Abstract
In this study, the capacity of cadmium (Cd)-resistant plant growth-promoting bacteria (PGPB) Burkholderia sp. SRB-1 (SRB-1) and its mechanisms were explored through morphological characterizations, biochemical response, plant growth-promoting traits, and functional gene expression patterns. The results showed that SRB-1 was an excellent Cd-resistant bacteria (MIC was 420 mg L−1), and its maximum Cd removal rate reached 72.25%. Biosorption was the main removal method of Cd for SRB-1, preventing intracellular Cd accumulation and maintaining cellular metabolism. Various functional groups on the cell wall were involved in Cd binding, which deposited as CdS and CdCO3 on the cell surface according to XPS analysis and might be critical for reducing Cd physiochemical toxicity. Furthermore, metals exporting (zntA, czcA, czcB, czcC), detoxification (dsbA, cysM), and antioxidation (katE, katG, SOD1) related genes were annotated in the SRB-1 genome. The results of Cd distribution and antioxidative enzyme activity in SRB-1 also illustrated that Cd2+ efflux and antioxidative response were the main intracellular Cd-resistant mechanisms. These conclusions were further verified by qRT-PCR analysis. Overall, the strategies of extracellular biosorption, cation efflux, and intracellular detoxification jointly build the Cd-resistant system, which invested Burkholderia sp. SRB-1 with potential for bioremediation in heavily Cd-contaminated environmental sites.
Similar content being viewed by others
Data availability
All data and materials generated or analyzed during this study are included in this published article.
References
Abbas SZ, Rafatullah M, Hossain K, Ismail N, Tajarudin HA, Abdul Khalil HPS (2017) A review on mechanism and future perspectives of cadmium-resistant bacteria. Int J Environ Sci Technol 15:243–262
Ankita I, Jabez W, Osborne M, Vaithilingam (2019) Enhanced uptake of Cd by biofilm forming Cd resistant plant growth promoting bacteria bioaugmented to the rhizosphere of Vetiveria zizanioides. Int J Phytorem 21(5):487–495
Bhakta JN, Munekage Y, Ohnishi K, Jana B, Balcazar JL (2014) Isolation and characterization of cadmium- and arsenic-absorbing bacteria for bioremediation. Water Air Soil Pollut 225:1–10
Chen Y, Chao Y, Li Y, Lin Q, Bai J, Tang L, Wang S, Ying R, Qiu R (2016) Survival strategies of the plant-associated bacterium Enterobacter sp. strain EG16 under cadmium stress. Appl Environ Microbiol 82:1734–1744
Chin C, Peluso P, Sedlazeck FJ, Nattestad M (2016) Phased diploid genome assembly with single-molecule real-time sequencing. Nat Methods 13:1050–1054
Chou T-S, Chao Y-Y, Kao CH (2012) Involvement of hydrogen peroxide in heat shock- and cadmium-induced expression of ascorbate peroxidase and glutathione reductase in leaves of rice seedlings. J Plant Physiol 169:478–486
Chu C, Huang R, Liu L, Tang G, Xiao J, Yoo H, Yuan M (2022) The rice heavy-metal transporter OsNRAMP1 regulates disease resistance by modulating ROS homoeostasis. Plant, Cell Environ 45(4):1109–1126
Dai Y, Liu R, Zhou Y, Li N, Hou L, Ma Q, Gao B (2020) Fire Phoenix facilitates phytoremediation of PAH-Cd co-contaminated soil through promotion of beneficial rhizosphere bacterial communities. Environ Int 136:105421
Dixit R, Wasiullah MD, Pandiyan K, Paul D (2015) Bioremediation of heavy metals from soil and aquatic environment: an overview of principles and criteria of fundamental processes. Sustainability 2015:2189–2212
Fan K, Delgado-Baquerizo M, Guo X, Wang D, Zhu YG, Chu H (2021) Biodiversity of key-stone phylotypes determines crop production in a 4-decade fertilization experiment. ISME J 15:550–561
Feng M, Yin H, Peng H, Liu Z, Lu G, Dang Z (2017) Hexavalent chromium induced oxidative stress and apoptosis in Pycnoporus sanguineus. Environ Pollut 228:128–139
Gregorio SD, Lampis S, Vallini G (2005) Selenite precipitation by a rhizospheric strain of Stenotrophomonas sp. isolated from the root system of Astragalus bisulcatus: a biotechnological perspective. Enviro Int 31(2):233–241
Haskett TL, Tkacz A, Poole PS (2020) Engineering rhizobacteria for sustainable agriculture. ISME J 15:949–964
Jebril N, Boden R, Braungardt C (2022) Cadmium resistant bacteria mediated cadmium remova1 a systematic review on resistance mechanism and bioremediation approaches. Earth Environ Sci 1002(1):12006
Jiang Z, Jiang L, Zhang L, Su M, Tian D, Wang T, Sun Y, Nong Y, Hu S, Wang S, Li Z (2020) Contrasting the Pb (II) and Cd (II) tolerance of Enterobacter sp. via its cellular stress responses. Environ Microbiol 22:1507–1516
Karthik C, Barathi S, Pugazhendhi A, Ramkumar VS, Thi N, Arulselvi PI (2017) Evaluation of Cr(VI) reduction mechanism and removal by Cellulosimicrobium funkei strain AR8, a novel haloalkaliphilic bacterium. J Hazard Mater 333:41–53
Ke T, Guo G, Liu J, Zhang C, Chen L (2021) Improvement of the Cu and Cd phytostabilization efficiency of perennial ryegrass through the inoculation of three metal-resistant PGPR strains. Environ Pollut 271:116314
Lexian X, Chu Y, Liyuan C, Guanzhou Q, Wenqing Q (2010) Metabolic changes of Acidithiobacillus caldus under Cu2+ stress. J Basic Microbiol 50:591–598
Li X, Dong S, Yao Y, Shi W, Wu M, Xu H (2016) Inoculation of bacteria for the bioremediation of heavy metals contaminated soil by Agrocybe aegerita. RSC Adv 6:65816–65824
Li X, Xiao K, Ma H, Li L, Tan H, Xu H, Li Y (2019) Mechanisms into the removal and translocation of cadmium by Oudemansiella radicata in soil. Environ Sci Pollut Res Int 26:6388–6398
Ling N, Wang T, Kuzyakov Y (2022) Rhizosphere bacteriome structure and functions. Nat Commun 13:836
Liu H, Wang C, Xie Y, Luo Y, Sheng M, Xu F, Xu H (2020a) Ecological responses of soil microbial abundance and diversity to cadmium and soil properties in farmland around an enterprise-intensive region. J Hazard Mater 392:122478
Liu H, Xie Y, Li J, Zeng G, Li H, Xu F, Feng S, Xu H (2020b) Effect of Serratia sp. K3 combined with organic materials on cadmium migration in soil-vetiveria zizanioides L. system and bacterial community in contaminated soil. Chemosphere 242:125164
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 ΔΔ C T method. Methods 25:402–408
Luo J, Gu S, Guo X, Liu Y, Tao Q, Zhao HP, Liang Y, Banerjee S, Li T (2022) Core microbiota in the rhizosphere of heavy metal accumulators and its contribution to plant performance. Environ Sci Technol 56:12975–12987
Manzoor M, Abid R, Rathinasabapathi B, De Oliveira LM, da Silva E, Deng F, Rensing C, Arshad M, Gul I, Xiang P, Ma LQ (2019) Metal tolerance of arsenic-resistant bacteria and their ability to promote plant growth of Pteris vittata in Pb-contaminated soil. Sci Total Environ 660:18–24
Mazhar SH, Herzberg M, Ben Fekih I, Zhang C, Bello SK, Li YP, Su J, Xu J, Feng R, Zhou S, Rensing C (2020) Comparative insights into the complete genome sequence of highly metal resistant Cupriavidus metallidurans strain BS1 isolated from a gold-copper mine. Front Microbiol 11:1–21
Minari GD, Saran LM, Lima Constancio MT, Correia da Silva R, Rosalen DL, José de Melo W, Carareto Alves LM (2020) Bioremediation potential of new cadmium, chromium, and nickel-resistant bacteria isolated from tropical agricultural soil. Ecotoxicol Environ Saf 204:111038
Minjie C, Yanjun Li, Li Z, Jianying W, Chunli Z (2015) Analysis of gene expression provides insights into the mechanism of cadmium tolerance in Acidithiobacillus ferrooxidans. Curr Microbiol 70:290–297
Mitra S, Pramanik K, Ghosh PK, Soren T, Sarkar A, Dey RS, Pandey S, Maiti TK (2018) Characterization of Cd-resistant Klebsiella michiganensis MCC3089 and its potential for rice seedling growth promotion under Cd stress. Microbiol Res 210:12–25
Naik MM, Dubey SK (2017) Lead- and mercury-resistant marine bacteria and their application in lead and mercury bioremediation 3. Springer, Singapore, pp 29–40
Naveed M, Mitter B, Reichenauer TG, Wieczorek K, Sessitsch A (2014) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39
Pacevski A, Moric I, Pavic N, Tatjana V, Branka I-T (2015) Diversity and biodeteriorative potential of bacterial isolates from deteriorated modern combined-technique canvas painting. Int Biodeterior Biodegradation 97:40–50
Pramanik K, Mitra S, Sarkar A, Soren T, Maiti TK (2017) Characterization of cadmium-resistant Klebsiella pneumoniae MCC 3091 promoted rice seedling growth by alleviating phytotoxicity of cadmium. Environ Sci Pollut Res 24:24419–24437
Rahman Z, Thomas L, Singh VP (2019) Biosorption of heavy metals by a lead (Pb) resistant bacterium, Staphylococcus hominis strain AMB-2. J Basic Microbiol 59:477–486
Rodríguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287:15–21
Sarwar N, Imran M, Shaheen MR, Ishaque W (2017) Phytoremediation strategies for soils contaminated with heavy metals: modifications and future perspectives. Chemosphere 171:710–721
Schindler BD, Frempong-Manso E, Demarco CE, Kosmidis C, Kaatz GW (2014) Analyses of multidrug efflux pump-like proteins encoded on the Staphylococcus aureus chromosome: TABLE 1. Antimicrob Agents Chemother 59(1):747–748
Shaaban MT, Ibrahim HAH, Abouhend AS, El-Moselhy KM (2015) Removal of heavy metals from aqueous solutions using multi-metals and antibiotics resistant bacterium isolated from the Red Sea, Egypt. Am J Microbiol Res 3:93–106
Shahid M, Dumat C, Khalid S, Niazi NK, Antunes P (2016) Cadmium bioavailability, uptake, toxicity and detoxification in soil-plant system. Rev Environ Contam Toxicol 241:73–137
Suelee AL, Hasan SNMS, Kusin FM, Yusuff FM, Ibrahim ZZ (2017) Phytoremediation potential of vetiver grass (Vetiveria zizanioides) for treatment of metal-contaminated water. Water Air Soil Pollut 228(4):158
Sun R, Wang L, Huang R, Huang F, Gan D, Wang J, Guan R, Han W, Qu J, Yan L, Zhang Y (2020) Cadmium resistance mechanisms of a functional strain Enterobacter sp. DNB-S2, isolated from black soil in Northeast China. Environ Pollut 263:114612
Tan H, Wang C, Zeng G, Luo Y, Li H, Xu H (2020) Bioreduction and biosorption of Cr(VI) by a novel Bacillus sp. CRB-B1 strain. J Hazard Mater 386:121628
Teng Z, Shao W, Zhang K, Huo Y, Li M (2019) Characterization of phosphate solubilizing bacteria isolated from heavy metal contaminated soils and their potential for lead immobilization. J Environ Manag 231:189–197
Vilela FP, Rodrigues DDP, Allard MW, Falcao JP (2022) Prevalence of efflux pump and heavy metal tolerance encoding genes among Salmonella enterica serovar Infantis strains from diverse sources in Brazil. PLoS One 17:e0277979
Wan Y, Luo S, Chen J, Xiao X, Chen L, Zeng G, Liu C, He Y (2012) Effect of endophyte-infection on growth parameters and Cd-induced phytotoxicity of Cd-hyperaccumulator Solanum nigrum L. Chemosphere 89:743–750
Wang C, Minghui Wu, Peng C, Yan F, Jia Y, Li X, Li M, Bin Wu, Heng Xu, Qiu Z (2022a) Bacterial dynamics and functions driven by a novel microbial agent to promote kitchen waste composting and reduce environmental burden. J Clean Prod 337:130491
Wang Y, Luo H, Peng H, Wang X, Xu F, Xu H (2022b) Coprinus comatus endophytic bacteria characteristics and mechanisms for the cadmium resistance. Environ Sci Pollut Res 29(1):584–593
WeiXie L, Yang R, Liu B, Lei N, Peng S, Li J, Tong J, Deng R, Li J (2022) Effects of Pb-, Cd-resistant bacterium Pantoea sp. on growth, heavy metal uptake and bacterial communities in oligotrophic growth substrates of Lolium multiflorum Lam. Environ Sci Pollut Res Int 29:50742–50754
Wu M, Li Y, Li J, Wang Y, Xu H, Zhao Y (2019) Bioreduction of hexavalent chromium using a novel strain CRB-7 immobilized on multiple materials. J Hazard Mater 368:412–420
Wu B, He T, Wang Z, Qiao S, Wang Y, Xu F, Xu H (2020) Insight into the mechanisms of plant growth promoting strain SNB6 on enhancing the phytoextraction in cadmium contaminated soil. J Hazard Mater 385:121587
Wu B, Luo H, Wang X, Liu H, Peng H, Sheng M, Xu F, Xu H (2022) Effects of environmental factors on soil bacterial community structure and diversity in different contaminated districts of Southwest China mine tailings. Sci Total Environ 802:149899
Yang P, Zhou XF, Wang LL, Li QS, Zhou T, Chen YK, Zhao ZY, He BY (2018) Effect of phosphate-solubilizing bacteria on the mobility of insoluble cadmium and metabolic analysis. Int J Environ Res Public Health 15(7):1330
Yong W, Luo S, Chen J, Xiao X, Chen L, Zeng G, Liu C, He Y (2012) Effect of endophyte-infection on growth parameters and Cd-induced phytotoxicity of Cd-hyperaccumulator Solanum nigrum L. Chemosphere 89:743–750
Zeng W, Li F, Wu C, Yu R, Wu X, Shen L, Liu Y, Qiu G, Li J (2020) Role of extracellular polymeric substance (EPS) in toxicity response of soil bacteria Bacillus sp. S3 to multiple heavy metals. Bioprocess Biosyst Eng 43:153–167
Zeng G, Qiao S, Wang X, Sheng M, Xu F (2021) Immobilization of cadmium by Burkholderia sp. QY14 through modified microbially induced phosphate precipitation. J Hazard Mater 421:125156
Zhang J, Li Q, Zeng Y, Zhang J, Lu G, Dang Z, Guo C (2019) Bioaccumulation and distribution of cadmium by Burkholderia cepacia GYP1 under oligotrophic condition and mechanism analysis at proteome level. Ecotoxicol Environ Saf 176:162–169
Zhao Y, Yao J, Yuan Z, Wang T, Zhang Y, Wang F (2017) Bioremediation of Cd by strain GZ-22 isolated from mine soil based on biosorption and microbially induced carbonate precipitation. Environ Sci Pollut Res 24:372–380
Zhong Y, Xun W, Wang X, Tian S, Zhang Y, Li D, Zhou Y, Qin Y, Zhang B, Zhao G, Cheng X, Liu Y, Chen H, Li L, Osbourn A, Lucas WJ, Huang S, Ma Y, Shang Y (2022) Root-secreted bitter triterpene modulates the rhizosphere microbiota to improve plant fitness. Nat Plants 8:887–896
Acknowledgements
The authors also wish to thank Professor Guanglei Cheng and Hui Wang from Sichuan University for the technical assistance.
Funding
This work was financially supported by the National Key Research and Development Program of China (2018YFC1802605, 2020YFC1807703) and the Regional Innovation Cooperation Project of Sichuan Province (2021YFQ0014).
Author information
Authors and Affiliations
Contributions
Huakang Liu: conceptualization, investigation, methodology, data curation, writing—original draft, writing—review and editing, visualization, supervision. Huayan Huang: investigation, methodology, data curation, writing—review and editing, visualization. Ke Liang: investigation, methodology, visualization. Kangkai Lin: visualization, data curation. Yuxian Shangguan: writing—review and editing, supervision, investigation, funding acquisition. Heng Xu: revising and editing, data processing, supervision, funding acquisition.
Corresponding author
Ethics declarations
Ethical approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
All authors whose names appear on the submission approved the version to be published and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
Competing of interests
The authors declare no competing interests.
Additional information
Responsible Editor: Robert Duran
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Liu, H., Huang, H., Liang, K. et al. Characterization of a cadmium-resistant functional bacteria (Burkholderia sp. SRB-1) and mechanism analysis at physiochemical and genetic level. Environ Sci Pollut Res 30, 78408–78422 (2023). https://doi.org/10.1007/s11356-023-27824-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-023-27824-2