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The Role of Soil Indigenous Microbes and Their Interactions with Maize Plants in Arsenic Uptake, Translocation, Speciation and Detoxification in the Soil-Plant System

Guan, Hang (2022). The Role of Soil Indigenous Microbes and Their Interactions with Maize Plants in Arsenic Uptake, Translocation, Speciation and Detoxification in the Soil-Plant System. (Thesis). Universität Bern, Bern

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Abstract

Arsenic (As) is a metalloid that is classified as a Class 1 carcinogen. Due to its high toxicity, As can cause a variety of human diseases such as anemia, leucopenia, and skin cancer. Arsenic is persistent, non-biodegradable, and bio-accumulative, and it persists in soils for extended periods of time and has negative effects on soil organisms. Since As is readily absorbed by plants, it can harm crop plants and result in a reduction in crop development and yields. Once these plants are consumed by animals or humans, As can enter the human food chain and poses a serious health risk to both animals and humans. To avoid such harmful repercussions, it is necessary to understand the uptake, translocation, speciation, and detoxification of As in the systemic soil-plant system. The overall goal of my research is to investigate the role of soil indigenous microbes to immobilize As in soils and decrease its bioavailability to plants. Specifically, there are three questions to be answered: (i) What are the effects of microbial disturbance, plant growth, and As treatments on the concentration and speciation of As in soil water and in soils? (ii) How do microbial disturbance and As treatments affect the concentration and speciation of As in maize (Zea mays L.) plants? And (iii) what effects do microbial disturbance and As treatments have on the health of maize plants? To answer these research questions, a greenhouse pot experiment was conducted to investigate the transformation of As in the soil-maize system and its influence on plant health. Three soil treatments with varying levels of soil microbial disturbance were performed in the experiment: native soil (NS, control soils), reconditioned soil (RS, sterilized soils and reconditioned with native soil microbes), and disturbed soil (DS, sterilized soil before planting). The DS and RS treatments were introduced to differentiate between biotic (microbial disturbance) and abiotic (soil sterilization) effects. The sterilization effect was the same in DS and RS, while the microbial disturbance effect was partly eliminated in the RS treatment due to the microbial reconditioning. Therefore, it is assumed that the difference between RS and DS showed the microbial disturbance effect, and the difference between NS and RS reflected the abiotic effect. The three soil treatments were intersected with three As treatments (uncontaminated soils (As0), moderate-As soils (As100, addition of 100 mg As kg−1 soil), and high-As soils (As200, addition of 200 mg As kg−1soil)). There were three replicates without maize (No-plant) and ten replicates with maize (Plant). This experiment thus comprised a total of 18 treatment groups. Arsenic concentration and speciation were analyzed in soil water, in soils, and in different maize tissues (roots, stem, leaves, and grains). Arsenic speciation was categorized into inorganic As species (inAs, i.e., arsenate (AsV) and arsenite (AsIII)) and organic As species (orgAs, including methylarsonic acid (MMAV), dimethylarsinic acid (DMAV), and trimethylarsine oxide (TMAO)). Various plant health parameters were also measured on a regular basis to examine the physiological responses of maize to microbial disturbance and As exposure, including plant height, fresh and dry biomass, BBCH-scale, leaf numbers per plant, leaf chlorophyll content, and damage scale of leaf spot. In soil water, total As (totAs) and As species followed a general concentration pattern of NS < RS ≤ DS, owing to the release of As into soil water caused by both the microbial disturbance and sterilization effects. Both effects played a greater role in the concentration of orgAs compared to that of inAs in soil water, implying that microbial disturbance may have influenced the methylation process of As, which converts inAs to organic forms. The microbial disturbance effect (difference RS-DS) is defined as the difference between RS and DS and is caused by the presence of soil indigenous microbes in RS. While the sterilization effect (difference NS-RS) is due to physicochemical changes and nutrient release after soil sterilization. For instance, the increased concentration of dissolved organic carbon (DOC) in soil water and lowered soil pH could mobilize As in soil water. Interestingly, the presence of maize plants mitigated both the microbial disturbance and sterilization effects, possibly helping soil microbes to recover from soil sterilization and favoring beneficial microbes in coping with As stress jointly (Chapter II). The concentrations of totAs and inAs in maize tissues followed the same order of NS < RS ≤ DS as in soil water. Among different maize tissues, totAs and inAs showed a concentration consequence of roots > leaves > stem > grains in uncontaminated soils, while in contaminated soils, the position of stem and leaves changed, indicating lower translocation of As into the maize leaves and grains. Moreover, the simultaneous presence of microbial disturbance and sterilization effects could exaggerate the adverse effects of As on plant health. Without added As (As0), both effects had no effect on dry biomass, which is one of the most critical indicators of plant growth and health. In the presence of As, however, the loss in dry biomass was more pronounced in maize grown in sterilized soils (RS and DS) than in unsterilized soils (NS) due to the sterilization effect. Furthermore, inAs and MMAV were revealed to be the species responsible for the loss in dry biomass, probably due to the high abundance and toxicity of inAs and the efficient translocation of MMA in maize (Chapter III). As with dry biomass, plant height and BBCH-scale were not affected by both the microbial disturbance and sterilization effects in maize grown on uncontaminated soils, implying that plants are capable to buffer both effects. In contrast, the effects of microbial disturbance on contaminated soils resulted in a reduction in plant height, leaf numbers, and chlorophyll content as well as an increase in the damage scale of leaf spot. Even at a high As concentration in soils, these affected health parameters were not or only slightly retarded in maize in NS indicating the resilience of an undisturbed soil-microbe-plant system. The sterilization effect caused phosphorus (P) and manganese (Mn) deficiencies in maize grown on high-As soils, which hampered plant growth and may have indirectly led to increased As accumulation in maize plants (Chapter IV). Overall, this research highlights the importance of soil indigenous microbes and their potential interaction with plants in their common resistance to the detrimental effects of As, which may improve the knowledge of As uptake, translocation, speciation, and detoxification in the soil-maize system and reduce As inputs into the food chain. This could also help to ensure food safety, food security, and sustainable food production as well as the protection of animal and human health. Further studies on soil microbial diversity, communities, and functioning (e.g., enzyme activity) as well as plant microbial communities, would be beneficial to learn more about As effects on soil health and plant health.

Item Type: Thesis
Dissertation Type: Cumulative
Date of Defense: 25 August 2022
Subjects: 500 Science > 550 Earth sciences & geology
500 Science > 580 Plants (Botany)
Institute / Center: 08 Faculty of Science > Institute of Geography
Depositing User: Hammer Igor
Date Deposited: 03 Oct 2022 15:13
Last Modified: 25 Aug 2023 22:25
URI: https://boristheses.unibe.ch/id/eprint/3840

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