A Novel Selenite-Reducing Bacterium Bacillus pseudomycoides SA14 Isolated from Se-Enriched Soil and Its Potential Se Biofortification on Brassica chinensis L.

Abstract

Microbial participation in biofortification can improve the availability of selenium (Se) in soil and contribute to the enrichment of Se in crops. In this study, a selenite (Se(IV)) reducing strain was isolated from Se-rich soil, and its Se transformation and bio-enhancement ability were studied. The strain was identified as Bacillus pseudomycoides and could reduce more than 93.48% of 1.0 mM Se(IV) in 54 h. The results of scanning electron microscope (SEM) and energy dispersive X-ray spectrometry (EDS) showed that Se(IV) was reduced to Se(0), and Se nanoparticles (SeNPs) were eventually formed. In pot experiments, B. pseudomycoides SA14 could promote the bioavailable Se in soils and the concentration of Se in Brassica chinensis L.. The concentrations of water-soluble Se, ion exchange Se and carbonate-binding Se in soil were increased by 23.13%, 22.05% and 30.89%, respectively. The Se concentration of Brassica chinensis L. in pot experiments was increased by 145.05%. The relative abundance of Bacillus in soil increased from 0.97% to 2.08% in the pot experiments. As far as we know, this is the first report of Se reduction by B. pseudomycoides. This study might provide a prospective strategy for microbial fortification of Se in crops.

Keywords

Se(IV) reduction / Bacillus pseudomycoides / bioavailability / biofortification / dominant community / natural environment

References

[1] Araújo do NascimentoC W, Viera da SilvaF B, de Brito Fabricio NetaA, et al.. Geopedology-Climate Interactions Govern the Spatial Distribution of Selenium in Soils: A Case Study in Northeastern Brazil. Geoderma, 2021, 399115119

[2] BaoP, SuJ Q, HuZ Y, et al.. Genome Sequence of the Anaerobic Bacterium Bacillus Sp. Strain ZYK, a Selenite and Nitrate Reducer from Paddy Soil. Standards in Genomic Sciences, 2014, 9(3): 646-654

[3] ChauhanR, AwasthiS, SrivastavaS, et al.. Understanding Selenium Metabolism in Plants and Its Role as a Beneficial Element. Critical Reviews in Environmental Science and Technology, 2019, 49(21): 1937-1958

[4] ChenY H, LiS S, LiuN, et al.. Effects of Different Types of Microbial Inoculants on Available Nitrogen and Phosphorus, Soil Microbial Community, and Wheat Growth in High-P Soil. Environmental Science and Pollution Research International, 2021, 28(18): 23036-23047

[5] ChilimbaA D C, YoungS D, BlackC R, et al.. Agronomic Biofortification of Maize with Selenium (Se) in Malawi. Field Crops Research, 2012, 125: 118-128

[6] D’AmatoR, RegniL, FalcinelliB, et al.. Current Knowledge on Selenium Biofortification to Improve the Nutraceutical Profile of Food: A Comprehensive Review. Journal of Agricultural and Food Chemistry, 2020, 68(14): 4075-4097

[7] DengL, WangT, LuoW, et al.. Effects of a Compound Microbial Agent and Plants on Soil Properties, Enzyme Activities, and Bacterial Composition of Pisha Sandstone. Environmental Science and Pollution Research International, 2021, 28(38): 53353-53364

[8] DinhQ T, WangM K, TranT A T, et al.. Bioavailability of Selenium in Soil-Plant System and a Regulatory Approach. Critical Reviews in Environmental Science and Technology, 2019, 49(6): 443-517

[9] DobiasJ, SuvorovaE I, Bernier-LatmaniR. Role of Proteins in Controlling Selenium Nanoparticle Size. Nanotechnology, 2011, 2219195605

[10] Domínguez-CastilloC, Alatorre-CruzJ M, Castañeda-AntonioD, et al.. Potential Seed Germination-Enhancing Plant Growth-Promoting Rhizobacteria for Restoration of Pinus Chiapensis Ecosystems. Journal of Forestry Research, 2021, 32(5): 2143-2153

[11] El-RamadyH, AbdallaN, AlshaalT, et al.. Selenium in Soils under Climate Change, Implication for Human Health. Environmental Chemistry Letters, 2015, 13(1): 1-19

[12] ErturkY, ErcisliS, HaznedarA, et al.. Effects of Plant Growth Promoting Rhizobacteria (PGPR) on Rooting and Root Growth of Kiwifruit (Actinidia Deliciosa) Stem Cuttings. Biological Research, 2010, 43(1): 91-98

[13] GolubkinaN A, FolmanisG E, TananaevI G. Comparative Evaluation of Selenium Accumulation by Allium Species after Foliar Application of Selenium Nanoparticles, Sodium Selenite and Sodium Selenate. Doklady Biological Sciences, 2012, 444: 176-179

[14] HapuarachchiS, SwearingenJ, ChasteenT G. Determination of Elemental and Precipitated Selenium Production by a Facultative Anaerobe Grown under Sequential Anaerobic/Aerobic Conditions. Process Biochemistry, 2004, 39(11): 1607-1613

[15] HockinS L, GaddG M. Linked Redox Precipitation of Sulfur and Selenium under Anaerobic Conditions by Sulfate-Reducing Bacterial Biofilms. Applied and Environmental Microbiology, 2003, 69(12): 7063-7072

[16] HuangC L, WangH L, ShiX Y, et al.. Two New Selenite Reducing Bacterial Isolates from Paddy Soil and the Potential Se Biofortification of Paddy Rice. Ecotoxicology, 2021, 30(7): 1465-1475

[17] HuangY P, WangQ Q, ZhangW J, et al.. Stoichiometric Imbalance of Soil Carbon and Nutrients Drives Microbial Community Structure under Long-Term Fertilization. Applied Soil Ecology, 2021, 168104119

[18] HuberR, SacherM, VollmannA, et al.. Respiration of Arsenate and Selenate by Hyperthermophilic Archaea. Systematic and Applied Microbiology, 2000, 23(3): 305-314

[19] HunterW J, KuykendallL D. Reduction of Selenite to Elemental Red Selenium by Rhizobium Sp. Strain B1. Current Microbiology, 2007, 55(4): 344-349

[20] IkeM, TakahashiK, FujitaT, et al.. Selenate Reduction by Bacteria Isolated from Aquatic Environment Free from Selenium Contamination. Water Research, 2000, 34(11): 3019-3025

[21] JiangD W, LiP, JiangZ, et al.. Chemolithoautotrophic Arsenite Oxidation by a Thermophilic Anoxybacillus Flavithermus Strain TCC9-4 from a Hot Spring in Tengchong of Yunnan, China. Frontiers in Microbiology, 2015, 6360

[22] Kamei-IshikawaN, TagamiK, UchidaS. Sorption Kinetics of Selenium on Humic Acid. Journal of Radioanalytical and Nuclear Chemistry, 2007, 274(3): 555-561

[23] KashiwaM, IkeM, MiharaH, et al.. Removal of Soluble Selenium by a Selenate-Reducing Bacterium Bacillus Sp. SF-1. BioFactors, 2001, 14(1/2/3/4): 261-265

[24] KulikovaN A, PerminovaI V. Interactions between Humic Substances and Microorganisms and Their Implications for Nature-Like Bioremediation Technologies. Molecules, 2021, 2692706

[25] KurodaM, NotaguchiE, SatoA, et al.. Characterization of Pseudomonas Stutzeri NT-I Capable of Removing Soluble Selenium from the Aqueous Phase under Aerobic Conditions. Journal of Bioscience and Bioengineering, 2011, 112(3): 259-264

[26] LiJ H, YangW P, GuoA N, et al.. Combined Foliar and Soil Selenium Fertilizer Increased the Grain Yield, Quality, Total Se, and Organic Se Content in Naked Oats. Journal of Cereal Science, 2021, 100103265

[27] LiJ H, YangW P, GuoA N, et al.. Combined Foliar and Soil Selenium Fertilizer Improves Selenium Transport and the Diversity of Rhizosphere Bacterial Community in Oats. Environmental Science and Pollution Research International, 2021, 28(45): 64407-64418

[28] LiS H, XiaoT F, ZhengB S. Medical Geology of Arsenic, Selenium and Thallium in China. Science of the Total Environment, 2012, 421: 31-40

[29] LiZ, KawamuraY, ShidaO, et al.. Bacillus Okuhidensis Sp. Nov., Isolated from the Okuhida Spa Area of Japan. International Journal of Systematic and Evolutionary Microbiology, 2002, 52(pt4): 1205-1209

[30] LiZ, LiangD L, PengQ, et al.. Interaction between Selenium and Soil Organic Matter and Its Impact on Soil Selenium Bioavailability: A Review. Geoderma, 2017, 295: 69-79

[31] LloydJ R. Microbial Reduction of Metals and Radionuclides. FEMS Microbiology Reviews, 2003, 27(2/3): 411-425

[32] LosiM E, FrankenbergerW T. Reduction of Selenium Oxyanions by Enterobacter Cloacae SLD1a-1: Isolation and Growth of the Bacterium and Its Expulsion of Selenium Particles. Applied and Environmental Microbiology, 1997, 63(8): 3079-3084

[33] MuleyaM, YoungS D, ReinaS V, et al.. Selenium Speciation and Bioaccessibility in Se-Fertilised Crops of Dietary Importance in Malawi. Journal of Food Composition and Analysis, 2021, 98103841

[34] NielsenP, FritzeD, PriestF G. Phenetic Diversity of Alkaliphilic Bacillus Strains: Proposal for Nine New Species. Microbiology, 1995, 141(7): 1745-1761

[35] PainterE P. The Chemistry and Toxicity of Selenium Compounds, with Special Reference to the Selenium Problem. Chemical Reviews, 1941, 28(2): 179-213

[36] PettineM, GennariF, CampanellaL, et al.. The Reduction of Selenium(IV) by Hydrogen Sulfide in Aqueous Solutions. Geochimica et Cosmochimica Acta, 2012, 83: 37-47

[37] RolewiczM, RusekP, BorowikK. Obtaining of Granular Fertilizers Based on Ashes from Combustion of Waste Residues and Ground Bones Using Phosphorous Solubilization by Bacteria Bacillus Megaterium. Journal of Environmental Management, 2018, 216: 128-132

[38] RyuJ H, JungJ H, ParkK Y, et al.. Humic Acid Removal and Microbial Community Function in Membrane Bioreactor. Journal of Hazardous Materials, 2021, 417126088

[39] SharmaV K, McDonaldT J, SohnM, et al.. Biogeochemistry of Selenium. a Review. Environmental Chemistry Letters, 2015, 13(1): 49-58

[40] SongD G, LiX X, ChengY Z, et al.. Aerobic Biogenesis of Selenium Nanoparticles by Enterobacter Cloacae Z0206 as a Consequence of Fumarate Reductase Mediated Selenite Reduction. Scientific Reports, 2017, 713239

[41] SongL, LiuH C, WangJ, et al.. Bacillus Oceani Sp. Nov., Isolated from Seawater. International Journal of Systematic and Evolutionary Microbiology, 2016, 66(2): 796-800

[42] StolzJ F, BasuP, OremlandR S. Microbial Transformation of Elements: The Case of Arsenic and Selenium. International Microbiology, 2002, 5(4): 201-207

[43] StolzJ F, BasuP, SantiniJ M, et al.. Arsenic and Selenium in Microbial Metabolism. Annual Review of Microbiology, 2006, 60: 107-130

[44] TanY Q, YaoR, WangR, et al.. Reduction of Selenite to Se(0) Nanoparticles by Filamentous Bacterium Streptomyces Sp. ES2-5 Isolated from a Selenium Mining Soil. Microbial Cell Factories, 2016, 151157

[45] Tejo PrakashN, SharmaN, PrakashR, et al.. Aerobic Microbial Manufacture of Nanoscale Selenium: Exploiting Nature’s Bio-Nanomineralization Potential. Biotechnology Letters, 2009, 31(12): 1857-1862

[46] TuranovA A, XuX M, CarlsonB A, et al.. Biosynthesis of Selenocysteine, the 21st Amino Acid in the Genetic Code, and a Novel Pathway for Cysteine Biosynthesis. Advances in Nutrition, 2011, 2(2): 122-128

[47] UllahA, SunB, WangF H, et al.. Isolation of Selenium-Resistant Bacteria and Advancement under Enrichment Conditions for Selected Probiotic Bacillus Subtilis (BSN313). Journal of Food Biochemistry, 2020, 446e13227

[48] WadgaonkarS L, NancharaiahY V, JacobC, et al.. Microbial Transformation of Se Oxyanions in Cultures of Delftia Lacustris Grown under Aerobic Conditions. Journal of Microbiology, 2019, 57(5): 362-371

[49] WangD, RensingC, ZhengS X. Microbial Reduction and Resistance to Selenium: Mechanisms, Applications and Prospects. Journal of Hazardous Materials, 2022, 421126684

[50] WangQ, YuY, LiJ X, et al.. Effects of Different Forms of Selenium Fertilizers on Se Accumulation, Distribution, and Residual Effect in Winter Wheat-Summer Maize Rotation System. Journal of Agricultural and Food Chemistry, 2017, 65(6): 1116-1123

[51] WangQ, ZhanS, HanF, et al.. The Possible Mechanism of Physiological Adaptation to the Low-Se Diet and Its Health Risk in the Traditional Endemic Areas of Keshan Diseases. Biological Trace Element Research, 2022, 200(5): 2069-2083

[52] WangS M, CuiJ T, LiX Y, ChengW. Effect of Microorganism on the Degradation and Formation of Humic Acid in Landfill Leachate. Science & Technology Vision, 2016, 7: 86-87(in Chinese with English Abstract)

[53] WangX, NingY J, ZhangP, et al.. Hair Multi-Bioelement Profile of Kashin-Beck Disease in the Endemic Regions of China. Journal of Trace Elements in Medicine and Biology, 2019, 54: 79-97

[54] WangY H, ShiX Y, HuangX X, et al.. Linking Microbial Community Composition to Farming Pattern in Selenium-Enriched Region: Potential Role of Microorganisms on Se Geochemistry. Journal of Environmental Sciences, 2022, 112: 269-279

[55] WangZ, HuangW, PangF. Selenium in Soil-Plant-Microbe: A Review. Bulletin of Environmental Contamination and Toxicology, 2022, 108(2): 167-181

[56] WeisburgW G, BarnsS M, PelletierD A, et al.. 16S Ribosomal DNA Amplification for Phylogenetic Study. Journal of Bacteriology, 1991, 173(2): 697-703

[57] WonS, HaM G, NguyenD D, et al.. Biological Selenite Removal and Recovery of Selenium Nanoparticles by Haloalkaliphilic Bacteria Isolated from the Nakdong River. Environmental Pollution, 2021, 280117001

[58] YinK, WangQ N, LvM, et al.. Microorganism Remediation Strategies towards Heavy Metals. Chemical Engineering Journal, 2019, 360: 1553-1563

[59] ZhangG L, ZhouL L, CaiD Q, et al.. Anion-Responsive Carbon Nanosystem for Controlling Selenium Fertilizer Release and Improving Selenium Utilization Efficiency in Vegetables. Carbon, 2018, 129: 711-719

[60] ZhangJ, WangY, ShaoZ Y, et al.. Two Selenium Tolerant Lysinibacillus Sp. Strains Are Capable of Reducing Selenite to Elemental Se Efficiently under Aerobic Conditions. Journal of Environmental Sciences, 2019, 77: 238-249

[61] ZhangL, LiD P, GaoP. Expulsion of Selenium/Protein Nanoparticles through Vesicle-Like Structures by Saccharomyces Cerevisiae under Microaerophilic Environment. World Journal of Microbiology & Biotechnology, 2012, 28(12): 3381-3386

[62] ZhangX M, GuoJ H, VogtR D, et al.. Soil Acidification as an Additional Driver to Organic Carbon Accumulation in Major Chinese Croplands. Geoderma, 2020, 366114234

[63] ZhangX, WangT, LiS E, et al.. A Spatial Ecology Study of Keshan Disease and Hair Selenium. Biological Trace Element Research, 2019, 189(2): 370-378

[64] ZhaoB, XingC, ZhouS B, et al.. Sources, Fraction Distribution and Health Risk Assessment of Selenium (Se) in Dashan Village, a Se-Rich Area in Anhui Province, China. Bulletin of Environmental Contamination and Toxicology, 2020, 104(4): 545-550

[65] ZhengS X, SuJ, WangL, et al.. Selenite Reduction by the Obligate Aerobic Bacterium Comamonas Testosteroni S44 Isolated from a Metal-Contaminated Soil. BMC Microbiology, 2014, 14204

[66] ZhongX L, GanY Q, DengY M. Distribution, Origin and Speciation of Soil Selenium in the Black Soil Region of Northeast China. Environmental Geochemistry and Health, 2021, 43(3): 1257-1271

[67] ZhouF, LiY N, MaY Z, et al.. Selenium Bioaccessibility in Native Seleniferous Soil and Associated Plants: Comparison between in Vitro Assays and Chemical Extraction Methods. Science of the Total Environment, 2021, 762143119

RIGHTS & PERMISSIONS

China University of Geosciences (Wuhan) and Springer-Verlag GmbH Germany, Part of Springer Nature