Bacterial Induced Plant Growth Promotion and Biotransformation of Selenium in Soils

Abstract

Selenium (Se) is an essential nutrient for both humans and livestock, but its toxicity becomes particularly evident in soils with naturally high Se concentrations. The present study aimed to investigate the diversity of bacterial communities in soils and roots of maize plants cultivated in seleniferous (SE) and non-seleniferous (NS) soils using Illumina Mi-SeqNext-Generation Sequencing. Metagenomic analysis identified Proteobacteria as the predominant phylum in both environments. The most dominant operational taxonomic unit (OTU) across both soil types belonged to the genus Bacillus. Se altered microbial community composition, increasing the abundance of the Bacillaceae family (30%) and Pseudomonadaceae family (25%) in SE soils compared to NS soils. Bacillus was the dominant genus in SE environment, indicating its tolerance to Se. The NS soil sample contained 46 distinct bacterial species, which make up 8.6% of the total detected species. The SE soil sample comprised 85 distinct bacterial species, and both soil samples exhibited substantial similarity, accounting for 75.5% of the total species. The NS root sample contained two distinct bacterial species (0.5% of the total detected species), whereas the SE root sample comprised 13 different species (3.5%). A total of 359 bacterial species were common to both samples, accounting for 96% of the detected community. Diversity indices indicated that NS soil samples had higher species richness, while SE samples exhibited a more stressed microbial structure. This study also focused on isolating bacteria from seleniferous agricultural soils (Se content: 6.86 ± 0.12 mg/kg), screening for Se tolerance, and evaluating their potential to promote plant growth and to influence Se speciation in maize tissues. Three bacterial isolates, Se3, Se38, and Se5, were selected as Se-tolerant and assessed for their effectiveness in enhancing maize growth and regulating Se uptake in seleniferous soils. These isolates exhibited high tolerance levels, withstanding up to 200 mM selenate and 150 mM selenite. These bacteria were identified as Proteus terrae (Se3), Corynebacterium glutamicum (Se38), and Halopseudomonas formosensis (Se5) based on their 16S rRNA sequence analysis. Under selenate exposure, Corynebacterium glutamicum exhibited the highest selenium accumulation compared to other isolates. In contrast, under selenite treatment, Proteus terrae demonstrated the greatest selenium biosorption capacity relative to the other two isolates. All three bacterial isolates exhibited plant growth-promoting traits, including indole acetic acid (IAA) production, phosphate solubilization, and siderophore production. Proteus terrae exhibited the highest IAA production (182.86 ± 4.55 μg/ml) compared to other bacterial isolates. Halopseudomonas formosensis showed the highest phosphate solubilization (245.07 ± 7.84 μgP/ml), followed by Proteus terrae (234.08 ± 2.15 μgP/ml) and Corynebacterium glutamicum (218.11 ± 6.27 μgP/ml). Proteus terrae produced the highest siderophore concentration (42.91 ± 0.02% siderophore units), followed by Corynebacterium glutamicum (31.32 ± 0.08%) and Halopseudomonas formosensis (29.59 ± 0.04%). Field trial in seleniferous soils showed that inoculation with Proteus terrae, Corynebacterium glutamicum, and Halopseudomonas formosensis significantly enhanced maize growth by 26.8%, 19.6%, and 21.9%, respectively, compared to the control in seleniferous soil. Plants inoculated with bacterial isolates grew healthier and had bigger maize cobs than control plants. The results demonstrated that bacterial inoculation significantly enhanced the growth and biomass production of maize plants when grown in seleniferous soil. There was an increase of 54.1%, 41.2%, 62.4% and 26.8%, 19.6%, 21.9% in the root length and shoot height of Corynebacterium glutamicum, Halopseudomonas formosensis, Proteus terrae inoculated plants. An increase of about 45.1%, 48.7%, and 54.2% in the root biomass and 49.7%, 47.2%, and 52.3% in the shoot biomass was detected in the case of Corynebacterium glutamicum, Halopseudomonas formosensis, and Proteus terrae inoculated plants compared to control plants. Bacterial inoculation also resulted in less Se uptake in maize tissues compared to control plants. The selenium accumulation in Halopseudomonas formosensis, Proteus terrae and Corynebacterium glutamicum inoculated plant roots was 69.3%, 74.9% and 72.2% lower compared to the control roots. There was 87.3%, 88.8%, and 81.3% lesser selenium accumulation in Halopseudomonas formosensis, Proteus terrae and Corynebacterium glutamicum inoculated plants respectively. In the case of seeds, there was 73.8%, 80.5% and 70.2% lesser Se content in Halopseudomonas formosensis, Proteus terrae and Corynebacterium glutamicum inoculated plants compared to the control. Selenium speciation in various maize plant tissues was analyzed using X-ray Absorption Near Edge Structure (XANES) spectroscopy. The results revealed a higher proportion of organic selenium species in the treated plants. Notably, volatile methylated compounds like dimethyl selenide (DMSe) and dimethyldiselenide (DMDSe) were more prevalent in inoculated samples. Elemental selenium (Se⁰), a biologically inert form, was detected exclusively in the roots of inoculated plants, indicating potential microbial-mediated transformation and sequestration. These results underscore the capability of native plant growth-promoting bacteria to attenuate selenium phytotoxicity through biotransformation of inorganic selenium into less harmful, volatile, or organically bound forms, thereby enhancing phytoremediation efficacy and limiting selenium translocation to edible plant tissues. This study demonstrated that Se-tolerant bacterial isolates, Proteus terrae (Se3), Halopseudomonas formosensis (Se5), and Corynebacterium glutamicum (Se38) offer a dual benefit in seleniferous soils by enhancing plant growth and mitigating selenium toxicity. These bacteria exhibit high Se tolerance, promote maize growth, and significantly reduce Se uptake in plant tissues, making them valuable biofertilizers. Moreover, their ability to bioaccumulate or biosorb selenium and convert it into elemental selenium (Se⁰) presents an environmentally friendly solution for bioremediation of Se-contaminated soils. By leveraging the synergy between selenium-tolerant plant growth-promoting bacteria and crops such as maize, it may be possible to transform selenium-affected soils into viable agricultural lands, ensuring greater food security and sustainable land management in regions where high selenium levels currently pose a challenge.