Phosphate-solubilizing fungi enhances the growth of Brassica chinensis L. and reduces arsenic uptake by reshaping the rhizosphere microbial community
Tóm tắt
High concentrations of arsenic in soil and plant systems are a threat to human health and ecosystems. The levels of phosphate ions in the soil strongly influence the soil efficacy and arsenic absorption by plants. This study investigated the effects of phosphate-solubilizing fungi (PSF) on environmental factors and structural changes in microbial community in soils contaminated with arsenic. Four experimental groups were created: control (CK), Penicillium GYAHH-CCT186 (W186), Aspergillus AHBB-CT196 (W196), and Penicillium GYAHH-CCT186 + Aspergillus AHBB-CT196 (W186 + W196), with Pakchoi (Brassica chinensis L.) as the test plant. Analysis of altered nutrient levels, enzyme activities and microbial community structure in the soil as well as the growth and physiological characteristics of Pakchoi, revealed a significant increase in the available phosphorus (AP), organic matter (OM), cation exchange capacity (CEC) and available arsenic (AAs) content of the soil following W186 + W196, W196 and W186 treatments. All experimental treatments enhanced the activity of soil β-glucosidase (β-GC) and soil catalase (S-CAT). W186 + W196 and W196 treatments significantly enhanced soil acid phosphatase (S-ACP) activity. Besides, W186 + W196 treatment significantly induced dehydrogenase (S-DHA) activity. Further, of the treatment with PSF increased the fresh weight, root length, plant height and chlorophyll levels while decreasing the arsenic accumulation in Pakchoi. Exposure to PSF also increased the activity of Ascomycota, Basidiomycota, Chytridiomycota, unclassified_Fungi, Mortierellomycota, Cryptomycota and Rozellomycota in the soil. The relative abundance of Ascomycota, Basidiomycota, and Mortierellomycota was positively correlated with the available nutrients (except iron) in the soil as well as enzyme activities. Consequently, the PSF improved the quality of soil and the safety of Pakchoi, suggesting that PSF can be utilized for the remediation of arsenic-contaminated soil.
Tài liệu tham khảo
Adams RI, Miletto M, Taylor JW, Bruns TD (2013) Dispersal in microbes: fungi in indoor air are dominated by outdoor air and show dispersal limitation at short distances. ISME J 7:1262–1273. https://doi.org/10.1038/ismej.2013.28
Adhikary A, Saini R, Kumar R, Singh I, Ramakrishna W, Kumar S (2022) Pseudomonas citronellolis alleviates arsenic toxicity and maintains cellular homeostasis in chickpea (Cicer arietinum L.). Plant Physiol Biochem 184:26–39. https://doi.org/10.1016/j.plaphy.2022.05.014
Alaei L, Izadi Z, Jafari S, Jahanshahi F, Jaymand M, Mohammadi P, Paray PA, Hasan A, Mojtaba F, Varnamkhasti BS, Saboury AA, Moosavi-Nejad Z, Sheikh-Hosseini M, Derakhshankhah H (2021) Irreversible thermal inactivation and conformational lock of alpha glucosidase. J Biomol Struct Dyn 39:3256–3262. https://doi.org/10.1080/07391102.2020.1762742
Aydi Ben Abdallah R, Jabnoun-Khiareddine H, Nefzi A, Mokni-Tlili S, Daami-Remadi M (2016) Biocontrol of Fusarium wilt and growth promotion of tomato plants using endophytic bacteria isolated from Solanum elaeagnifolium stems. J Phytopathol 164:811–824. https://doi.org/10.1111/jph.12501
Bartsev SI, Pochekutov AA (2016) The vertical distribution of soil organic matter predicted by a simple continuous model of soil organic matter transformations. Ecol Model 328:95–98. https://doi.org/10.1016/j.ecolmodel.2016.02.020
Beheshti M, Alikhani HA, Pourbabaee AA, Etesami H, Asadi Rahmani H, Norouzi M (2021) Periphytic biofilm and rice rhizosphere phosphate-solubilizing bacteria and fungi: A possible use for activating occluded P in periphytic biofilms in paddy fields. Rhizosphere 19:100395. https://doi.org/10.1016/j.rhisph.2021.100395
Bhalla S, Garg N (2021) Arbuscular mycorrhizae and silicon alleviate arsenic toxicity by enhancing soil nutrient availability starch degradation and productivity in Cajanus cajan (L.) Millsp. Mycorrhiza 31(6) 735–754. https://doi.org/10.1007/s00572-021-01056-z
Błońska E, Lasota J, Gruba P (2016) Effect of temperate forest tree species on soil dehydrogenase and urease activities in relation to other properties of soil derived from loess and glaciofluvial sand. Ecol Res 31:655–664. https://doi.org/10.1007/s11284-016-1375-6
Boro M, Sannyasi S, Chettri D, Verma AK (2022) Microorganisms in biological control strategies to manage microbial plant pathogens: a review. Arch Microbiol 204:666. https://doi.org/10.1007/s00203-022-03279-w
Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–46
Burke DJ, Weintraub MN, Hewins CR, Kalisz S (2011) Relationship between soil enzyme activities, nutrient cycling and soil fungal communities in a northern hardwood forest. Soil Biol Biochem 43:795–803. https://doi.org/10.1016/j.soilbio.2010.12.014
Cao GH, Wang XF, Li ZD, Zhang X, Li XG, Gu W, Zhang F, Yu J, He S (2022) A Panax notoginseng phosphate transporter, PnPht1; 3, greatly contributes to phosphate and arsenate uptake. Funct Plant Biol 49:259–271. https://doi.org/10.1071/fp21218
Chen Z, Ma S, Liu LL (2008) Studies on phosphorus solubilizing activity of a strain of phosphobacteria isolated from chestnut type soil in China. Biores Technol 99:6702–6707. https://doi.org/10.1016/j.biortech.2007.03.064
Costa AS, Nascimento AL, Botero WG, Carvalho CM, Tonholo J, Santos JC, Anunciaçao ˜DS (2022) Interaction between humic substances and arsenic species simulating environmental conditions. Sci Total Environ 802:149779. https://doi.org/10.1016/j.scitotenv.2021.149779
Ding C, Long X, Zeng G, Ouyang Y, Lei B, Zeng R, Wang J, Zhou Z (2023) Efficiency Recycling and Utilization of Phosphate from Wastewater Using LDHs-Modified Biochar. Int J Environ Res Public Health 20:3051. https://doi.org/10.3390/ijerph20043051
Gao T, Tian H, Niu H, Wang Z, Dai M, Megharaj M, He W (2023) Soil phosphatase assay to evaluate arsenic toxicity should be performed at the soil’s actual pH. Sci Total Environ 859:160184. https://doi.org/10.1016/j.scitotenv.2022.160184
Golfinopoulos SK, Varnavas SP, Alexakis DE (2021) The status of arsenic pollution in the Greek and Cyprus environment: An overview. Water 13:224. https://doi.org/10.3390/w13020224
Gong JY, Hou WP, Liu J, Malik K, Kong X, Wang L, Chen XL, Tang M, Zhu RQ, Cheng C, Liu YL, Wang JF, Yi Y (2022) Effects of different land use types and soil depths on soil mineral elements, soil enzyme activity, and fungal community in karst area of Southwest China. Int J Environ Res Public Health 19:3120. https://doi.org/10.3390/ijerph19053120
Gong X, Wei L, Yu X, Li S, Sun X, Wang X (2017) Effects of rhamnolipid and microbial inoculants on the vermicomposting of green waste with Eisenia fetida. PLoS ONE 12:e0170820. https://doi.org/10.1371/journal.pone.0170820
Gruba P, Mulder J (2015) Tree species affect cation exchange capacity (CEC) and cation binding properties of organic matter in acid forest soils. Sci Total Environ 511:655–662. https://doi.org/10.1016/j.scitotenv.2015.01.013
Jie W, Yang D, Yao Y, Guo N (2022) Effects of Rhizophagus intraradices on soybean yield and the composition of microbial communities in the rhizosphere soil of continuous cropping soybean. Sci Rep 12:17390. https://doi.org/10.1038/s41598-022-22473-w
Kamiya T, Islam R, Duan G, Uraguchi S, Fujiwara T (2013) Phosphate deficiency signaling pathway is a target of arsenate and phosphate transporterOsPT1is involved in As accumulation in shoots of rice. Soil Sci Plant Nutr 59:580–590. https://doi.org/10.1080/00380768.2013.804390
Koranda M, Rinnan R, Michelsen A (2023) Close coupling of plant functional types with soil microbial community composition drives soil carbon and nutrient cycling in tundra heath. Plant Soil 488:551–572. https://doi.org/10.1007/s11104-023-05993-w
Lechon-Alonso P, Clegg T, Cook J, Smith TP, Pawar S (2021) The role of competition versus cooperation in microbial community coalescence PLOS Computational Biology 17(11) e1009584. https://doi.org/10.1371/journal.pcbi.1009584
Lee JC, Kim EJ, Kim HW, Baek K (2016) Oxalate-based remediation of arsenic bound to amorphous Fe and Al hydrous oxides in soil. Geoderma 270:76–82. https://doi.org/10.1016/j.geoderma.2015.09.015
Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Biochar efects on soil biota–a review. Soil Biol Biochem 43:1812–1836. https://doi.org/10.1016/j.soilbio.2011.04.022
Li N, Sheng K, Zheng Q, Hu D, Zhang L, Wang J, Zhang W (2022a) Inoculation with phosphate-solubilizing bacteria alters microbial community and activates soil phosphorus supply to promote maize growth. Land Degrad Dev 34:777–788. https://doi.org/10.1002/ldr.4494
Li Q, Wu Q, Zhang T, Xiang P, Bao Z, Tu W, Li L, Wang Q (2022b) Phosphate mining activities affect crop rhizosphere fungal communities. Sci Total Environ 838:156196. https://doi.org/10.1016/j.scitotenv.2022.156196
Li SP, Tan JQ, Yang X, Ma C, Jiang L (2018) Niche and fitness differences determine invasion success and impact in laboratory bacterial communities. ISME J 13:402–412. https://doi.org/10.1038/s41396-018-0283-x
Li YB, Li Q, Guan GH, Chen SF (2020) Phosphate solubilizing bacteria stimulate wheat rhizosphere and endosphere biological nitrogen fixation by improving phosphorus content. PeerJ 8:e9062. https://doi.org/10.7717/peerj.9062
Likar M, Grašič M, Stres B, Regvar M, Gaberščik A (2022) Original leaf colonisers shape fungal decomposer communities of Phragmites australis in Intermittent habitats. J Fungi 8:284. https://doi.org/10.3390/jof8030284
Lin TY, Wei CC, Huang CW, Chang CH, Hsu FL, Liao VHC (2016) Both phosphorus fertilizers and indigenous bacteria enhance arsenic release into groundwater in arsenic-contaminated aquifers. J Agric Food Chem 64:2214–2222. https://doi.org/10.1021/acs.jafc.6b00253
Liu HY, Cheng JN, Jin H, Xu ZX, Yang XY, Min D, Xu XX, Shao XF, Lu DX, Qin B (2022) Characterization of rhizosphere and endophytic microbial communities associated with Stipa purpurea and their correlation with soil environmental factors. Plants 11:363. https://doi.org/10.3390/plants11030363
Lu RK (2000) Analytical Methods for Soil Agrochemistry. Chinese Agricultural Science and Technology Publishing House, Beijing (in Chinese)
Luan MD, Liu JL, Liu YW, Han XB, Sun GF, Lan WZ, Luan S (2018) Vacuolar phosphate transporter 1 (VPT1) affects arsenate tolerance by regulating phosphate homeostasis in Arabidopsis. Plant Cell Physiol 59:1345–1352. https://doi.org/10.1093/pcp/pcy025
Ma XM, Zhou Z, Chen J, Xu H, Ma SH, Dippold MA, Kuzyakov Y (2023) Long-term nitrogen and phosphorus fertilization reveals that phosphorus limitation shapes the microbial community composition and functions in tropical montane forest soil. Sci Total Environ 854:18709. https://doi.org/10.1016/j.scitotenv.2022.158709
Mącik M, Gryta A, Sas-Paszt L, Frąc M (2020) The status of soil microbiome as affected by the application of phosphorus biofertilizer: Fertilizer enriched with beneficial bacterial strains. Int J Mol Sci 21:8003. https://doi.org/10.3390/ijms21218003
Mckindles KM, Manes MA, Mckay RM, Davis TW, Bullerjahn GS, Beisner BE (2021) Environmental factors affecting chytrid (Chytridiomycota) infection rates on Planktothrix agardhii. J Plankton Res 43:658–672. https://doi.org/10.1093/plankt/fbab058
Meharg AA, Hartley-Whitaker J (2002) Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytol 154:29–43. https://doi.org/10.1046/j.1469-8137.2002.00363.x
Mei C, Chretien RL, Amaradasa BS, He Y, Turner A, Lowman S (2021) Characterization of phosphate solubilizing bacterial endophytes and plant growth promotion in vitro and in greenhouse. Microorganisms 9:1935. https://doi.org/10.3390/microorganisms9091935
Mohd S, Kushwaha AS, Shukla J, Mandrah K, Shankar J, Arjaria N, Saxena PN, Khare P, Narayan R, Dixit S, Siddiqui MH, Tuteja N, Das M, Roy SK, Kumar M (2019) Fungal mediated biotransformation reduces toxicity of arsenic to soil dwelling microorganism and plant. Ecotoxicol Environ Saf 176:108–118. https://doi.org/10.1016/j.ecoenv.2019.03.053
Mohite BV, Koli SH, Narkhede CP, Patil SN, Patil SV (2017) Prospective of microbial exopolysaccharide for heavy metal exclusion. Appl Biochem Biotechnol 183:582–600. https://doi.org/10.1007/s12010-017-2591-4
Muneer MA, Huang XM, Hou W, Zhang YD, Cai YY, Munir MZ, Wu LQ, Zheng CY (2021) Response of fungal diversity, community composition, and functions to nutrients management in red soil. J Fungi 7:554. https://doi.org/10.3390/jof7070554
Nurzhan A, Tian H, Nuralykyzy B, He W (2022) Soil enzyme activities and enzyme activity indices in long-term arsenic-contaminated soils. Eurasian Soil Sci 55:1425–1435. https://doi.org/10.1134/s106422932210012x
Osorio NW, Habte M (2012) Phosphate desorption from the surface of soil mineral particles by a phosphate-solubilizing fungus. Biol Fertil Soils 49:481–486. https://doi.org/10.1007/s00374-012-0763-5
Qiao JT, Li XM, Li FB, Liu TX, Young LY, Huang WL, Sun K, Tong H, Hu M (2019) Humic substances facilitate arsenic reduction and release in flooded paddy soil. Environ Sci Technol 53:5034–5042. https://doi.org/10.1021/acs.est.8b06333
Qiu ZG, Paungfoo-Lonhienne C, Ye J, Garcia AG, Petersen I, Bella LD, Hobbs R, Ibanez M, Heenan M, Wang WJ, Reeves S, Schmidt S (2022) Biofertilizers can enhance nitrogen use efficiency of sugarcane. Environ Microbiol 24:3655–3671. https://doi.org/10.1111/1462-2920.16027
Ramos FT, Dores EFGDC, Weber OLDS, Beber DC, Campelo JH, Maia JCDS (2018) Soil organic matter doubles the cation exchange capacity of tropical soil under no-till farming in Brazil. J Sci Food Agric 98:3595–3602. https://doi.org/10.1002/jsfa.8881
Rawat P, Das S, Shankhdhar D, Shankhdhar SC (2020) Phosphate-solubilizing microorganisms: mechanism and their role in phosphate solubilization and uptake. J Soil Sci Plant Nutr 21:49–68. https://doi.org/10.1007/s42729-020-00342-7
Rezakhani L, Motesharezadeh B, Tehrani MM, Etesami H, Hosseini HM (2022) The effect of silicon fertilization and phosphate-solubilizing bacteria on chemical forms of silicon and phosphorus uptake by wheat plant in a calcareous soil. Plant Soil 477:259–280. https://doi.org/10.1007/s11104-021-05274-4
Salo K, Domisch T, Kouki J (2019) Forest wildfire and 12 years of post-disturbance succession of saprotrophic macrofungi (Basidiomycota, Ascomycota). For Ecol Manage 451:117454. https://doi.org/10.1016/j.foreco.2019.117454
Scholz B, Küpper FC, Vyverman W, Karsten U (2016) Effects of eukaryotic pathogens (Chytridiomycota and Oomycota) on marine benthic diatom communities in the Solthörn tidal flat (southern North Sea, Germany). Eur J Phycol 51:253–269. https://doi.org/10.1080/09670262.2015.1134814
Smith SE, Christophersen HM, Pope S, Smith FA (2009) Arsenic uptake and toxicity in plants: integrating mycorrhizal influences. Plant Soil 327:1–21. https://doi.org/10.1007/s11104-009-0089-8
Summer ME, Miller WP (1996) Cation exchange capacity and exchange coefficients. In: Sparks, D.L. (Ed.), Methods of Soil Analysis. Part 3. Chemical Methods. Soil Science Society of America, Madison, WI, USA, pp 1201–1229
Tang JY, Zhang LH, Zhang JC, Ren LH, Zhou YY, Zheng YY, Luo L, Yang Y, Huang HL, Chen AW (2020) Physicochemical features, metal availability and enzyme activity in heavy metal-polluted soil remediated by biochar and compost. Sci Total Environ 701:134751. https://doi.org/10.1016/j.scitotenv.2019.134751
Thomas GW (1996) Soil pH and soil acidity. In: Sparks, D.L. (Ed.), Methods of Soil Analysis. Part 3. Chemical Methods. Soil Science Society of America, Madison, WI, USA, pp 475–490
Vasques ICF, De Mello JWV, Veloso RW, Ferreira VDP, WaP A (2018) Effectiveness of ferric, ferrous, and aluminum (hydr)oxide coprecipitation to treat water contaminated with arsenate. J Environ Qual 47:1339–1346. https://doi.org/10.2134/jeq2018.01.0014
Wang JH, Liu L, Gao XY, Hao JX, Wang ML (2021) Elucidating the effect of biofertilizers on bacterial diversity in maize rhizosphere soil. PLoS ONE 16:e0249834. https://doi.org/10.1371/journal.pone.0249834
Wang YQ, Kong LX, Wang K, Tao YJ, Qi H, Wan YA, Wang Q, Li HF (2022) The combined impacts of selenium and phosphorus on the fate of arsenic in rice seedlings (Oryza sativa L.). Chemosphere 308:136590. https://doi.org/10.1016/j.chemosphere.2022.136590
Wang ZQ, Tian HX, Lei M, Megharaj M, Tan XP, WangF JHZ, He WX (2020) Soil enzyme kinetics indicate ecotoxicity of long-term arsenic pollution in the soil at field scale. Ecotoxicol Environ Saf 191:110215. https://doi.org/10.1016/j.ecoenv.2020.11021
Wang ZH, Zhang HH, Liu L, Li SJ, Xie JF, Xue X, Jiang Y (2022b) Screening of phosphate-solubilizing bacteria and their abilities of phosphorus solubilization and wheat growth promotion. BMC Microbiol 22:296. https://doi.org/10.1186/s12866-022-02715-7
Woolson EA, Axley JH, Kearney PC (1971) Correlation between available soil arsenic, estimated by six methods, and response of corn (Zea mays L.). Soil Sci Soc Am J 35:101–105. https://doi.org/10.2136/sssaj1971.03615995003500010030x
Wu F, Fang Q, Yan SW, Pan L, Tang XJ, Ye WL (2020) Effects of zinc oxide nanoparticles on arsenic stress in rice (Oryza sativa L.): germination, early growth, and arsenic uptake. Environ Sci Pollut Res 27:26974–26981. https://doi.org/10.1007/s11356-020-08965-0
Wu JW, Liang JL, Björn LO, Li JT, Shu WS, Wang YT (2022) Phosphorus-arsenic interaction in the ‘soil-plant-microbe’ system and its influence on arsenic pollution. Sci Total Environ 802:149796. https://doi.org/10.1016/j.scitotenv.2021.149796
Wu ZC, Ren HY, Mcgrath SP, Wu P, Zhao FJ (2011) Investigating the contribution of the phosphate transport pathway to arsenic accumulation in rice. Plant Physiol 157:498–508. https://doi.org/10.1104/pp.111.178921
Xu ZW, Yu GR, Zhang XY, Ge JP, He NP, Wang QF, Wang D (2015) The variations in soil microbial communities, enzyme activities and their relationships with soil organic matter decomposition along the northern slope of Changbai Mountain. Appl Soil Ecol 86:19–29. https://doi.org/10.1016/j.apsoil.2014.09.015
Xue SG, Jiang XX, Wu C, Hartley W, Qian ZY, Luo XH, Li WC (2020) Microbial driven iron reduction affects arsenic transformation and transportation in soil-rice system. Environ Pollut 260:114010. https://doi.org/10.1016/j.envpol.2020.114010
Yan JY, Ren T, Wang KK, Ye TH, Song Y, Cong RH, Li XK, Lu ZF, Lu JW (2022) Optimizing phosphate fertilizer input to reduce phosphorus loss in rice-oilseed rape rotation. Environ Sci Pollut Res 30:31533–33145. https://doi.org/10.1007/s11356-022-24133-y
Yang JS, Yang FL, Yang Y, Xing GL, Deng CP, Shen YT, Luo LQ, Li BZ, Yuan HL (2016) A proposal of “core enzyme” bioindicator in long-term Pb-Zn ore pollution areas based on topsoil property analysis. Environ Pollut 213:760–769. https://doi.org/10.1016/j.envpol.2016.03.030
Zhang J, Zhou WX, Liu BB, He J, Shen QR, Zhao FJ (2015) Anaerobic arsenite oxidation by an autotrophic arsenite-oxidizing bacterium from an arsenic-contaminated paddy soil. Environ Sci Technol 49:5956–5964. https://doi.org/10.1021/es506097c
Zhang KY, Teng ZD, Shao W, Wang Y, Li M, Lam SS (2020) Effective passivation of lead by phosphate solubilizing bacteria capsules containing tricalcium phosphate. J Hazard Mater 397:122754. https://doi.org/10.1016/j.jhazmat.2020.122754
Zhang XJ, Zhan YB, Zhang H, Wang RH, Tao XL, Zhang LP, Zuo YL, Zhang L, Wei YQ, Li J (2021) Inoculation of phosphate-solubilizing bacteria (Bacillus) regulates microbial interaction to improve phosphorus fractions mobilization during kitchen waste composting. Biores Technol 340:125714. https://doi.org/10.1016/j.biortech.2021.125714
Zhao YH, Naeth MA (2022) Soil amendment with a humic substance and arbuscular mycorrhizal Fungi enhance coal mine reclamation. Sci Total Environ 823:153696. https://doi.org/10.1016/j.scitotenv.2022.153696