Chromium phytoextraction and physiological responses of the hyperaccumulator Leersia hexandra Swartz to plant growth-promoting rhizobacterium inoculation

Xuehong Zhang , Yuanyuan Zhang , Dan Zhu , Zhiyi Lin , Na Sun , Chang Su , Hua Lin , Junjian Zheng

Front. Environ. Sci. Eng. ›› 2023, Vol. 17 ›› Issue (1) : 9

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Front. Environ. Sci. Eng. ›› 2023, Vol. 17 ›› Issue (1) : 9 DOI: 10.1007/s11783-023-1609-0
RESEARCH ARTICLE
RESEARCH ARTICLE

Chromium phytoextraction and physiological responses of the hyperaccumulator Leersia hexandra Swartz to plant growth-promoting rhizobacterium inoculation

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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.

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Keywords

Hexavalent chromium / Hyperaccumulator / Rhizobacteria / Leersia hexandra Swartz / Bacillus cereus / Consortia

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Xuehong Zhang, Yuanyuan Zhang, Dan Zhu, Zhiyi Lin, Na Sun, Chang Su, Hua Lin, Junjian Zheng. Chromium phytoextraction and physiological responses of the hyperaccumulator Leersia hexandra Swartz to plant growth-promoting rhizobacterium inoculation. Front. Environ. Sci. Eng., 2023, 17(1): 9 DOI:10.1007/s11783-023-1609-0

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References

[1]

AgarG, TaspinarM S, YildirimE, AydinM, YuceM. (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

[2]

AnfarZ, Ait AhsaineH, ZbairM, AmedlousA, Ait El FakirA, JadaA, El AlemN. (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

[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]

AsadS A, FarooqM, AfzalA, WestH. (2019). Integrated phytobial heavy metal remediation strategies for a sustainable clean environment: a review. Chemosphere, 217 : 925– 941

[5]

BakerA J M, BrooksR R. (1989). Terrestrial higher plants which hyperaccumulate metallic elements - a review of their distribution, ecology and phytochemistry. Biorecovery, 1 : 81– 126

[6]

BanuDoğanlar Z. (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

[7]

Cabello-ConejoM I, Becerra-CastroC, Prieto-FernándezA, MonterrosoC, Saavedra-FerroA, MenchM, KiddP S. (2014). Rhizobacterial inoculants can improve nickel phytoextraction by the hyperaccumulator Alyssum pintodasilvae. Plant and Soil, 379( 1–2): 35– 50

[8]

CendrowskiS, MacArthurW, HannaP. (2004). Bacillus anthracis requires siderophore biosynthesis for growth in macrophages and mouse virulence. Molecular Microbiology, 51( 2): 407– 417

[9]

DasS, MishraJ, DasS K, PandeyS, RaoD S, ChakrabortyA, SudarshanM, DasN, ThatoiH. (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

[10]

DimkpaC O, SvatošA, DabrowskaP, SchmidtA, BolandW, KotheE. (2008). Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere, 74( 1): 19– 25

[11]

DurandA, PiuttiS, RueM, MorelJ L, EchevarriaG, BenizriE. (2016). Improving nickel phytoextraction by co-cropping hyperaccumulator plants inoculated by plant growth promoting rhizobacteria. Plant and Soil, 399( 1–2): 179– 192

[12]

DworkinM, FosterJ W. (1958). Experiments with some microorganisms which utilize ethane and hydrogen. Journal of Bacteriology, 75( 5): 592– 603

[13]

GeJ, WangH, LinJ, TianS, ZhaoJ, LinX, LuL. (2020). Nickel tolerance, translocation and accumulation in a Cd/Zn co-hyperaccumulator plant Sedum alfredii. Journal of Hazardous Materials, 398 : 123074

[14]

GordonS A, WeberR P. (1951). Colorimetric estimation of indoleacetic acid. Plant Physiology, 26( 1): 192– 195

[15]

KarimiA, KhodaverdilooH, Rasouli SadaghianiM H. (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

[16]

KoppischA T, BrowderC C, MoeA L, ShelleyJ T, KinkelB A, HersmanL E, IyerS, RuggieroC E. (2005). Petrobactin is the primary siderophore synthesized by Bacillus anthracis str. Sterne under conditions of iron starvation. Biometals, 18( 6): 577– 585

[17]

KotaśJ, StasickaZ. (2000). Chromium occurrence in the environment and methods of its speciation. Environmental Pollution, 107( 3): 263– 283

[18]

LiW C, YeZ H, WongM H ( 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

[19]

LinH, YouS, LiuL. (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

[20]

LiuJ, DuanC, ZhangX, ZhuY, LuX. (2011a). Potential of Leersia hexandra Swartz for phytoextraction of Cr from soil. Journal of Hazardous Materials, 188( 1–3): 85– 91

[21]

LiuJ, DuanC-Q, ZhangX-H, ZhuY-N, HuC. (2011b). Characteristics of chromium(III) uptake in hyperaccumulator Leersia hexandra Swartz. Environmental and Experimental Botany, 74 : 122– 126

[22]

LiuJ, ZhangX-H, YouS-H, WuQ-X, ZhouK-N. (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

[23]

LiuS, AliS, YangR, TaoJ, RenB. (2019). A newly discovered Cd-hyperaccumulator Lantana camara L. Journal of Hazardous Materials, 371 : 233– 242

[24]

LuoS, XuT, ChenL, ChenJ, RaoC, XiaoX, WanY, ZengG, LongF, LiuC, LiuY. (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

[25]

MaY, RajkumarM, ZhangC, FreitasH. (2016). Beneficial role of bacterial endophytes in heavy metal phytoremediation. Journal of Environmental Management, 174 : 14– 25

[26]

Mesa-MarínJ, Del-SazN F, Rodríguez-LlorenteI D, Redondo-GómezS, PajueloE, Ribas-CarbóM, Mateos-NaranjoE. (2018). PGPR reduce root respiration and oxidative stress enhancing Spartina maritima root growth and heavy metal rhizoaccumulation. Frontiers in Plant Science, 9 : 1500

[27]

PanF, MengQ, LuoS, ShenJ, ChenB, KhanK Y, JapengaJ, MaX, YangX, FengY. (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

[28]

RajkumarM, AeN, PrasadM N V, FreitasH. (2010). Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends in Biotechnology, 28( 3): 142– 149

[29]

Saeed-Ur-RahmanM, KhalidN, HuiS I, KayaniK. (2020). Diversity and versatile functions of metallothioneins produced by plants: a review. Pedosphere, 30( 5): 577– 588

[30]

SchwynB, NeilandsJ B. (1987). Universal chemical assay for the detection and determination of siderophores. Analytical Biochemistry, 160( 1): 47– 56

[31]

ShimJ, KimJ W, SheaP J, OhB T. (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

[32]

SilambarasanS, LogeswariP, CornejoP, AbrahamJ, ValentineA. (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

[33]

SinhaV, ManikandanN A, PakshirajanK, ChaturvediR. (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

[34]

StoltJ P, SnellerF E C, BryngelssonT, LundborgT, SchatH. (2003). Phytochelatin and cadmium accumulation in wheat. Environmental and Experimental Botany, 49( 1): 21– 28

[35]

TanH, WangC, ZengG, LuoY, LiH, XuH. (2020). Bioreduction and biosorption of Cr(VI) by a novel Bacillus sp. CRB-B1 strain. Journal of Hazardous Materials, 386 : 121628

[36]

TangD, ShaferM M, VangK, KarnerD A, ArmstrongD E. (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

[37]

TawarayaK, HorieR, WagatsumaT, SaitoK, OikawaA. (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

[38]

VacheronJ, DesbrossesG, BouffaudM L, TouraineB, Moënne-LoccozY, MullerD, LegendreL, Wisniewski-DyéF, Prigent-CombaretC. (2013). Plant growth-promoting rhizobacteria and root system functioning. Frontiers in Plant Science, 4 : 356

[39]

WanX, Lei M, ChenT ( 2020). Review on remediation technologies for arsenic-contaminated soil. Frontiers of Environmental Science & Engineering. 14( 2): 24

[40]

WangD, ZhangX, LiuJ, ZhuY, ZhangH, ZhangA, JinX. (2012). Oxalic acid enhances Cr tolerance in the accumulating plant Leersia hexandra Swartz. International Journal of Phytoremediation, 14( 10): 966– 977

[41]

WangW, QiuZ, TanH, CaoL. (2014). Siderophore production by actinobacteria. Biometals, 27( 4): 623– 631

[42]

WilsonM K, AbergelR J, RaymondK N, ArceneauxJ E L, ByersB R. (2006). Siderophores of Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis. Biochemical and Biophysical Research Communications, 348( 1): 320– 325

[43]

WuY, MaL, LiuQ, SikderM M, VestergårdM, ZhouK, WangQ, YangX, FengY. (2020). Pseudomonas fluorescens promote photosynthesis, carbon fixation and cadmium phytoremediation of hyperaccumulator Sedum alfredii. Science of the Total Environment, 726 : 138554

[44]

XiaX, WuS, ZhouZ, WangG. (2021). Microbial Cd(II) and Cr(VI) resistance mechanisms and application in bioremediation. Journal of Hazardous Materials, 401 : 123685

[45]

YamauchiT, ColmerT D, PedersenO, NakazonoM. (2018). Regulation of root traits for internal aeration and tolerance to soil waterlogging-flooding stress. Plant Physiology, 176( 2): 1118– 1130

[46]

YuX Z, LingQ L, LiY H, LinY J. (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

[47]

ZhangX, LiuJ, WangD, ZhuY, HuC, SunJ. (2009). Bioaccumulation and chemical form of chromium in Leersia hexandra Swartz. Bulletin of Environmental Contamination and Toxicology, 82( 3): 358– 362

[48]

ZhangX H, LiuJ, HuangH T, ChenJ, ZhuY N, WangD Q. (2007). Chromium accumulation by the hyperaccumulator plant Leersia hexandra Swartz. Chemosphere, 67( 6): 1138– 1143

[49]

ZhaoJ Y, YeZ H, ZhongH ( 2018). Rice root exudates affect microbial methylmercury production in paddy soils. Environmental Pollution, 242(Pt B): 1921– 1929

[50]

ZuY, LiY, MinH, ZhanF, QinL, WangJ. (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

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