil geochemistry and arsenic concentrations in rice is not yet fully understood. Objectives:The primary objective of this project was to investigate the relationship between arsenic concentrations in irrigation water, soil and rice collected from different sites in Cambodia. A secondary objective was to explore arsenic and phosphorus levels in fertilizer samples obtained from the study area in Cambodia. Methods:The present study collected 61 well water samples, 105 rice samples, 70 soil samples, 11 inorganic fertilizer samples and conducted interviews with 44 families along the Mekong River in Cambodia. Analyses for metals, total arsenic, and arsenic species in the water and rice were conducted in Canada by inductively coupled plasma mass spectrometry. Analyses for metals, total arsenic and phosphorus in soils and inorganic fertilizers were conducted in Cambodia and Singapore by X-ray fluorescence. Results:The concentration of arsenic in rice paddy soils was highly variable and as much as 20 times higher near the irrigation wells than in more distal areas of the paddy. Two farmers in Preak Russey had integrated soil samples with arsenic levels above the concentration associated with toxicity to rice in Taiwan (40 mg/kg) and above the Dutch concentration requiring intervention or remediation (55 mg/kg). The highest total arsenic measured in soil was 95 mg/kg. In Preak Russey, the loading of arsenic from irrigation water was 3710 times greater than the loading of arsenic from inorganic fertilizers. Half of the commercial inorganic fertilizers had less than 50% of the labelled content of phosphorus. Conclusions:Emphasis should be placed on improving the management of irrigation water, not on inactivation of arsenic in soil. The high levels of iron in groundwater mitigate arsenic toxicity, but the accumulation of iron could later result in lower rice productivity. Irrigation of rice with groundwater is not likely sustainable. To improve rice productivity, the content of phosphorus in local inorganic fertilizers must be improved to world standards. X-ray fluorescence analysis can quickly identify poor quality fertilizers. Informed Consent:Obtained. Competing Interests:The authors declare no competing financial interests.

Project description:BackgroundIdentification of the allelopathy-interrelated metabolites from the allelopathic rice rhizosphere is crucial to understand the allelopathic mechanism of rice, which in turn can promote its applications to farming. In this study, the metabolites from the rhizosphere soil of five different rice lines, including allelopathic rice accession PI312777 (PI) and non-allelopathic rice accession Lemont (Le) as well as their genetic derivatives (e.g., phenylalanine ammonia-lyase (PAL) gene overexpression transgenic lines of PI and Le, namely, PO and LO respectively, and PAL RNA interference line of PI, namely, PR) were identified and comparatively analyzed to explore the positive compounds that are involved in the process of rice allelopathy.ResultsThe results showed that 21 non-polar compounds and 21 polar compounds differed in content in the rhizosphere soil of PI and Le, which include several volatile fatty acids and long-chain fatty acids. The relative contents of fatty acids also differed between PAL overexpressing or RNA interference (RNAi)-silenced line and their wild-type respectively. Acetic acid content also differed among groups, i.e., it is higher in the high allelopathic potential rice. Further analysis showed that different metabolites from the ADS8 resin-extracted phase were more abundant than that those from the ADS21 resin-extracted phase, suggesting that the allelochemicals in root exudates of allelopathic rice are mainly non-polar substances. KEGG annotation of these differential metabolites revealed that these compounds were related to nutrient metabolism, secondary metabolite synthesis, signaling substance synthesis, and toxin degradation.ConclusionsRice allelochemicals deposited in the ADS8 resin-extracted phase were more abundant than those in the ADS21 resin-extracted phase. Allelochemicals in root exudates of allelopathic rice are mainly non-polar substances, and long-chain fatty acids are considered as allelopathy interrelated metabolites.

Dataset Information

Niche Differentiation of Arsenic-Transforming Microbial Groups in the Rice Rhizosphere Compartments as Impacted by Water Management and Soil-Arsenic Concentrations.

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