Abstract
Purpose
Cadmium (Cd) accumulation in rice can be regulated by applying sulfur (S) fertilizers and water management, but the mechanism and the effect on soil microorganisms are unclear. This study aims to clarify the effect of sulfur forms on rice Cd accumulation and soil microbial community structure under different irrigation regimes.
Methods
The present study investigated the effects of sulfur fertilizers (S0 and Na2SO4) and water management by continuous flooding (flooded) and intermittent flooding and draining (Int-F3D5) on soil Cd bioavailability and the microbial community structure using inductively coupled plasma mass spectrometry (ICP-MS), scanning electron microscopy with energy dispersive X-ray spectrometry (SEM–EDS), and 16S rRNA gene sequencing technology.
Results
When flooded, S0 and Na2SO4 increased the dry weight of rice grain 2.3- and 0.9-fold, respectively, and reduced the Cd concentration by 152% and 61%, respectively. The ascorbic citrate acetic (ACA) extractable Fe content from flooded rice surface treated with S0 and Na2SO4 increased by 98% and 64%, respectively, indicating that the S fertilizer promoted iron plaque formation on the surfaces of rice roots. Gammaproteobacteria were the most predominant under all management conditions. Syntrophobacteraceae and Geobacter were particularly abundant in the rice rhizosphere treated with Int-F3D5 and exogenous Na2SO4, and it might play a crucial role in alleviating Cd stress caused by S fertilizer.
Conclusion
Under flooded conditions, S0 had a more significant effect on the reduction of cadmium uptake by rice. Sulfur fertilizers promoted iron plaque formation partially to hinder Cd accumulation. Under Int-F3D5 conditions, Na2SO4 recruited more beneficial rhizosphere bacteria, which may be a potential mechanism of reducing Cd transfer from soil to rice.
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Data availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Abbreviations
- ACA:
-
Ascorbic-citric-acetic acid
- DTPA:
-
Diethylene triamine pentaacetic acid
- EDTA:
-
Ethylene diamaine tetraacetic acid
- GSH:
-
Glutathione
- PCs:
-
Phytochelatins
- ICP-MS:
-
Inductively coupled plasma mass spectrometry
- SEM-EDS:
-
Scanning electron microscopy with energy dispersive X-ray spectrometry
- LDA:
-
Least discriminant analysis
- LSD:
-
Least significant difference
- PCoA:
-
Principal coordinate analysis
- SOB:
-
S-oxidizing bacteria
- SRB:
-
S-reducing bacteria
- PERMANOVA:
-
Permutational multivariate analysis of variance
References
Ahmed HP, Schoenau JJ, King T, Kar G (2016) Effects of seed-placed sulfur fertilizers on canola, wheat, and pea yield; sulfur uptake; and soil sulfate concentrations over time in three prairie soils. J Plant Nutr 40(4):543–557. https://doi.org/10.1080/01904167.2016.1262413
Alfvén T, Elinder C-G, Carlsson MD, Grubb A, Hellström L, Persson B, Pettersson C, Spång G, Schütz A, Järup L (2000) Low-level cadmium exposure and osteoporosis. J Bone Miner Res 15(8):1579–1586. https://doi.org/10.1359/jbmr.2000.15.8.1579
Alquethamy Saleh F, Adams Felise G, Maharjan R, Delgado Natasha N, Zang M, Ganio K, Paton James C, Hassan Karl A, Paulsen Ian T, McDevitt Christopher A, Cain Amy K, Eijkelkamp Bart A (2021) The molecular basis of acinetobacter baumannii cadmium toxicity and resistance. Appl Environ Microbiol 87(22):e01718-e1721. https://doi.org/10.1128/AEM.01718-21
Ambreetha S, Chinnadurai C, Marimuthu P, Balachandar D (2018) Plant-associated Bacillus modulates the expression of auxin-responsive genes of rice and modifies the root architecture. Rhizosphere 5:57–66. https://doi.org/10.1016/j.rhisph.2017.12.001
Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E, Umar S, Ahmad A, Khan NA, Iqbal M, Prasad MNV (2011) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids—a review. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2011.07.002
Armstrong J, Armstrong W (2005) Rice: sulfide-induced barriers to root radial oxygen loss, Fe2+ and water uptake, and lateral root emergence. Ann Bot 96(4):625–638. https://doi.org/10.1093/aob/mci215
Cao Z-Z, Qin M-L, Lin X-Y, Zhu Z-W, Chen M-X (2018) Sulfur supply reduces cadmium uptake and translocation in rice grains (Oryza sativa L.) by enhancing iron plaque formation, cadmium chelation and vacuolar sequestration. Environ Pollut 238:76–84. https://doi.org/10.1016/j.envpol.2018.02.083
Chen Z, Zhu Y-G, Liu W-J, Meharg AA (2005) Direct evidence showing the effect of root surface iron plaque on arsenite and arsenate uptake into rice (Oryza sativa) roots. New Phytol 165(1):91–97. https://doi.org/10.1111/j.1469-8137.2004.01241.x
Cheng H, Wang M, Wong MH, Ye Z (2014) Does radial oxygen loss and iron plaque formation on roots alter Cd and Pb uptake and distribution in rice plant tissues? Plant Soil 375(1):137–148. https://doi.org/10.1007/s11104-013-1945-0
Czarny J, Staninska-Pięta J, Piotrowska-Cyplik A, Juzwa W, Wolniewicz A, Marecik R, Ławniczak Ł, Chrzanowski Ł (2020) Acinetobacter sp. as the key player in diesel oil degrading community exposed to PAHs and heavy metals. J Hazard Mater 383:121168. https://doi.org/10.1016/j.jhazmat.2019.121168
Fan J-L, Hu Z-Y, Ziadi N, Xia X, Wu C-Y-H (2010) Excessive sulfur supply reduces cadmium accumulation in brown rice (Oryza sativa L.). Environ Pollut 158(2):409–415. https://doi.org/10.1016/j.envpol.2009.08.042
Fan K, Delgado-Baquerizo M, Guo X, Wang D, Zhu Y-G, Chu H (2021) Biodiversity of key-stone phylotypes determines crop production in a 4-decade fertilization experiment. ISME J 15(2):550–561. https://doi.org/10.1038/s41396-020-00796-8
Flynn TM, O’Loughlin EJ, Mishra B, DiChristina TJ, Kemner KM (2014) Sulfur-mediated electron shuttling during bacterial iron reduction. Science 344(6187):1039–1042. https://doi.org/10.1126/science.1252066
Gao MX, Hu ZY, Wang GD, Xia X (2010) Effect of elemental sulfur supply on cadmium uptake into rice seedlings when cultivated in low and excess cadmium soils. Commun Soil Sci Plant Anal 41(8):990–1003. https://doi.org/10.1080/00103621003646071
Giotta L, Agostiano A, Italiano F, Milano F, Trotta M (2006) Heavy metal ion influence on the photosynthetic growth of Rhodobacter sphaeroides. Chemosphere 62(9):1490–1499. https://doi.org/10.1016/j.chemosphere.2005.06.014
Gross Briana L, Zhao Z (2014) Archaeological and genetic insights into the origins of domesticated rice. Proc Natl Acad Sci 111(17):6190–6197. https://doi.org/10.1073/pnas.1308942110
Hashimoto Y, Furuya M, Yamaguchi N, Makino T (2016) Zerovalent iron with high sulfur content enhances the formation of cadmium sulfide in reduced paddy soils. Soil Sci Soc Am J 80(1):55–63. https://doi.org/10.2136/sssaj2015.06.0217
Hassan MJ, Wang Z, Zhang G (2005) Sulfur alleviates growth inhibition and oxidative stress caused by cadmium toxicity in rice. J Plant Nutr 28(10):1785–1800. https://doi.org/10.1080/01904160500251092
Hester ER, Vaksmaa A, Valè G, Monaco S, Jetten MSM, Lüke C (2022) Effect of water management on microbial diversity and composition in an Italian rice field system. Fems Microbiol Ecol 98(3):fiac018. https://doi.org/10.1093/femsec/fiac018
Hu Y, Cheng H, Tao S (2016) The challenges and solutions for cadmium-contaminated rice in China: a critical review. Environ Int 92–93:515–532. https://doi.org/10.1016/j.envint.2016.04.042
Huang G, Ding C, Li Y, Zhang T, Wang X (2020) Selenium enhances iron plaque formation by elevating the radial oxygen loss of roots to reduce cadmium accumulation in rice (Oryza sativa L.). J Hazard Mater 398:122860. https://doi.org/10.1016/j.jhazmat.2020.122860
Hussain B, Ashraf MN, Shafeeq ur Rahman AA, Li J, Farooq M (2021) Cadmium stress in paddy fields: effects of soil conditions and remediation strategies. Sci Total Environ 754:142188. https://doi.org/10.1016/j.scitotenv.2020.142188
Irawati W, Parhusip AJ, Sopiah N (2016) Heavy metals biosorption by copper resistant bacteria of acinetobacter sp. IrC2. Microbiol Indones 9(4):4. https://doi.org/10.5454/mi.9.4.4
Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7(2):60–72. https://doi.org/10.2478/intox-2014-0009
Jørgensen BB (1982) Mineralization of organic matter in the sea bed—the role of sulphate reduction. Nature 296(5858):643–645. https://doi.org/10.1038/296643a0
Khanam R, Kumar A, Nayak AK, Shahid M, Tripathi R, Vijayakumar S, Bhaduri D, Kumar U, Mohanty S, Panneerselvam P, Chatterjee D, Satapathy BS, Pathak H (2020) Metal(loid)s (As, Hg, Se, Pb and Cd) in paddy soil: bioavailability and potential risk to human health. Sci Total Environ 699:134330. https://doi.org/10.1016/j.scitotenv.2019.134330
Lafferty BJ, Loeppert RH (2005) Methyl arsenic adsorption and desorption behavior on iron oxides. Environ Sci Technol 39(7):2120–2127. https://doi.org/10.1021/es048701+
Leustek T, Saito K (1999) Sulfate transport and assimilation in plants. Plant Physiol 120(3):637–644. https://doi.org/10.1104/pp.120.3.637
Li J, Xu Y (2018) Effects of clay combined with moisture management on Cd immobilization and fertility index of polluted rice field. Ecotox Environ Safe 158:182–186. https://doi.org/10.1016/j.ecoenv.2018.04.031
Li M, Fang A, Yu X, Zhang K, He Z, Wang C, Peng Y, Xiao F, Yang T, Zhang W, Zheng X, Zhong Q, Liu X, Yan Q (2021) Microbially-driven sulfur cycling microbial communities in different mangrove sediments. Chemosphere 273:128597. https://doi.org/10.1016/j.chemosphere.2020.128597
Liu P, Pommerenke B, Conrad R (2018) Identification of Syntrophobacteraceae as major acetate-degrading sulfate reducing bacteria in Italian paddy soil. Environ Microbiol 20(1):337–354. https://doi.org/10.1111/1462-2920.14001
Liu WJ, Zhu YG, Smith FA, Smith SE (2004) Do iron plaque and genotypes affect arsenate uptake and translocation by rice seedlings (Oryza sativa L.) grown in solution culture? J Exp Bot 55(403):1707–1713. https://doi.org/10.1093/jxb/erh205
Liu Y, Wu T, White JC, Lin D (2021a) A new strategy using nanoscale zero-valent iron to simultaneously promote remediation and safe crop production in contaminated soil. Nat Nanotechnol 16(2):197–205. https://doi.org/10.1038/s41565-020-00803-1
Liu Z, Wang Q-Q, Huang S-Y, Kong L-X, Zhuang Z, Wang Q, Li H-F, Wan Y-N (2022) The risks of sulfur addition on cadmium accumulation in paddy rice under different water-management conditions. J Environ Sci 118:101–111. https://doi.org/10.1016/j.jes.2021.08.022
Liu Z, Zhuang Z, Yu Y, Wang Q, Wan Y-N, Li H-F (2021b) Arsenic transfer and accumulation in the soil-rice system with sulfur application and different water managements. Chemosphere 269:128772. https://doi.org/10.1016/j.chemosphere.2020.128772
Malhi S, Schoenau J, Grant C (2005) A review of sulphur fertilizer management for optimum yield and quality of canola in the Canadian Great Plains. Can J Plant Sci 85:297–307. https://doi.org/10.4141/P04-140
Masuda S, Bao Z, Okubo T, Sasaki K, Ikeda S, Shinoda R, Anda M, Kondo R, Mori Y, Minamisawa K (2016) Sulfur fertilization changes the community structure of rice root-, and soil- associated bacteria. Microbes Environ 31(1):70–75. https://doi.org/10.1264/jsme2.ME15170
Mendis HC, Thomas VP, Schwientek P, Salamzade R, Chien JT, Waidyarathne P, Kloepper J, De La Fuente L (2018) Strain-specific quantification of root colonization by plant growth promoting rhizobacteria Bacillus firmus I-1582 and Bacillus amyloliquefaciens QST713 in non-sterile soil and field conditions. PLoS ONE 13(2):e0193119. https://doi.org/10.1371/journal.pone.0193119
Mugford SG, Lee BR, Koprivova A, Matthewman C, Kopriva S (2011) Control of sulfur partitioning between primary and secondary metabolism. Plant J 65(1):96–105. https://doi.org/10.1111/j.1365-313X.2010.04410.x
Murase J, Kimura M (1997) Anaerobic reoxidation of Mn 2+, Fe 2+, S 0 and S 2- in submerged paddy soils. Biol Fertil Soils 25:302–306. https://doi.org/10.1007/s003740050319
Muyzer G, Stams AJ (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6(6):441–454. https://doi.org/10.1038/nrmicro1892
Noctor G, Queval G, Mhamdi A, Chaouch S, Foyer CH (2011) Glutathione. Arabidopsis Book 9:e0142. https://doi.org/10.1199/tab.0142
Pereira EG, Oliva MA, Siqueira-Silva AI, Rosado-Souza L, Pinheiro DT, Almeida AM (2014) Tropical rice cultivars from lowland and upland cropping systems differ in iron plaque formation. J Plant Nutr 37(9):1373–1394. https://doi.org/10.1080/01904167.2014.888744
Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11(11):789–799. https://doi.org/10.1038/nrmicro3109
Pishchik VN, Vorob’ev NI, Provorov NA, Khomyakov YV (2016) Mechanisms of plant and microbial adaptation to heavy metals in plant–microbial systems. Microbiology 85(3):257–271. https://doi.org/10.1134/s0026261716030097
Rennenberg H (1984) The fate of excess sulfur in higher plants. Annu Rev Plant Physiol 35(1):121–153. https://doi.org/10.1146/annurev.pp.35.060184.001005
Roane TM, Pepper IL (1999) Microbial responses to environmentally toxic cadmium. Microb Ecol 38(4):358–364. https://doi.org/10.1007/s002489901001
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12(6):R60. https://doi.org/10.1186/gb-2011-12-6-r60
Shinoda R, Bao Z, Minamisawa K (2019) CH4 oxidation-dependent 15N2 fixation in rice roots in a low-nitrogen paddy field and in Methylosinus sp. strain 3S–1 isolated from the roots. Soil Biol Biochem 132:40–46. https://doi.org/10.1016/j.soilbio.2019.01.021
Srivastava S, Srivastava S, Bist V, Awasthi S, Chauhan R, Chaudhry V, Singh PC, Dwivedi S, Niranjan A, Agrawal L, Chauhan PS, Tripathi RD, Nautiyal CS (2018) Chlorella vulgaris and Pseudomonas putida interaction modulates phosphate trafficking for reduced arsenic uptake in rice (Oryza sativa L.). J Hazard Mater 351:177–187. https://doi.org/10.1016/j.jhazmat.2018.02.039
Sun L, Yang J, Fang H, Xu C, Peng C, Huang H, Lu L, Duan D, Zhang X, Shi J (2017) Mechanism study of sulfur fertilization mediating copper translocation and biotransformation in rice (Oryza sativa L.) plants. Environ Pollut 226:426–434. https://doi.org/10.1016/j.envpol.2017.03.080
Sun L-N, Zhang Y-F, He L-Y, Chen Z-J, Wang Q-Y, Qian M, Sheng X-F (2010) Genetic diversity and characterization of heavy metal-resistant-endophytic bacteria from two copper-tolerant plant species on copper mine wasteland. Biores Technol 101(2):501–509. https://doi.org/10.1016/j.biortech.2009.08.011
Tang X, Li L, Wu C, Khan MI, Manzoor M, Zou L, Shi J (2020) The response of arsenic bioavailability and microbial community in paddy soil with the application of sulfur fertilizers. Environ Pollut 264:114679. https://doi.org/10.1016/j.envpol.2020.114679
Tripathi RD, Tripathi P, Dwivedi S, Kumar A, Mishra A, Chauhan PS, Norton GJ, Nautiyal CS (2014) Roles for root iron plaque in sequestration and uptake of heavy metals and metalloids in aquatic and wetland plants. Metallomics 6(10):1789–1800. https://doi.org/10.1039/c4mt00111g
Uraguchi S, Fujiwara T (2012) Cadmium transport and tolerance in rice: perspectives for reducing grain cadmium accumulation. Rice (N Y) 5(1):5–5. https://doi.org/10.1186/1939-8433-5-5
Wang B, Du Y (2013) Cadmium and its neurotoxic effects. Oxid Med Cell Longev 2013:898034. https://doi.org/10.1155/2013/898034
Wang R, Wei S, Jia P, Liu T, Hou D, Xie R, Lin Z, Ge J, Qiao Y, Chang X, Lu L, Tian S (2019) Biochar significantly alters rhizobacterial communities and reduces Cd concentration in rice grains grown on Cd-contaminated soils. Sci Total Environ 676:627–638. https://doi.org/10.1016/j.scitotenv.2019.04.133
Wei B, Yang L (2010) A review of heavy metal contaminations in urban soils, urban road dusts and agricultural soils from China. Microchem J 94(2):99–107. https://doi.org/10.1016/j.microc.2009.09.014
Wood JL, Zhang C, Mathews ER, Tang C, Franks AE (2016) Microbial community dynamics in the rhizosphere of a cadmium hyper-accumulator. Sci Rep 6:36067. https://doi.org/10.1038/srep36067
Wu G, Hu P, Zhou J, Dong B, Wu L, Luo Y, Christie P (2019a) Sulfur application combined with water management enhances phytoextraction rate and decreases rice cadmium uptake in a Sedum plumbizincicola - Oryza sativa rotation. Plant Soil 440(1):539–549. https://doi.org/10.1007/s11104-019-04095-w
Wu S, Li R, Xie S, Shi C (2019b) Depth-related change of sulfate-reducing bacteria community in mangrove sediments: the influence of heavy metal contamination. Mar Pollut Bull 140:443–450. https://doi.org/10.1016/j.marpolbul.2019.01.042
Yoo J, Kim W, Kim J-Y, Römkens P, Lee J-B, Kim D (2013) Effects of chemical applications to metal polluted soils on cadmium uptake by rice plant. E3S Web Conf 1:01006. https://doi.org/10.1051/e3sconf/20130101006
Zandi P, Xia X, Yang J, Liu J, Remusat L, Rumpel C, Bloem E, Krasny BB, Schnug E (2023) Speciation and distribution of chromium (III) in rice root tip and mature zone: the significant impact of root exudation and iron plaque on chromium bioavailability. J Hazard Mater 448:130992. https://doi.org/10.1016/j.jhazmat.2023.130992
Zandi P, Yang J, Xia X, Tian Y, Li Q, Możdżeń K, Barabasz-Krasny B, Wang Y (2020) Do sulfur addition and rhizoplane iron plaque affect chromium uptake by rice (Oryza sativa L.) seedlings in solution culture? J Hazard Mater 388:121803. https://doi.org/10.1016/j.jhazmat.2019.121803
Zhang D, Du G, Chen D, Shi G, Rao W, Li X, Jiang Y, Liu S, Wang D (2019a) Effect of elemental sulfur and gypsum application on the bioavailability and redistribution of cadmium during rice growth. Sci Total Environ 657:1460–1467. https://doi.org/10.1016/j.scitotenv.2018.12.057
Zhang J, Wang L-H, Yang J-C, Liu H, Dai J-L (2015) Health risk to residents and stimulation to inherent bacteria of various heavy metals in soil. Sci Total Environ 508:29–36. https://doi.org/10.1016/j.scitotenv.2014.11.064
Zhang Q, Chen H, Huang D, Xu C, Zhu H, Zhu Q (2019b) Water managements limit heavy metal accumulation in rice: dual effects of iron-plaque formation and microbial communities. Sci Total Environ 687:790–799. https://doi.org/10.1016/j.scitotenv.2019.06.044
Zhang Q, Chen HF, Huang DY, Guo XB, Xu C, Zhu HH, Li B, Liu TT, Feng RW, Zhu QH (2022) Sulfur fertilization integrated with soil redox conditions reduces Cd accumulation in rice through microbial induced Cd immobilization. Sci Total Environ 824:153868. https://doi.org/10.1016/j.scitotenv.2022.153868
Zhang Y, Wang X, Zhen Y, Mi T, He H, Yu Z (2017) Microbial diversity and community structure of sulfate-reducing and sulfur-oxidizing bacteria in sediment cores from the East China Sea. Front Microbiol 8:2133. https://doi.org/10.3389/fmicb.2017.02133
Zhang Z, Furman A (2021) Soil redox dynamics under dynamic hydrologic regimes - a review. Sci Total Environ 763:143026. https://doi.org/10.1016/j.scitotenv.2020.143026
Zheng H, Wang M, Chen S, Li S, Lei X (2019) Sulfur application modifies cadmium availability and transfer in the soil-rice system under unstable pe+pH conditions. Ecotox Environ Safe 184:109641. https://doi.org/10.1016/j.ecoenv.2019.109641
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The present study was financially supported by the Zhejiang Provincial Natural Science Foundation of China (grant number LZ22D010004), the National Nature Science Foundation of China (grant number 41401366), and the National Key Research and Development Program of China (grant number 2016YFD0800805 and 2017YFD0801303).
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Yili Zang and Jie Zhao: methodology, data curation, formal analysis, investigation, writing—original draft, writing—review, and editing. Weikang Chen: methodology, formal analysis, investigation, and visualization. Lingli Lu: writing—review and editing, supervision. Jiuzhou Chen: formal analysis and investigation. Zhi Lin: investigation. Yabei Qiao: investigation. Haizhong Lin: writing—review, and editing. Shengke Tian: conceptualization, supervision, funding acquisition, and project administration.
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Zang, Y., Zhao, J., Chen, W. et al. Sulfur and water management mediated iron plaque and rhizosphere microorganisms reduced cadmium accumulation in rice. J Soils Sediments 23, 3177–3190 (2023). https://doi.org/10.1007/s11368-023-03537-4
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DOI: https://doi.org/10.1007/s11368-023-03537-4