|
|
Chromium phytoextraction and physiological responses of the hyperaccumulator Leersia hexandra Swartz to plant growth-promoting rhizobacterium inoculation |
Xuehong Zhang1,2, Yuanyuan Zhang1, Dan Zhu3, Zhiyi Lin2, Na Sun1, Chang Su1, Hua Lin2( ), Junjian Zheng1( ) |
1. College of Life and Environmental Science, Guilin University of Electronic Technology, Guilin 541004, China 2. College of Environmental Science and Engineering, Guilin University of Technology, Guilin 541004, China 3. College of Mathematics and Science, Wuhan Institute of Technology, Wuhan 430205, China |
|
|
Abstract ● Improved Cr phytoextration efficiency was achieved by B. cereus inoculation. ● B. cereus could produce plant-beneficial PGPR factors at diverse Cr stresses. ● Enhanced resistance of inoculated L. hexandra towards elevated Cr stress. ● The majority of Cr existed in the stable forms in the tissues of L. hexandra. Phytoextraction is a promising option for purifying hexavalent chromium (Cr(VI))-laden wastewater, but the long remediation period incurred by poor growth rate of Cr hyperaccumulators remains a primary hindrance to its large-scale application. In this study, we performed a hydroponic experiment to evaluate the feasibility of promoting the growth and phytoextraction efficiency of Cr hyperaccumulator Leersia hexandra Swartz (L. hexandra) by inoculating plant growth-promoting rhizobacteria (PGPR) Bacillus cereus (B. cereus). In batch tests, the Cr(VI) removal rates of L. hexandra and B. cereus co-culture were greater than the sum of their respective monocultures. This was likely due to the microbial reduction of Cr(VI) to Cr(III), which is amiable to plant uptake. Besides, the PGPR factors of B. cereus, including indoleacetic acid (IAA) production, 1-aminocyclopropane-1-carboxylic acid deamination (ACCd) activity, phosphate solubilization capacity, and siderophore production, were quantified. These PGPR factors helped explain the biomass augmentation, root elongation and enhanced Cr enrichment of the inoculated L. hexandra in pot experiments. Despite the increased Cr uptake, no aggravated oxidative damage to the cell membrane was observed in the inoculated L. hexandra. This was attributed to its capacity to confront the increased intracellular Cr stress by upregulating both the activities of antioxidative enzymes and expression of metal-binding proteins/peptides. Moreover, L. hexandra could always conserve the majority of Cr in the residual and oxalic integrated forms with low mobility and phytotoxicity, irrespective of the B. cereus inoculation. These results highlight the constructed Cr hyperaccumulator-rhizobacteria consortia as an effective candidate for decontaminating Cr(VI)-laden wastewater.
|
Keywords
Hexavalent chromium
Hyperaccumulator
Rhizobacteria
Leersia hexandra Swartz
Bacillus cereus
Consortia
|
Corresponding Author(s):
Hua Lin,Junjian Zheng
|
About author: Tongcan Cui and Yizhe Hou contributed equally to this work. |
Issue Date: 18 August 2022
|
|
1 |
G Agar, M S Taspinar, E Yildirim, M Aydin, M Yuce. (2020). Effects of ascorbic acid and copper treatments on metallothionein gene expression and antioxidant enzyme activities in Helianthus annuus L. exposed to chromium stress. Journal of Plant Growth Regulation, 39( 2): 897– 904
https://doi.org/10.1007/s00344-019-10031-0
|
2 |
Z Anfar, H Ait Ahsaine, M Zbair, A Amedlous, A Ait El Fakir, A Jada, N El Alem. (2020). Recent trends on numerical investigations of response surface methodology for pollutants adsorption onto activated carbon materials: a review. Critical Reviews in Environmental Science and Technology, 50( 10): 1043– 1084
https://doi.org/10.1080/10643389.2019.1642835
|
3 |
APHA ( 1989). Standard methods for the examination of water and wastewater. New York: American Public Health Association, American Water Works Association, Water Pollution Control Federation, and Water Environment Federation
|
4 |
S A Asad, M Farooq, A Afzal, H West. (2019). Integrated phytobial heavy metal remediation strategies for a sustainable clean environment: a review. Chemosphere, 217 : 925– 941
https://doi.org/10.1016/j.chemosphere.2018.11.021
pmid: 30586789
|
5 |
A J M Baker, R R Brooks. (1989). Terrestrial higher plants which hyperaccumulate metallic elements - a review of their distribution, ecology and phytochemistry. Biorecovery, 1 : 81– 126
|
6 |
Doğanlar Z Banu. (2013). Metal accumulation and physiological responses induced by copper and cadmium in Lemna gibba, L. minor and Spirodela polyrhiza. Chemical Speciation and Bioavailability, 25( 2): 79– 88
https://doi.org/10.3184/095422913X13706128469701
|
7 |
M I Cabello-Conejo, C Becerra-Castro, A Prieto-Fernández, C Monterroso, A Saavedra-Ferro, M Mench, P S Kidd. (2014). Rhizobacterial inoculants can improve nickel phytoextraction by the hyperaccumulator Alyssum pintodasilvae. Plant and Soil, 379( 1–2): 35– 50
https://doi.org/10.1007/s11104-014-2043-7
|
8 |
S Cendrowski, W MacArthur, P Hanna. (2004). Bacillus anthracis requires siderophore biosynthesis for growth in macrophages and mouse virulence. Molecular Microbiology, 51( 2): 407– 417
https://doi.org/10.1046/j.1365-2958.2003.03861.x
pmid: 14756782
|
9 |
S Das, J Mishra, S K Das, S Pandey, D S Rao, A Chakraborty, M Sudarshan, N Das, H Thatoi. (2014). Investigation on mechanism of Cr(VI) reduction and removal by Bacillus amyloliquefaciens, a novel chromate tolerant bacterium isolated from chromite mine soil. Chemosphere, 96 : 112– 121
https://doi.org/10.1016/j.chemosphere.2013.08.080
pmid: 24091247
|
10 |
C O Dimkpa, A Svatoš, P Dabrowska, A Schmidt, W Boland, E Kothe. (2008). Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere, 74( 1): 19– 25
https://doi.org/10.1016/j.chemosphere.2008.09.079
pmid: 18986679
|
11 |
A Durand, S Piutti, M Rue, J L Morel, G Echevarria, E Benizri. (2016). Improving nickel phytoextraction by co-cropping hyperaccumulator plants inoculated by plant growth promoting rhizobacteria. Plant and Soil, 399( 1–2): 179– 192
https://doi.org/10.1007/s11104-015-2691-2
|
12 |
M Dworkin, J W Foster. (1958). Experiments with some microorganisms which utilize ethane and hydrogen. Journal of Bacteriology, 75( 5): 592– 603
https://doi.org/10.1128/jb.75.5.592-603.1958
pmid: 13538930
|
13 |
J Ge, H Wang, J Lin, S Tian, J Zhao, X Lin, L Lu. (2020). Nickel tolerance, translocation and accumulation in a Cd/Zn co-hyperaccumulator plant Sedum alfredii. Journal of Hazardous Materials, 398 : 123074
https://doi.org/10.1016/j.jhazmat.2020.123074
pmid: 32768837
|
14 |
S A Gordon, R P Weber. (1951). Colorimetric estimation of indoleacetic acid. Plant Physiology, 26( 1): 192– 195
https://doi.org/10.1104/pp.26.1.192
pmid: 16654351
|
15 |
A Karimi, H Khodaverdiloo, M H Rasouli Sadaghiani. (2017). Characterisation of growth and biochemical response of Onopordum acanthium L. under lead stress as affected by microbial inoculation. Chemistry and Ecology, 33( 10): 963– 976
https://doi.org/10.1080/02757540.2017.1391798
|
16 |
A T Koppisch, C C Browder, A L Moe, J T Shelley, B A Kinkel, L E Hersman, S Iyer, C E Ruggiero. (2005). Petrobactin is the primary siderophore synthesized by Bacillus anthracis str. Sterne under conditions of iron starvation. Biometals, 18( 6): 577– 585
https://doi.org/10.1007/s10534-005-1782-6
pmid: 16388397
|
17 |
J Kotaś, Z Stasicka. (2000). Chromium occurrence in the environment and methods of its speciation. Environmental Pollution, 107( 3): 263– 283
https://doi.org/10.1016/S0269-7491(99)00168-2
pmid: 15092973
|
18 |
W C Li, Z H Ye, M H Wong ( 2010). Metal mobilization and production of short-chain organic acids by rhizosphere bacteria associated with a Cd/Zn hyperaccumulating plant, Sedum alfredii. Plant and Soil, 326( 1– 2): 453– 467
https://doi.org/10.1007/s11104-009-0025-y
|
19 |
H Lin, S You, L Liu. (2019). Characterization of microbial communities, identification of Cr(VI) reducing bacteria in constructed wetland and Cr(VI) removal ability of Bacillus cereus. Scientific Reports, 9( 1): 12873
https://doi.org/10.1038/s41598-019-49333-4
pmid: 31492913
|
20 |
J Liu, C Duan, X Zhang, Y Zhu, X Lu. (2011a). Potential of Leersia hexandra Swartz for phytoextraction of Cr from soil. Journal of Hazardous Materials, 188( 1–3): 85– 91
https://doi.org/10.1016/j.jhazmat.2011.01.066
pmid: 21320751
|
21 |
J Liu, C-Q Duan, X-H Zhang, Y-N Zhu, C Hu. (2011b). Characteristics of chromium(III) uptake in hyperaccumulator Leersia hexandra Swartz. Environmental and Experimental Botany, 74 : 122– 126
https://doi.org/10.1016/j.envexpbot.2011.05.008
|
22 |
J Liu, X-H Zhang, S-H You, Q-X Wu, K-N Zhou. (2015). Function of Leersia hexandra Swartz in constructed wetlands for Cr(VI) decontamination: A comparative study of planted and unplanted mesocosms. Ecological Engineering, 81 : 70– 75
https://doi.org/10.1016/j.ecoleng.2015.04.025
|
23 |
S Liu, S Ali, R Yang, J Tao, B Ren. (2019). A newly discovered Cd-hyperaccumulator Lantana camara L. Journal of Hazardous Materials, 371 : 233– 242
https://doi.org/10.1016/j.jhazmat.2019.03.016
pmid: 30852275
|
24 |
S Luo, T Xu, L Chen, J Chen, C Rao, X Xiao, Y Wan, G Zeng, F Long, C Liu, Y Liu. (2012). Endophyte-assisted promotion of biomass production and metal-uptake of energy crop sweet sorghum by plant-growth-promoting endophyte Bacillus sp. SLS18. Applied Microbiology and Biotechnology, 93( 4): 1745– 1753
https://doi.org/10.1007/s00253-011-3483-0
pmid: 21792590
|
25 |
Y Ma, M Rajkumar, C Zhang, H Freitas. (2016). Beneficial role of bacterial endophytes in heavy metal phytoremediation. Journal of Environmental Management, 174 : 14– 25
https://doi.org/10.1016/j.jenvman.2016.02.047
pmid: 26989941
|
26 |
J Mesa-Marín, N F Del-Saz, I D Rodríguez-Llorente, S Redondo-Gómez, E Pajuelo, M Ribas-Carbó, E Mateos-Naranjo. (2018). PGPR reduce root respiration and oxidative stress enhancing Spartina maritima root growth and heavy metal rhizoaccumulation. Frontiers in Plant Science, 9 : 1500
https://doi.org/10.3389/fpls.2018.01500
pmid: 30386359
|
27 |
F Pan, Q Meng, S Luo, J Shen, B Chen, K Y Khan, J Japenga, X Ma, X Yang, Y Feng. (2017). Enhanced Cd extraction of oilseed rape (Brassica napus) by plant growth-promoting bacteria isolated from Cd hyperaccumulator Sedum alfredii Hance. International Journal of Phytoremediation, 19( 3): 281– 289
https://doi.org/10.1080/15226514.2016.1225280
pmid: 27593491
|
28 |
M Rajkumar, N Ae, M N V Prasad, H Freitas. (2010). Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends in Biotechnology, 28( 3): 142– 149
https://doi.org/10.1016/j.tibtech.2009.12.002
pmid: 20044160
|
29 |
M Saeed-Ur-Rahman, N Khalid, S I Hui, K Kayani. (2020). Diversity and versatile functions of metallothioneins produced by plants: a review. Pedosphere, 30( 5): 577– 588
https://doi.org/10.1016/S1002-0160(20)60022-4
|
30 |
B Schwyn, J B Neilands. (1987). Universal chemical assay for the detection and determination of siderophores. Analytical Biochemistry, 160( 1): 47– 56
https://doi.org/10.1016/0003-2697(87)90612-9
pmid: 2952030
|
31 |
J Shim, J W Kim, P J Shea, B T Oh. (2015). IAA production by Bacillus sp. JH 2-2 promotes Indian mustard growth in the presence of hexavalent chromium. Journal of Basic Microbiology, 55( 5): 652– 658
https://doi.org/10.1002/jobm.201400311
pmid: 25283159
|
32 |
S Silambarasan, P Logeswari, P Cornejo, J Abraham, A Valentine. (2019). Simultaneous mitigation of aluminum, salinity and drought stress in Lactuca sativa growth via formulated plant growth promoting Rhodotorula mucilaginosa CAM4. Ecotoxicology and Environmental Safety, 180 : 63– 72
https://doi.org/10.1016/j.ecoenv.2019.05.006
pmid: 31075717
|
33 |
V Sinha, N A Manikandan, K Pakshirajan, R Chaturvedi. (2017). Continuous removal of Cr(VI) from wastewater by phytoextraction using Tradescantia pallida plant based vertical subsurface flow constructed wetland system. International Biodeterioration & Biodegradation, 119 : 96– 103
https://doi.org/10.1016/j.ibiod.2016.10.003
|
34 |
J P Stolt, F E C Sneller, T Bryngelsson, T Lundborg, H Schat. (2003). Phytochelatin and cadmium accumulation in wheat. Environmental and Experimental Botany, 49( 1): 21– 28
https://doi.org/10.1016/S0098-8472(02)00045-X
|
35 |
H Tan, C Wang, G Zeng, Y Luo, H Li, H Xu. (2020). Bioreduction and biosorption of Cr(VI) by a novel Bacillus sp. CRB-B1 strain. Journal of Hazardous Materials, 386 : 121628
https://doi.org/10.1016/j.jhazmat.2019.121628
pmid: 31744729
|
36 |
D Tang, M M Shafer, K Vang, D A Karner, D E Armstrong. (2003). Determination of dissolved thiols using solid-phase extraction and liquid chromatographic determination of fluorescently derivatized thiolic compounds. Journal of Chromatography. A, 998( 1–2): 31– 40
https://doi.org/10.1016/S0021-9673(03)00639-3
pmid: 12862369
|
37 |
K Tawaraya, R Horie, T Wagatsuma, K Saito, A Oikawa. (2018). Metabolite profiling of shoot extract, root extract, and root exudate of rice under nitrogen and phosphorus deficiency. Soil Science and Plant Nutrition, 64( 3): 312– 322
https://doi.org/10.1080/00380768.2018.1476828
|
38 |
J Vacheron, G Desbrosses, M L Bouffaud, B Touraine, Y Moënne-Loccoz, D Muller, L Legendre, F Wisniewski-Dyé, C Prigent-Combaret. (2013). Plant growth-promoting rhizobacteria and root system functioning. Frontiers in Plant Science, 4 : 356
https://doi.org/10.3389/fpls.2013.00356
pmid: 24062756
|
39 |
X Wan, M Lei, T Chen ( 2020). Review on remediation technologies for arsenic-contaminated soil. Frontiers of Environmental Science & Engineering. 14( 2): 24
|
40 |
D Wang, X Zhang, J Liu, Y Zhu, H Zhang, A Zhang, X Jin. (2012). Oxalic acid enhances Cr tolerance in the accumulating plant Leersia hexandra Swartz. International Journal of Phytoremediation, 14( 10): 966– 977
https://doi.org/10.1080/15226514.2011.636406
pmid: 22908658
|
41 |
W Wang, Z Qiu, H Tan, L Cao. (2014). Siderophore production by actinobacteria. Biometals, 27( 4): 623– 631
https://doi.org/10.1007/s10534-014-9739-2
pmid: 24770987
|
42 |
M K Wilson, R J Abergel, K N Raymond, J E L Arceneaux, B R Byers. (2006). Siderophores of Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis. Biochemical and Biophysical Research Communications, 348( 1): 320– 325
https://doi.org/10.1016/j.bbrc.2006.07.055
pmid: 16875672
|
43 |
Y Wu, L Ma, Q Liu, M M Sikder, M Vestergård, K Zhou, Q Wang, X Yang, Y Feng. (2020). Pseudomonas fluorescens promote photosynthesis, carbon fixation and cadmium phytoremediation of hyperaccumulator Sedum alfredii. Science of the Total Environment, 726 : 138554
https://doi.org/10.1016/j.scitotenv.2020.138554
pmid: 32305763
|
44 |
X Xia, S Wu, Z Zhou, G Wang. (2021). Microbial Cd(II) and Cr(VI) resistance mechanisms and application in bioremediation. Journal of Hazardous Materials, 401 : 123685
https://doi.org/10.1016/j.jhazmat.2020.123685
pmid: 33113721
|
45 |
T Yamauchi, T D Colmer, O Pedersen, M Nakazono. (2018). Regulation of root traits for internal aeration and tolerance to soil waterlogging-flooding stress. Plant Physiology, 176( 2): 1118– 1130
https://doi.org/10.1104/pp.17.01157
pmid: 29118247
|
46 |
X Z Yu, Q L Ling, Y H Li, Y J Lin. (2018). mRNA Analysis of genes encoded with phytochelatin synthase (PCs) in rice seedlings exposed to chromium: the role of phytochelatins in Cr detoxification. Bulletin of Environmental Contamination and Toxicology, 101( 2): 257– 261
https://doi.org/10.1007/s00128-018-2362-0
pmid: 29785647
|
47 |
X Zhang, J Liu, D Wang, Y Zhu, C Hu, J Sun. (2009). Bioaccumulation and chemical form of chromium in Leersia hexandra Swartz. Bulletin of Environmental Contamination and Toxicology, 82( 3): 358– 362
https://doi.org/10.1007/s00128-008-9587-2
pmid: 18953472
|
48 |
X H Zhang, J Liu, H T Huang, J Chen, Y N Zhu, D Q Wang. (2007). Chromium accumulation by the hyperaccumulator plant Leersia hexandra Swartz. Chemosphere, 67( 6): 1138– 1143
https://doi.org/10.1016/j.chemosphere.2006.11.014
pmid: 17207838
|
49 |
J Y Zhao, Z H Ye, H Zhong ( 2018). Rice root exudates affect microbial methylmercury production in paddy soils. Environmental Pollution, 242(Pt B): 1921– 1929
https://doi.org/10.1016/j.envpol.2018.07.072
pmid: 30072222
|
50 |
Y Zu, Y Li, H Min, F Zhan, L Qin, J Wang. (2015). Subcellular distribution and chemical form of Pb in hyperaccumulator Arenaria orbiculata and response of root exudates to Pb addition. Frontiers of Environmental Science & Engineering, 9( 2): 250– 258
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|