Insights into microbe assisted remediation in plants: a brief account on mechanisms and multi-omic strategies against heavy metal toxicity

Abstract

Mercury (Hg), arsenic (As), cadmium (Cd), lead (Pb) and other toxic heavy metals (HM) pose significant risks to the environment, negatively impacting the morpho-physiological and biological traits of plants. At present, toxic elements constitute a significant proportion of the food chain, exerting an impact on human health due to their mobility and biomagnification. The metal exclusion biological technique stands out for its robust performance, even when dealing with extremely low metal concentrations. Its eco-friendly nature and cost-effectiveness further enhance its value. Due to the exponential growth pattern of bacteria, these exhibit high metal persistence and are recommended for metal exclusion processes. Moreover, vacuoles like vesicles present in mycorrhizal fungi can hold extremely high levels of HM. Microbe-assisted phytoremediation primarily occurs through two mechanisms: through the direct provision of the essential nutrients and phytohormones, such as plant growth regulators, siderophores, enzymes, and mineral; or indirectly by modulating the metal detoxification process. This indirect mechanism involves microbes aiding in the accumulation and sequestration of metals in plants through the secretion of specific extracellular substances like organic acids, biosurfactants, and chelators. Moreover, the metal bioavailability and translocation in the rhizosphere are also altered via various mechanisms like acidification, precipitation, complexation or redox reactions. The understanding of the molecular and physiological processes underpinning the functions of arbuscular mycorrhizal fungi (AMF) in reducing HM toxicity, improving plant performance by procuring nutrients under HM-toxicity has significantly improved in recent years. In this review, adaptive and persistent methods related to physiological and cross-protective mechanisms in bacteria and mycorrhizal fungi (MF) resulting from the evolutionary consequences of dealing with HM toxicity have been addressed. Furthermore, the article offers details on the physiological and molecular reactions of host plants with fungi, and bacteria to HM stress, which may be useful for unveiling new knowledge about the strategies of HMs remediation.

References

[] Alavi P, Starcher MR, Zachow C, Müller H, Berg G (2013) Root-microbe systems: the effect and mode of interaction of stress protecting agent (SPA) Stenotrophomonas rhizophila DSM14405T. Front Plant Sci 4:141–153. https://doi.org/10.3389/fpls.2013.00141

[] Albelda-Berenguer M, Monachon M, Joseph E (2019) Siderophores: From natural roles to potential applications. Adv Appl Microbiol 106:193–225. https://doi.org/10.1016/bs.aambs.2018.12.001

[] Al-Dhabaan FA (2019) Morphological, biochemical and molecular identification of petroleum hydrocarbons biodegradation bacteria isolated from oil polluted soil in Dhahran, Saud Arabia. Saudi J Biol Sci 26:1247–1252. https://doi.org/10.1016/j.sjbs.2018.05.029

[] Alexander PD, Alloway BJ, Dourado AM (2006) Genotypic variations in the accumulation of Cd, Cu, Pb and Zn exhibited by six commonly grown vegetables. Environ Pollut 144:736–745. https://doi.org/10.1016/j.envpol.2006.03.001

[] Antoniadis V, Levizou E, Shaheen SM, Ok YS, Sebastian A, Baum C, Prasad MNV, Wenzel WW, Rinklebe J (2017) Trace elements in the soil-plant interface: Phytoavailability, translocation, and phytoremediation–A review. Earth-Science Rev 171:621–645. https://doi.org/10.1016/j.earscirev.2017.06.005

[] Anzano A, Bonanomi G, Mazzoleni S, Lanzotti V (2021) Plant metabolomics in biotic and abiotic stress: a critical overview. Phytochem Rev 19:1–22. https://doi.org/10.1007/s11101-021-09786-w

[] Aqeel M, Ran J, Hu W, Irshad MK, Dong L, Akram MA, Eldesoky GE, Aljuwayid AM, Chuah LF, Deng J (2023) Plant-soil-microbe interactions in maintaining ecosystem stability and coordinated turnover under changing environmental conditions. Chemosphere 318:137–151. https://doi.org/10.1016/j.chemosphere.2023.137924

[] Bensidhoum L, Nabti E, Tabli N, Kupferschmied P, Weiss A, Rothballer M, Schmid M, Keel C, Hartmann A (2016) Heavy metal tolerant Pseudomonas protegens isolates from agricultural well water in northeastern Algeria with plant growth promoting, insecticidal and antifungal activities. Eur J Soil Biol 75:38–46. https://doi.org/10.1016/j.ejsobi.2016.04.006

[] Bilal S, Shahzad R, Khan AL, Al-Harrasi A, Kim CK, Lee I-J (2019) Phytohormones enabled endophytic Penicillium funiculosum LHL06 protects Glycine max L. from synergistic toxicity of heavy metals by hormonal and stress-responsive proteins modulation. J Hazard Mater 379:120–132. https://doi.org/10.1016/j.jhazmat.2019.120824

[] Bilal S, Shahzad R, Khan AL, Kang S-M, Imran QM, Al-Harrasi A, Yun B-W, Lee I-J (2018) Endophytic microbial consortia of phytohormones-producing fungus Paecilomyces formosus LHL10 and bacteria Sphingomonas sp. LK11 to Glycine max L. regulates physio-hormonal changes to attenuate aluminum and zinc stresses. Front Plant Sci 9:127–139. https://doi.org/10.3389/fpls.2018.01273

[] Bilal S, Shahzad R, Lee I-J (2021) Synergistic interaction of fungal endophytes, Paecilomyces formosus LHL10 and Penicillium funiculosum LHL06, in alleviating multi-metal toxicity stress in Glycine max L. Environ Sci Pollut Res 28:67429–67444. https://doi.org/10.3389/fpls.2018.01273

[] Bräutigam A, Gowik U (2010) What can next generation sequencing do for you? Next generation sequencing as a valuable tool in plant research. Plant Biol 12:831–841. https://doi.org/10.1111/j.1438-8677.2010.00373.x

[] Bundy JG, Willey TL, Castell RS, Ellar DJ, Brindle KM (2005) Discrimination of pathogenic clinical isolates and laboratory strains of Bacillus cereus by NMR-based metabolomic profiling. FEMS Microbiol Lett 242:127–136. https://doi.org/10.1016/j.femsle.2004.10.048

[] Cao Y, Zhang X, Deng J, Zhao Q, Xu H (2012) Lead and cadmium-induced oxidative stress impacting mycelial growth of Oudemansiella radicata in liquid medium alleviated by microbial siderophores. World J Microbiol Biotechnol 28:1727–1737. https://doi.org/10.1007/s11274-011-0983-0

[] Chakraborty J, Das S (2014) Biosurfactant-based bioremediation of toxic metals. In: Microbial biodegradation and bioremediation. Elsevier, pp 167–201. https://doi.org/10.1016/B978-0-12-800021-2.00007-8

[] Checcucci A, Bazzicalupo M, Mengoni A (2017) Exploiting nitrogen-fixing rhizobial symbionts genetic resources for improving phytoremediation of contaminated soils. In: Enhancing Cleanup Environmental Pollution. Springer, pp 275–288. https://doi.org/10.1007/978-3-319-55426-6_13

[] Chen L, Luo S, Xiao X, Guo H, Chen J, Wan Y, Li B, Xu T, Xi Q, Rao C (2010) Application of plant growth-promoting endophytes (PGPE) isolated from Solanum nigrum L. for phytoextraction of Cd-polluted soils. Appl Soil Ecol 46:383–389. https://doi.org/10.1016/j.apsoil.2010.10.003

[] Chen Y, Yang W, Chao Y, Wang S, Tang Y-T, Qiu R-L (2017) Metal-tolerant Enterobacter sp. strain EG16 enhanced phytoremediation using Hibiscus cannabinus via siderophore-mediated plant growth promotion under metal contamination. Plant Soil 413:203–216. https://doi.org/10.1007/s11104-016-3091-y

[] Curaba J, Singh MB, Bhalla PL (2014) miRNAs in the crosstalk between phytohormone signalling pathways. J Exp Bot 65:1425–1438. https://doi.org/10.1093/jxb/eru002

[] De Castro AP, Sartori da Silva MR, Quirino BF, Kruger RH (2013) Combining" omics" strategies to analyze the biotechnological potential of complex microbial environments. Curr Protein Pept Sci 14:447–458. https://doi.org/10.2174/13892037113149990062

[] Defez R, Esposito R, Angelini C, Bianco C (2016) Overproduction of indole-3-acetic acid in free-living rhizobia induces transcriptional changes resembling those occurring in nodule bacteroid. Mol Plant-Microbe Interact 29:484–495. https://doi.org/10.1094/mpmi-01-16-0010-r

[] Deng Z, Wang W, Tan H, Cao L (2012) Characterization of heavy metal-resistant endophytic yeast Cryptococcus sp. CBSB78 from rapes (Brassica chinensis) and its potential in promoting the growth of Brassica spp. in metal-contaminated soils. Water, Air, Soil Pollut 223:5321–5329. https://doi.org/10.1007/s11270-012-1282-6

[] Devi R, Kaur T, Kour D, Hricovec M, Mohan R, Yadav N, Rai PK, Rai AK, Yadav A, Kumar M, Yadav AN (2022) Microbes-mediated alleviation of heavy metal stress in crops: Current research and future challenges. J Appl Biol Biotechnol 10:25–37. https://doi.org/10.7324/jabb.2022.10s203

[] Dighton J, White JF (2005) Fungal activity as determined by microscale methods with special emphasis on interactions with heavy metals. In: The fungal community. CRC Press, pp 307–326. https://doi.org/10.1201/9781420027891.sec2

[] Dutta P, Karmakar A, Majumdar S, Roy S (2018) Klebsiella pneumoniae (HR1) assisted alleviation of Cd (II) toxicity in Vigna mungo: a case study of biosorption of heavy metal by an endophytic bacterium coupled with plant growth promotion. Euro-Mediterranean J Environ Integr 3:1–10. https://doi.org/10.1007/s41207-018-0069-6

[] El-Maraghy SS, Tohamy TA, Hussein KA (2020) Expression of SidD gene and physiological characterization of the rhizosphere plant growth-promoting yeasts. Heliyon 6:324–336. https://doi.org/10.1016/j.heliyon.2020.e04384

[] Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015:1–18. https://doi.org/10.1155/2015/756120

[] Franke S, Grass G, Nies RC, DH, (2003) Molecular analysis of the copper transporting efflux system CusCFBA of Escherichia coli. J Bacteriol 185:3804–3812. https://doi.org/10.1128/jb.185.13.3804-3812.2003

[] Gaonkar T, Bhosle S (2013) Effect of metals on a siderophore producing bacterial isolate and its implications on microbial assisted bioremediation of metal contaminated soils. Chemosphere 93:1835–1843. https://doi.org/10.1016/j.chemosphere.2013.06.036

[] Ghosh S, Kamble NU, Verma P, Salvi P, Petla BP, Roy S, Rao V, Hazra A, Varshney V, Kaur H (2020a) Arabidopsis protein l-isoaspartyl methyltransferase repairs isoaspartyl damage to antioxidant enzymes and increases heat and oxidative stress tolerance. J Biol Chem 295:783–799. https://doi.org/10.1074/jbc.ra119.010779

[] Ghosh SK, Bera T, Chakrabarty AM (2020b) Microbial siderophore–A boon to agricultural sciences. Biol Control 144:104–114. https://doi.org/10.1016/j.biocontrol.2020.104214

[] Gnanamani A, Kavitha V, Radhakrishnan N, Rajakumar GS, Sekaran G, Mandal AB (2010) Microbial products (biosurfactant and extracellular chromate reductase) of marine microorganism are the potential agents reduce the oxidative stress induced by toxic heavy metals. Colloids Surfaces B Biointerfaces 79:334–339. https://doi.org/10.1016/j.colsurfb.2010.04.007

[] Gomaa EZ, El-Meihy RM (2019) Bacterial biosurfactant from Citrobacter freundii MG812314. 1 as a bioremoval tool of heavy metals from wastewater. Bull Natl Res Cent 43:1–14. https://doi.org/10.1186/s42269-019-0088-8

[] Gravel V, Antoun H, Tweddell RJ (2007) Growth stimulation and fruit yield improvement of greenhouse tomato plants by inoculation with Pseudomonas putida or Trichoderma atroviride: possible role of indole acetic acid (IAA). Soil Biol Biochem 39:1968–1977. https://doi.org/10.1016/j.soilbio.2007.02.015

[] Grichko VP, Glick BR (2001) Amelioration of flooding stress by ACC deaminase-containingplant growth-promoting bacteria. Plant Physiol Biochem 39:11–17. https://doi.org/10.1016/S0981-9428(00)01212-2

[] Gu Y-G, Lin Q, Gao Y-P (2016) Metals in exposed-lawn soils from 18 urban parks and its human health implications in southern China’s largest city, Guangzhou. J Clean Prod 115:122–129. https://doi.org/10.1016/j.jclepro.2015.12.031

[] Gube M (2016) 4 Fungal molecular response to heavy metal stress. In: Hoffmeister, D. (eds) The Mycota, vol III. Springer, Cham. Biochem Mol Biol 3:47–68. https://doi.org/10.1007/978-3-319-27790-5_4

[] Guo B, Peng Z, Han F, Shan X, Lin J (2007) Study of low-molecular weight organic acids in maize roots under the stress of cadmium using capillary zone electrophoresis. J Sep Sci 30:2742–2747. https://doi.org/10.1002/jssc.200700207

[] Gupta P, Diwan B (2017) Bacterial exopolysaccharide mediated heavy metal removal: a review on biosynthesis, mechanism and remediation strategies. Biotechnol Reports 13:58–71. https://doi.org/10.1016/j.btre.2016.12.006

[] Han H, Zhang H, Qin S, Zhang J, Yao L, Chen Z, Yang J (2021) Mechanisms of Enterobacter bugandensis TJ6 immobilization of heavy metals and inhibition of Cd and Pb uptake by wheat based on metabolomics and proteomics. Chemosphere 276:130–147. https://doi.org/10.1016/j.chemosphere.2021.130157

[] Hao X, Zhu J, Rensing C, Liu Y, Gao S, Chen W, Huang Q, Liu Y-R (2021) Recent advances in exploring the heavy metal (loid) resistant microbiome. Comput Struct Biotechnol J 19:94–109. https://doi.org/10.1016/j.csbj.2020.12.006

[] Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad AJP (2012) Behavior. Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466. https://doi.org/10.4161/psb.21949

[] He H, Ye Z, Yang D, Yan J, Xiao L, Zhong T, Yuan M, Cai X, Fang Z, Jing Y (2013) Characterization of endophytic Rahnella sp. JN6 from Polygonum pubescens and its potential in promoting growth and Cd, Pb. Zn Uptake by Brassica Napus Chemosphere 90:1960–1965. https://doi.org/10.1016/j.chemosphere.2012.10.057

[] Hu B, Jia X, Hu J, Xu D, Xia F, Li Y (2017) Assessment of heavy metal pollution and health risks in the soil-plant-human system in the Yangtze River Delta, China. Int J Environ Res Public Health 14:10–25. https://doi.org/10.3390/ijerph14091042

[] Husna, Hussain A, Shah M, Hamayun M, Iqbal A, Qadir M, Alataway A, Dewidar AZ, Elansary HO, Lee IJ (2023) Phytohormones producing rhizobacteria alleviate heavy metals stress in soybean through multilayered response. Microbiol Res 266:1–14. https://doi.org/10.1016/j.micres.2022.127237

[] Ikram M, Ali N, Jan G, Jan FG, Rahman IU, Iqbal A, Hamayun M (2018) IAA producing fungal endophyte Penicillium roqueforti Thom., enhances stress tolerance and nutrients uptake in wheat plants grown on heavy metal contaminated soils. PLoS ONE 13:208–223. https://doi.org/10.1371/journal.pone.0208150

[] Islam F, Yasmeen T, Ali Q, Ali S, Arif MS, Hussain S, Rizvi H (2014) Influence of Pseudomonas aeruginosa as PGPR on oxidative stress tolerance in wheat under Zn stress. Ecotoxicol Environ Saf 104:285–293. https://doi.org/10.1016/j.ecoenv.2014.03.008

[] Ji L, Zhang W, Yu D, Cao Y, Xu H (2012) Effect of heavy metal-solubilizing microorganisms on zinc and cadmium extractions from heavy metal contaminated soil with Tricholoma lobynsis. World J Microbiol Biotechnol 28:293–301. https://doi.org/10.1007/s11274-011-0819-y

[] Jian L, Bai X, Zhang H, Song X, Li Z (2019) Promotion of growth and metal accumulation of alfalfa by coinoculation with Sinorhizobium and Agrobacterium under copper and zinc stress. Peer J 7:68–79. https://doi.org/10.7717/peerj.6875

[] Jing YX, Yan JL, He HD, Yang DJ, Xiao L, Zhong T, Yuan M, De CX, Bin LS (2014) Characterization of bacteria in the rhizosphere soils of Polygonum pubescens and their potential in promoting growth and Cd, Pb, Zn uptake by Brassica napus. Int J Phytoremediation 16:321–333. https://doi.org/10.1080/15226514.2013.773283

[] Johnson DB (2018) The evolution, current status, and future prospects of using biotechnologies in the mineral extraction and metal recovery sectors. Minerals 8:34–43. https://doi.org/10.3390/min8080343

[] Joshi PM, Juwarkar AA (2009) In vivo studies to elucidate the role of extracellular polymeric substances from Azotobacter in immobilization of heavy metals. Environ Sci Technol 43:5884–5889. https://doi.org/10.1021/es900063b

[] Juwarkar AA, Nair A, Dubey KV, Singh SK, Devotta S (2007) Biosurfactant technology for remediation of cadmium and lead contaminated soils. Chemosphere 68:1996–2002. https://doi.org/10.1016/j.chemosphere.2007.02.027

[] Kaewdoung B, Sutjaritvorakul T, Gadd GM, Whalley AJS, Sihanonth P (2016) Heavy metal tolerance and biotransformation of toxic metal compounds by new isolates of wood-rotting fungi from Thailand. Geo Microbiol J 33:283–288. https://doi.org/10.1080/01490451.2015.1048394

[] Kang S-M, Waqas M, Hamayun M, Asaf S, Khan AL, Kim A-Y, Park Y-G, Lee I-J (2017) Gibberellins and indole-3-acetic acid producing rhizospheric bacterium Leifsonia xyli SE134 mitigates the adverse effects of copper-mediated stress on tomato. J Plant Interact 12:373–380. https://doi.org/10.1080/17429145.2017.1370142

[] Kantar M, Lucas SJ, Budak H (2011) miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233:471–484. https://doi.org/10.1007/s00425-010-1309-4

[] Karaouzas I, Kapetanaki N, Mentzafou A, Kanellopoulos TD, Skoulikidis N (2021) Heavy metal contamination status in Greek surface waters: A review with application and evaluation of pollution indices. Chemosphere 263:128–131. https://doi.org/10.1016/j.chemosphere.2020.128192

[] Kaushal M, Wani SP (2016) Rhizobacterial-plant interactions: strategies ensuring plant growth promotion under drought and salinity stress. Agric Ecosys Environ 231:68–78. https://doi.org/10.1016/j.agee.2016.06.031

[] Khan A, Singh P, Srivastava A (2018) Synthesis, nature and utility of universal iron chelator–Siderophore: A review. Microbiol Res 212:103–111. https://doi.org/10.1016/j.micres.2017.10.012

[] Kubicek CP, Herrera-Estrella A, Seidl-Seiboth V, Martinez DA, Druzhinina IS, Thon M, Zeilinger S, Casas-Flores S, Horwitz BA, Mukherjee PK (2011) Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol 12:1–15. https://doi.org/10.1186/gb-2011-12-4-r40

[] Kuffner M, De Maria S, Puschenreiter M, Fallmann K, Wieshammer G, Gorfer M, Strauss J, Rivelli AR, Sessitsch A (2010) Culturable bacteria from Zn-and Cd-accumulating Salix caprea with differential effects on plant growth and heavy metal availability. J Appl Microbiol 108:1471–1484. https://doi.org/10.1111/j.1365-2672.2010.04670.x

[] Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJJ (2004) Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant-Microbe Interact 17:6–15. https://doi.org/10.1094/mpmi.2004.17.1.6

[] Kumar A, Yadav AN, Mondal R, Kour D, Subrahmanyam G, Shabnam AA, Khan SA, Yadav KK, Sharma GK, Cabral-Pinto M (2021) Myco-remediation: A mechanistic understanding of contaminants alleviation from natural environment and future prospect. Chemosphere 284:131–145. https://doi.org/10.1016/j.chemosphere.2021.131325

[] Li Y, Zheng Y, Addo-Quaye C, Zhang L, Saini A, Jagadeeswaran G, Axtell MJ, Zhang W, Sunkar R (2010) Transcriptome-wide identification of microRNA targets in rice. Plant J 62:742–759. https://doi.org/10.1111/j.1365-313x.2010.04187.x

[] Li K, Pidatala VR, Shaik R, Datta R, Ramakrishna W (2014) Integrated metabolomic and proteomic approaches dissect the effect of metal-resistant bacteria on maize biomass and copper uptake. Environ Sci Technol 48:1184–1193. https://doi.org/10.1021/es4047395

[] Li JL, Cui J, Cheng DY (2015) Computational identification and characterization of conserved miRNAs and their target genes in beet (Beta vulgaris). Genet Mol Res 14:9103–9108. https://doi.org/10.4238/2015.august.7.19

[] Li S, Hu S, Shi S, Ren L, Yan W, Zhao H (2019) Microbial diversity and metaproteomic analysis of activated sludge responses to naphthalene and anthracene exposure. RSC Adv 9:22841–22852. https://doi.org/10.1039/c9ra04674g

[] Li C, Wang H, Liao X, Xiao R, Liu K, Bai J, Li B, He Q (2022) Heavy metal pollution in coastal wetlands: A systematic review of studies globally over the past three decades. J Hazard Mater 424:127–143. https://doi.org/10.1016/j.jhazmat.2021.127312

[] Li W, Chen K, Li Q, Tang Y, Jiang Y, Su Y (2023) Effects of arbuscular mycorrhizal fungi on alleviating cadmium stress in Medicago truncatula gaertn. Plants 12:547–561. https://doi.org/10.3390/plants12030547

[] Lima JC, Arenhart RA, Margis-Pinheiro M, Margis R (2011) Aluminum triggers broad changes in microRNA expression in rice roots. Genet Mol Res 10:2817–2832. https://doi.org/10.4238/2011.november.10.4

[] Mahurpawar M (2015) Effects of heavy metals on human health. Int J Res Granthaalayah 530:1–7. https://doi.org/10.29121/granthaalayah.v3.i9SE.2015.3282

[] Martin S, Griswold W. Human health effects of heavy metals Environ Sci Technol Briefs Citizens, 2009, 15: 429-442

[] Mattarozzi M, Manfredi M, Montanini B, Gosetti F, Sanangelantoni AM, Marengo E, Careri M, Visioli G (2017) A metaproteomic approach dissecting major bacterial functions in the rhizosphere of plants living in serpentine soil. Anal Bioanal Chem 409:2327–2339. https://doi.org/10.1007/s00216-016-0175-8

[] Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530. https://doi.org/10.1016/j.plantsci.2003.10.025

[] Mei X, Wang Y, Li Z, Larousse M, Pere A, da Rocha M, Zhan F, He Y, Pu L, Panabières F (2022) Root-associated microbiota drive phytoremediation strategies to lead of Sonchus Asper (L.) Hill as revealed by intercropping-induced modifications of the rhizosphere microbiome. Environ Sci Pollut Res 29:23026–23040. https://doi.org/10.1007/s11356-021-17353-1

[] Miller GAD, Suzuki N, Ciftci-Yilmaz S, Mittler RON (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467. https://doi.org/10.1111/j.1365-3040.2009.02041.x

[] Mishra J, Singh R, Arora NK (2017) Alleviation of heavy metal stress in plants and remediation of soil by rhizosphere microorganisms. Front Microbiol 8:170–186. https://doi.org/10.3389/fmicb.2017.01706

[] Mohammadabadi SI, Javanbakht V (2020) Ultrasonic assisted hydrolysis of barley straw biowastes into construction of a novel hemicellulose-based adsorbent and its adsorption properties for Pb²⁺ ions from aqueous solutions. Renew Energy 161:893–906. https://doi.org/10.1016/j.renene.2020.07.021

[] Mohammadi AA, Zarei A, Esmaeilzadeh M, Taghavi M, Yousefi M, Yousefi Z, Sedighi F, Javan S (2020) Assessment of heavy metal pollution and human health risks assessment in soils around an industrial zone in Neyshabur. Iran Biol Trace Elem Res 195:343–352. https://doi.org/10.1007/s12011-019-01816-1

[] Narendrula-Kotha R, Nkongolo KK (2017) Microbial response to soil liming of damaged ecosystems revealed by pyrosequencing and phospholipid fatty acid analyses. PLoS ONE 12:168–187. https://doi.org/10.1371/journal.pone.0168497

[] Neshat M, Abbasi A, Hosseinzadeh A, Sarikhani MR, Dadashi Chavan D, Rasoulnia A (2022) Plant growth promoting bacteria (PGPR) induce antioxidant tolerance against salinity stress through biochemical and physiological mechanisms. Physiol Mol Biol Plants 28:347–361. https://doi.org/10.1007/s12298-022-01128-0

[] Nies DH, Nies A, Chu L, Silver S (1989) Expression and nucleotide sequence of a plasmid-determined divalent cation efflux system from Alcaligenes eutrophus. Proc Natl Acad Sci U S A 86:7351–7355. https://doi.org/10.1073/pnas.86.19.7351

[] Nikolic B, Schwab H, Sessitsch A (2011) Metagenomic analysis of the 1-aminocyclopropane-1-carboxylate deaminase gene (acdS) operon of an uncultured bacterial endophyte colonizing Solanum tuberosum L. Arch Microbiol 193:665–676. https://doi.org/10.1007/s00203-011-0703-z

[] Niu X, Wang S, Zhou J, Di D, Sun P, Huang D (2021) Inoculation with indigenous rhizosphere microbes enhances aboveground accumulation of lead in Salix integra Thunb. by improving transport coefficients. Front Microbiol 12:686–702. https://doi.org/10.3389/fmicb.2021.686812

[] Nosrati R, Dehghani S, Karimi B, Yousefi M, Taghdisi SM, Abnous K, Alibolandi M, Ramezani M (2018) Siderophore-based biosensors and nanosensors; new approach on the development of diagnostic systems. Biosens Bioelectron 117:1–14. https://doi.org/10.1016/j.bios.2018.05.057

[] Ortiz J, Soto J, Almonacid L, Fuentes A, Campos-Vargas R, Arriagada C (2019) Alleviation of metal stress by Pseudomonas orientalis and Chaetomium cupreum strains and their effects on Eucalyptus globulus growth promotion. Plant Soil 436:449–461. https://doi.org/10.1007/s11104-019-03946-w

[] Pacheco GJ, Ciapina EMP, de Gomes E, B, Pereira Junior N, (2010) Biosurfactant production by Rhodococcus erythropolis and its application to oil removal. Brazilian J Microbiol 41:685–693. https://doi.org/10.1590/s1517-83822010000300019

[] Pacwa-Płociniczak M, Płaza GA, Piotrowska-Seget Z, Cameotra SS (2011) Environmental applications of biosurfactants: recent advances. Int J Mol Sci 12:633–654. https://doi.org/10.3390/ijms12010633

[] Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15. https://doi.org/10.1034/j.1399-3054.2003.00086.x

[] Peterson E, Kaur P (2018) Antibiotic resistance mechanisms in bacteria: relationships between resistance determinants of antibiotic producers, environmental bacteria, and clinical pathogens. Front Microbio 9:426686. https://doi.org/10.3389/fmicb.2018.02928

[] Pinter IF, Salomon MV, Berli F, Bottini R, Piccoli P (2017) Characterization of the As (III) tolerance conferred by plant growth promoting rhizobacteria to in vitro-grown grapevine. Appl Soil Ecol 109:60–68. https://doi.org/10.1016/j.apsoil.2016.10.003

[] Pires C, Franco AR, Pereira SIA, Henriques I, Correia A, Magan N, Castro PML (2017) Metal (loid)-contaminated soils as a source of culturable heterotrophic aerobic bacteria for remediation applications. Geo Microbiol J 34:760–768. https://doi.org/10.1080/01490451.2016.1261968

[] Poole K (2007) Efflux pumps as antimicrobial resistance mechanisms. Ann Med 39:162–176. https://doi.org/10.1080/07853890701195262

[] Priya P, Aneesh B, Sivakumar KC, Harikrishnan K (2022) Comparative proteomic analysis of saline tolerant, phosphate solubilizing endophytic Pantoea sp., and Pseudomonas sp. isolated from Eichhornia rhizosphere. Microbiol Res 265:127–141. https://doi.org/10.1016/j.micres.2022.127217

[] Qadir M, Hussain A, Hamayun M, Shah M, Iqbal A, Murad W (2020) Phytohormones producing rhizobacterium alleviates chromium toxicity in Helianthus annuus L. by reducing chromate uptake and strengthening antioxidant system. Chemosphere 258:127–143. https://doi.org/10.1016/j.chemosphere.2020.127386

[] Rai PK, Singh M, Anand K, Saurabh S, Kaur T, Kour D, Yadav AN, Kumar M (2020) Role and potential applications of plant growth-promoting rhizobacteria for sustainable agriculture. In: New and future developments in microbial biotechnology and bioengineering. Elsevier, pp 49–60. https://doi.org/10.1016/B978-0-12-820526-6.00004-X

[] Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149. https://doi.org/10.1016/j.tibtech.2009.12.002

[] Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574. https://doi.org/10.1016/j.biotechadv.2012.04.011

[] Ratan S, Bhawana P, Fulekar MH. Characterization of PGP traits by heavy metals tolerant Pseudomonas putida and Bacillus safensis strain isolated from rhizospheric zone of weed (Phyllanthus urinaria) and its efficiency in Cd and Pb removal Int J Curr Microbiol Appl Sci, 2015, 4: 954-975

[] Rawat R, Tewari L (2011) Effect of abiotic stress on phosphate solubilization by biocontrol fungus Trichoderma sp. Curr Microbiol 62:1521–1526. https://doi.org/10.1007/s00284-011-9888-2

[] Riaz M, Kamran M, Fang Y, Wang Q, Cao H, Yang G, Deng L, Wang Y, Zhou Y, Anastopoulos I (2021) Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: A critical review. J Hazard Mater 402:123–138. https://doi.org/10.1016/j.jhazmat.2020.123919

[] Rizvi A, Ahmed B, Khan MS, Rajput VD, Umar S, Minkina T, Lee J (2022) Maize associated bacterial microbiome linked mitigation of heavy metal stress: a multidimensional detoxification approach. Environ Exp Bot 200:104–121. https://doi.org/10.1016/j.envexpbot.2022.104911

[] Rojas-Tapias DF, Bonilla R, Dussán J (2014) Effect of inoculation and co-inoculation of Acinetobacter sp. RG30 and Pseudomonas putida GN04 on growth, fitness, and copper accumulation of maize (Zea mays). Water, Air, Soil Pollut 225:1–13. https://doi.org/10.1007/s11270-014-2232-2

[] Rosen BP (2002) Biochemistry of arsenic detoxification. FEBS Lett 529:86–92. https://doi.org/10.1016/s0014-5793(02)03186-1

[] Rufino RD, Luna JM, Campos-Takaki GM, Ferreira SR, Sarubbo LA (2012) Application of the biosurfactant produced by Candida lipolytica in the remediation of heavy metals. Chem Eng 27:61–66. https://doi.org/10.3303/CET1227011

[] Santona L, Castaldi P, Melis P (2006) Evaluation of the interaction mechanisms between red muds and heavy metals. J Hazard Mater 136:324–329. https://doi.org/10.1016/j.jhazmat.2005.12.022

[] Sarkodie EK, Jiang L, Li K, Yang J, Guo Z, Shi J, Deng Y, Liu H, Jiang H, Liang Y (2022) A review on the bioleaching of toxic metal (loid) s from contaminated soil: Insight into the mechanism of action and the role of influencing factors. Front Microbiol 13:104–117. https://doi.org/10.3389/fmicb.2022.1049277

[] Saxena G, Purchase D, Mulla SI, Saratale GD, Bharagava RN (2020) Phytoremediation of heavy metal-contaminated sites: eco-environmental concerns, field studies, sustainability issues, and future prospects. Rev Environ Contam Toxicol 249:71–131. https://doi.org/10.1007/398_2019_24

[] Schütze E, Ahmed E, Voit A, Klose M, Greyer M, Svatoš A, Merten D, Roth M, Holmström SJM, Kothe E (2015) Siderophore production by streptomycetes—stability and alteration of ferrihydroxamates in heavy metal-contaminated soil. Environ Sci Pollut Res 22:19376–19383. https://doi.org/10.1007/s11356-014-3842-3

[] Schwabe R, Senges CHR, Bandow JE, Heine T, Lehmann H, Wiche O, Schlömann M, Levicán G, Tischler D (2020) Cultivation dependent formation of siderophores by Gordonia rubripertincta CWB2. Microbiol Res 238:126–148. https://doi.org/10.1016/j.micres.2020.126481

[] Seneviratne M, Vithanage M. The role of siderophores on plants under heavy meal stress: a view from the rhizosphere Res Rev: J Bot Sci, 2015, 2: 617-630

[] Seneviratne M, Seneviratne G, Madawala H, Vithanage M (2017) Role of rhizospheric microbes in heavy metal uptake by plants. Agro-Environmental Sustain 2:147–163. https://doi.org/10.1007/978-3-319-49727-3_8

[] Sepehri M, Khatabi B (2021) Combination of siderophore-producing bacteria and Piriformospora indica provides an efficient approach to improve cadmium tolerance in alfalfa. Microb Ecol 81:717–730. https://doi.org/10.1007/s00248-020-01629-z

[] Shilev S, Babrikova I, Babrikov T (2020) Consortium of plant growth-promoting bacteria improves spinach (Spinacea oleracea L.) growth under heavy metal stress conditions. J Chem Technol Biotechnol 95:932–939. https://doi.org/10.1002/JCTB.6077

[] Shreya D, Jinal HN, Kartik VP, Amaresan N (2020) Amelioration effect of chromium-tolerant bacteria on growth, physiological properties and chromium mobilization in chickpea (Cicer arietinum) under chromium stress. Arch Microbiol 202:887–894. https://doi.org/10.1007/s00203-019-01801-1

[] Siddiqua A, Hahladakis JN, Al-Attiya WAKA (2022) An overview of the environmental pollution and health effects associated with waste landfilling and open dumping. Environ Sci Pollut Res 29:58514–58536. https://doi.org/10.1007/s11356-022-21578-z

[] Silva-Sanchez C, Li H, Chen S (2015) Recent advances and challenges in plant phosphoproteomics. Proteomics 15:1127–1141. https://doi.org/10.1002/pmic.201400410

[] Singh AK, Cameotra SS (2013) Efficiency of lipopeptide biosurfactants in removal of petroleum hydrocarbons and heavy metals from contaminated soil. Environ Sci Pollut Res 20:7367–7376. https://doi.org/10.1007/s11356-013-1752-4

[] Singh N, Gaddam SR, Singh D, Trivedi PK (2021) Regulation of arsenic stress response by ethylene biosynthesis and signaling in Arabidopsis thaliana. Environ Exp Bot 185:104–118. https://doi.org/10.1016/j.envexpbot.2021.104408

[] Smolders E, Oorts K, Van Sprang P, Schoeters I, Janssen CR, McGrath SP, McLaughlin MJ (2009) Toxicity of trace metals in soil as affected by soil type and aging after contamination: using calibrated bioavailability models to set ecological soil standards. Environ Toxicol Che 28:1633–1642. https://doi.org/10.1897/08-592.1

[] Sriram MI, Gayathiri S, Gnanaselvi U, Jenifer PS, Raj SM, Gurunathan S (2011) Novel lipopeptide biosurfactant produced by hydrocarbon degrading and heavy metal tolerant bacterium Escherichia fergusonii KLU01 as a potential tool for bioremediation. Bioresource Technol 102:9291–9295. https://doi.org/10.1016/j.biortech.2011.06.094

[] Sukweenadhi J, Kim Y-J, Choi E-S, Koh S-C, Lee S-W, Kim Y-J, Yang DC (2015) Paenibacillus yonginensis DCY84T induces changes in Arabidopsis thaliana gene expression against aluminum, drought, and salt stress. Microbiol Res 172:7–15. https://doi.org/10.1016/j.micres.2015.01.007

[] Sun J, Deng Z, Yan A (2014) Bacterial multidrug efflux pumps: mechanisms, physiology and pharmacological exploitations. BBRC 453:254–267. https://doi.org/10.1016/j.bbrc.2014.05.090

[] Sytar O, Kumar A, Latowski D, Kuczynska P, Strzałka K, Prasad MNV (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35:985–999. https://doi.org/10.1007/s11738-012-1169-6

[] Tiwari G, Duraivadivel P, Sharma S, Hariprasad P (2018) 1-Aminocyclopropane-1-carboxylic acid deaminase producing beneficial rhizobacteria ameliorate the biomass characters of Panicum maximum Jacq. by mitigating drought and salt stress. Sci Rep 8(1):17513. https://doi.org/10.1038/s41598-018-35565-3

[] Trivedi P, Batista BD, Bazany KE, Singh BK (2022) Plant–microbiome interactions under a changing world: Responses, consequences and perspectives. New Phytol 234:1951–1959. https://doi.org/10.1111/nph.18016

[] Turner TR, Ramakrishnan K, Walshaw J, Heavens D, Alston M, Swarbreck D, Osbourn A, Grant A, Poole PS (2013) Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J 7:2248–2258. https://doi.org/10.1038/ismej.2013.119

[] Venkatesh NM, Vedaraman N (2012) Remediation of soil contaminated with copper using rhamnolipids produced from Pseudomonas aeruginosa MTCC 2297 using waste frying rice bran oil. Ann Microbiol 62:85–91. https://doi.org/10.1007/s13213-011-0230-9

[] Violante AUDN, Cozzolino VUDN, Perelomov LPSU, Caporale AG, Pigna MUDN (2010) Mobility and bioavailability of heavy metals and metalloids in soil environments. J Soil Science Plant Nut 10:268–292. https://doi.org/10.4067/S0718-95162010000100005

[] Wang A, Fu W, Feng Y, Liu Z, Song D (2022) Synergetic effects of microbial-phytoremediation reshape microbial communities and improve degradation of petroleum contaminants. J Hazard Mater 429:128–140. https://doi.org/10.1016/j.jhazmat.2022.128396

[] Wani PA, Rafi N, Wani U, Bilikis AH, Khan MSA (2023) Simultaneous bioremediation of heavy metals and biodegradation of hydrocarbons by metal resistant Brevibacillus parabrevis OZF5 improves plant growth promotion. Bioremediat J 27:20–31. https://doi.org/10.1080/10889868.2021.1989371

[] Wei X, Fang L, Cai P, Huang Q, Chen H, Liang W, Rong X (2011) Influence of extracellular polymeric substances (EPS) on Cd adsorption by bacteria. Environ Pollut 159:1369–1374. https://doi.org/10.1016/j.envpol.2011.01.006

[] Wingender J, Neu TR, Flemming H-C (1999) What are bacterial extracellular polymeric substances? Microbial Extracellular Polymeric Substances. Springer, Berlin Heidelberg, pp 1–19. https://doi.org/10.1007/978-3-642-60147-7_1

[] Wishart DS (2019) Metabolomics for investigating physiological and pathophysiological processes. Physiol Rev 99:1819–1875. https://doi.org/10.1152/physrev.00035.2018

[] Właśniewski S, Hajduk E (2012) The accumulation of cadmium in soils and selected vegetables cultivated in the allotment gardens of Rzeszów. Soil Sci Ann 63:55–60. https://doi.org/10.2478/v10239-012-0013-4

[] Xiang M, Li Y, Yang J, Lei K, Li Y, Li F, Zheng D, Fang X, Cao Y (2021) Heavy metal contamination risk assessment and correlation analysis of heavy metal contents in soil and crops. Environ Pollut 278:116–127. https://doi.org/10.1016/j.envpol.2021.116911

[] Xu X, Huang Q, Huang Q, Chen W (2012a) Soil microbial augmentation by an EGFP-tagged Pseudomonas putida X4 to reduce phytoavailable cadmium. Int Biodeter Biodegr 71:55–60. https://doi.org/10.1016/j.ibiod.2012.03.006

[] Xu Y, Lu Y, Xie C, Gao S, Wan J, Prasanna BM (2012b) Whole-genome strategies for marker-assisted plant breeding. Mol Breed 29:833–854. https://doi.org/10.1007/s11032-012-9699-6

[] Yadav AN (2021) Microbial biotechnology for bio-prospecting of microbial bioactive compounds and secondary metabolites. J Appl Biol Biotechnol 9:1–6. https://doi.org/10.7324/JABB.2021.92ed

[] Yadav AN, Sharma D, Gulati S, Singh S, Dey R, Pal KK, Kaushik R, Saxena AK (2015) Haloarchaea endowed with phosphorus solubilization attribute implicated in phosphorus cycle. Sci Rep 5:122–139. https://doi.org/10.1038/srep12293

[] Zhang Y, He L, Chen Z, Wang Q, Qian M, Sheng X (2011a) Characterization of ACC deaminase-producing endophytic bacteria isolated from copper-tolerant plants and their potential in promoting the growth and copper accumulation of Brassica napus. Chemosphere 83:57–62. https://doi.org/10.1016/j.enconman.2017.02.022

[] Zhang Y, He L, Chen Z, Zhang W, Wang Q, Qian M, Sheng X (2011b) Characterization of lead-resistant and ACC deaminase-producing endophytic bacteria and their potential in promoting lead accumulation of rape. J Hazard Mater 186:1720–1725. https://doi.org/10.1016/j.jhazmat.2010.12.069

[] Zhong X, Chen Z, Li Y, Ding K, Liu W, Liu Y, Yuan Y, Zhang M, Baker AJM, Yang W (2020) Factors influencing heavy metal availability and risk assessment of soils at typical metal mines in Eastern China. J Hazard Mater 400:123–134. https://doi.org/10.1016/j.jhazmat.2020.123289

[] Zhu F, Fan W, Wang X, Qu LI, Yao S (2011) Health risk assessment of eight heavy metals in nine varieties of edible vegetable oils consumed in China. Food Chem Toxicol 49:3081–3085. https://doi.org/10.1016/j.fct.2011.09.019