Abstract
Cadmium (Cd) presence and bioavailability in soils is a serious concern for cocoa producers. Cocoa plants can bioaccumulate Cd that can reach humans through the food chain, thus posing a threat to human health, as Cd is a highly toxic metal. Currently, microbiologically induced carbonate precipitation (MICP) by the ureolytic path has been proposed as an effective technique for Cd remediation. In this work, the Cd remediation potential and Cd resistance of two ureolytic bacteria, Serratia sp. strains 4.1a and 5b, were evaluated. The growth of both Serratia strains was inhibited at 4 mM Cd(II) in the culture medium, which is far higher than the Cd content that can be found in the soils targeted for remediation. Regarding removal efficiency, for an initial concentration of 0.15 mM Cd(II) in liquid medium, the maximum removal percentages for Serratia sp. 4.1.a and 5b were 99.3% and 99.57%, respectively. Their precipitates produced during Cd removal were identified as calcite by X-ray diffraction. Energy dispersive X-ray spectroscopy analysis showed that a portion of Cd was immobilized in this matrix. Finally, the presence of a partial gene from the czc operon, involved in Cd resistance, was observed in Serratia sp. 5b. The expression of this gene was found to be unaffected by the presence of Cd(II), and upregulated in the presence of urea. This work is one of the few to report the use of bacterial strains of the Serratia genus for Cd remediation by MICP, and apparently the first one to report differential expression of a Cd resistance gene due to the presence of urea.
Similar content being viewed by others
Data availability
The authors confirm that the data supporting the findings of this study are available within the article and its supplementary materials.
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. https://doi.org/10.1007/s13762-017-1400-5
Benzerara K, Miot J, Morin G, Ona-Nguema G, Skouri-Panet F, Férard C (2011) Significance, mechanisms and environmental implications of microbial biomineralization. C R - Geosci 343(2–3):160–167. https://doi.org/10.1016/j.crte.2010.09.002
Bhattacharya A, Naik SN, Khare SK (2018) Harnessing the bio-mineralization ability of urease producing Serratia marcescens and Enterobacter cloacae EMB19 for remediation of heavy metal cadmium (II). J Environ Manag 215:145–152. https://doi.org/10.1016/j.jenvman.2018.03.055
Bravo D, Leon-Moreno C, Martínez CA, Varón-Ramírez VM, Araujo-Carrillo GA, Vargas R, Quiroga-Mateus R, Zamora A, Gutiérrez-Rodríguez EA (2021) The First National Survey of Cadmium in Cacao Farm Soil in Colombia. Agronomy 11(761). https://doi.org/10.3390/agronomy11040761
Bustin S, Benes V, Garson J, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl N, Shipley G, Vandesompele J, Wittwer C (2009) The MIQE Guidelines: Minimum Information for Publication of Quantitative Real-Time PCR Experiments. Clin Chem 55(4):611–622. https://doi.org/10.1373/clinchem.2008.112797
Chen YP, Liu Q, Liu YJ, Jia FA, He XH (2014) Responses of soil microbial activity to cadmium pollution and elevated CO2. Sci Rep 4(4287). https://doi.org/10.1038/srep04287
Chi Y, Huang Y, Wang J, Chen X, Chu S, Hayat K, Xu Z, Xu H, Zhou P, Zhang D (2020) Two plant growth promoting bacterial Bacillus strains possess different mechanisms in adsorption and resistance to cadmium. Sci Total Environ 741:140422. https://doi.org/10.1016/j.scitotenv.2020.140422
Choudhary S, Islam E, Kazy S, Sar P (2012) Uranium and other heavy metal resistance and accumulation in bacteria isolated from uranium mine wastes. J Environ Sci Health A 47(4):622–637. https://doi.org/10.1080/10934529.2012.650584
Das S, Dash HR (2017) Handbook of metal-microbe interactions and bioremediation. Taylor & Francis, Boca Raton
Díaz A, Marrero J, Cabrera G, Coto O, Gómez JM (2022) Biosorption of nickel, cobalt, zinc and copper ions by Serratia marcescens strain 16 in mono and multimetallic systems. Biodegradation 33:33–43. https://doi.org/10.1007/s10532-021-09964-9
Diez-Marulanda JC, Brandão PFB (2023) Isolation of urease-producing bacteria from cocoa farms soils in Santander, Colombia, for cadmium remediation. 3 Biotech 13(98). https://doi.org/10.1007/s13205-023-03495-1
Federación Nacional de Cacaoteros [FEDECACAO] (2021) National Economy. https://www.fedecacao.com.co/economianacional. Accessed 07 June 2022 (in Spanish)
Frankel RB, Bazylinski DA (2003) Biologically Induced Mineralization by Bacteria. Rev Mineral Geochem 54(1):95–114. https://doi.org/10.2113/0540095
Haroun AA, Kamaluddeen KK, Alhaji I, Magaji Y, Oaikhena EE (2017) Evaluation of Heavy Metal Tolerance Level (MIC) and Bioremediation Potentials of Pseudomonas aeruginosa Isolated from Makera-Kakuri Industrial Drain in Kaduna, Nigeria. Eur J Exp Biol 7(5). https://doi.org/10.21767/2248-9215.100028
Huang S, Liu R, Sun M, Li X, Guan Y, Lian B (2022) Transcriptome expression analysis of the gene regulation mechanism of bacterial mineralization tolerance to high concentrations of Cd2+. Sci Total Environ 806(4):150911. https://doi.org/10.1016/j.scitotenv.2021.150911
Jain S, Bhatt A (2013) Molecular and in situ characterization of cadmium-resistant diversified extremophilic strains of Pseudomonas for their bioremediation potential. 3 Biotech 4(3):297–304. https://doi.org/10.1007/s13205-013-0155-z
Kamika I, Momba M (2013) Assessing the resistance and bioremediation ability of selected bacterial and protozoan species to heavy metals in metal-rich industrial wastewater. BMC Microbiol 13(28). https://doi.org/10.1186/1471-2180-13-28
Karelová E, Harichová J, Stojnev T, Pangallo D, Ferianc P (2011) The isolation of heavy-metal resistant culturable bacteria and resistance determinants from a heavy-metal-contaminated site. Biologia 1:18–26. https://doi.org/10.2478/s11756-010-0145-0
Khadim HJ, Ammar SH, Ebrahim SE (2019) Biomineralization based remediation of cadmium and nickel contaminated wastewater by ureolytic bacteria isolated from barn horses soil. Environ Technol Innov 14:100315. https://doi.org/10.1016/j.eti.2019.100315
Khalid S, Shahid M, Khan N, Murtaza B, Bibi I, Dumat C (2017) A comparison of technologies for remediation of heavy metal contaminated soils. J Geochem Explor 182(part B):247–268. https://doi.org/10.1016/j.gexplo.2016.11.021
Khan AR, Park GS, Asaf S, Hong SJ, Jung B, Shin JH (2017) Complete genome analysis of Serratia marcescens RSC-14: A plant growth-promoting bacterium that alleviates cadmium stress in host plants. PLoS One 12(2):e0171534. https://doi.org/10.1371/journal.pone.0171534
Khan Z, Rehman A, Hussain S, Nisar MA, Zulfiqar S, Shakoori AR (2016) Cadmium resistance and uptake by bacterium, Salmonella enterica 43C, isolated from industrial effluent. AMB Express 6(54). https://doi.org/10.1186/s13568-016-0225-9
Kumar P, Gupta SB, Anurag, Soni R (2019) Bioremediation of Cadmium by Mixed Indigenous Isolates Serratia liquefaciens BSWC3 and Klebsiella Pneumoniae RpSWC3 Isolated from Industrial and Mining Affected Water Samples. Pollution 5(2):351–360. https://doi.org/10.22059/poll.2018.268603.533
Kumari D, Pan X, Lee D, Achal V (2014) Immobilization of cadmium in soil by microbially induced carbonate precipitation with Exiguobacterium undae at low temperature. Int Biodeterior Biodegrad 94:98–102. https://doi.org/10.1016/j.ibiod.2014.07.007
Li W, Liu L, Chen W, Yu L, Li W, Yu H (2010) Calcium carbonate precipitation and crystal morphology induced by microbial carbonic anhydrase and other biological factors. Process Biochem 45(6):1017–1021. https://doi.org/10.1016/j.procbio.2010.03.004
Méndez V, Fuentes S, Morgante V, Hernández M, González M, Moore E, Seeger M (2017) Novel hydrocarbonoclastic metal-tolerant Acinetobacter and Pseudomonas strains from Aconcagua river oil-polluted soil. J Soil Sci Plant Nutr 17(4). https://doi.org/10.4067/S0718-95162017000400017
Meter A, Atkinson RJ, Laliberte B (2019) Cadmium in cacao from Latin America and the Caribbean: A review of research and potential mitigation solutions. Bioversity International, Rome
Montaño-Salazar SM, Lizarazo-Marriaga J, Brandão PFB (2018) Isolation and Potential Biocementation of Calcite Precipitation Inducing Bacteria from Colombian Buildings. Curr Microbiol 75:256–265. https://doi.org/10.1007/s00284-017-1373-0
Montoya C, Márquez MA, López JM, Cuervo C (2005) Characterization of calcite crystals bioprecipitated by a native isolate of Bacillus subtilis. Rev Colomb Biotecnol 7(2):19–25 (in Spanish)
Naz N, Young H, Ahmed N, Gadd G (2005) Cadmium Accumulation and DNA Homology with Metal Resistance Genes in Sulfate-Reducing Bacteria. Appl Environ Microbiol 71(8):4610–4618. https://doi.org/10.1128/AEM.71.8.4610-4618.2005
Nongkhlaw M, Joshi SR (2019) Molecular insight into the expression of metal transporter genes in Chryseobacterium sp. PMSZPI isolated from uranium deposit. PLoS One 14(5):e0216995. https://doi.org/10.1371/journal.pone.0216995
Oger C, Mahillon J, Petit F (2003) Distribution and diversity of a cadmium resistance (cadA) determinant and occurrence of IS257 insertion sequences in Staphylococcal bacteria isolated from a contaminated estuary (Seine, France). FEMS Microbiol Ecol 43(2):173–183. https://doi.org/10.1111/j.1574-6941.2003.tb01056.x
Peng D, Qiao S, Luo Y, Ma H, Zhang L, Hou S, Wu B, Xu H (2020) Performance of microbial induced carbonate precipitation for immobilizing Cd in water and soil. J Hazard Mater 400:123116. https://doi.org/10.1016/j.jhazmat.2020.123116
Rajasekar A, Wilkinson S, Moy C (2021) MICP as a potential sustainable technique to treat or entrap contaminants in the natural environment: A review. Environ Sci Ecotechnol 6(100096). https://doi.org/10.1016/j.ese.2021.100096
Rocha DJP, Santos CS, Pacheco LGC (2015) Bacterial reference genes for gene expression studies by RT-qPCR: survey and analysis. Antonie Van Leeuwenhoek 108:685–693. https://doi.org/10.1007/s10482-015-0524-1
Roosa S, Wattiez R, Prygiel E, Lesven L, Billon G, Gillan D (2014) Bacterial metal resistance genes and metal bioavailability in contaminated sediments. Environ Pollut 189:143–151. https://doi.org/10.1016/j.envpol.2014.02.031
Sharma S, Tiwari S, Hasan A, Saxena V, Pandey LM (2018) Recent advances in conventional and contemporary methods for remediation of heavy metal-contaminated soils. 3 Biotech 8(16):1–18. https://doi.org/10.1007/s13205-018-1237-8
Tamayo-Figueroa DP, Castillo E, Brandão PFB (2019) Metal and metalloid immobilization by microbiologically induced carbonates precipitation. World J Microbiol Biotechnol 35(58). https://doi.org/10.1007/s11274-019-2626-9
Tanwir K, Javed MT, Abbas S, Shahid M, Akram MS, Chaudhary HJ, Iqbal M (2021) Serratia sp. CP-13 alleviates Cd toxicity by morpho-physio-biochemical improvements, antioxidative potential and diminished Cd uptake in Zea mays L. cultivars differing in Cd tolerance. Ecotoxicol Environ Saf 208:111584. https://doi.org/10.1016/j.ecoenv.2020.111584
Vidhyaparkavi A, Osborne J, Babu S (2017) Analysis of zntA gene in environmental Escherichia coli and additional implications on its role in zinc translocation. 3 Biotech 7(9). https://doi.org/10.1007/s13205-017-0613-0
Wei T, Sun Y, Yashir N, Li X, Guo J, Liu X, Jia H, Ren X, Hua L (2022) Inoculation with Rhizobacteria Enhanced Tolerance of Tomato (Solanum lycopersicum L.) Plants in Response to Cadmium Stress. J Plant Growth Regul 41:445–460. https://doi.org/10.1007/s00344-021-10315-4
Xie F, Xiao P, Chen D, Xu L, Zhang B (2012) miRDeepFinder: a miRNA analysis tool for deep sequencing of plant small RNAs. Plant Mol Biol 80(1):75–84. https://doi.org/10.1007/s11103-012-9885-2
Yao Z, Li J, Xie H, Yu C (2012) Review on Remediation Technologies of Soil Contaminated by Heavy Metals. Procedia Environ Sci 16:722–729. https://doi.org/10.1016/j.proenv.2012.10.099
Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden T (2012) Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinform 13:134. https://doi.org/10.1186/1471-2105-13-134
Yin T, Lin H, Dong Y, Li B, He Y, Liu C, Chen X (2021) A novel constructed carbonate-mineralized functional bacterial consortium for high-efficiency cadmium biomineralization. J Hazard Mater 401:123269. https://doi.org/10.1016/j.jhazmat.2020.123269
Yun J, Heisler L, Hwang I, Wilkins O, Lau S, Hyrcza M, Jayabalasingham B, Jin J, McLaurin J, Tsao M, Der S (2006) Genomic DNA functions as a universal external standard in quantitative real-time PCR. Nucleic Acids Res 34(12):e85. https://doi.org/10.1093/nar/gkl400
Zagorac D, Müller H, Ruehl S, Zagorac J, Rehme S (2019) Recent developments in the Inorganic Crystal Structure Database: theoretical crystal structure data and related features. J Appl Crystallogr 52:918–925. https://doi.org/10.1107/S160057671900997X
Zhang Y, Zhang H, Li X, Su Z, Zhang C (2008) The cadA Gene in Cadmium-Resistant Bacteria from Cadmium-Polluted Soil in the Zhangshi Area of Northeast China. Curr Microbiol 56(3):236–239. https://doi.org/10.1007/s00284-007-9064-x
Zhao Y, Yao J, Yuan Z, Wang T, Zhang Y, Wang F (2016) Bioremediation of Cd by strain GZ-22 isolated from mine soil based on biosorption and microbially induced carbonate precipitation. Environ Sci Pollut Res 24(1):372–380. https://doi.org/10.1007/s11356-016-7810-y
Zhao X, Wang M, Wang H, Tang D, Huang J, Sun Yu (2019) Study on the Remediation of Cd Pollution by the Biomineralization of Urease-Producing Bacteria. Int J Environ Res Public Health 16(268). https://doi.org/10.3390/ijerph16020268
Zheng X, Chen L, Chen M, Chen J, Li X (2019) Functional Metagenomics to Mine Soil Microbiome for Novel Cadmium Resistance Genetic Determinants. Pedosphere 29(3):298–310. https://doi.org/10.1016/s1002-0160(19)60804-0
Zheng Y, Xiao C, Chi R (2021) Remediation of soil cadmium pollution by biomineralization using microbial-induced precipitation: a review. World J Microbiol Biotechnol 37(208):1–15. https://doi.org/10.1007/s11274-021-03176-2
Acknowledgements
The authors thank Miguel Angel Beltrán, from the Asociación de Campesinos Vecinos del Parque Natural Nacional Serranía de los Yariguies (ASOCAPAYARI), El Carmen de Chucurí, Santander, Colombia, for access to the original soil samples from where the microorganisms used in this work were obtained. We also thank, at the Universidad Nacional de Colombia, Professor Elianna Castillo Serna, from the Chemistry Department, for the help provided during Cd quantification by AAS, and Professor Esperanza Torres Rojas and Engineer Juliana Miranda, from the Agricultural Sciences Department, for their contribution with the RNA related work. Finally, we acknowledge the help provided by Professor Ibonne Aydee Garcia Romero, from the Instituto de Biotecnología—Universidad Nacional de Colombia (IBUN), for cDNA quantification and molecular biology related work. This work was financially supported by the Dirección de Investigación y Extensión sede Bogotá (DIEB) at the Universidad Nacional de Colombia (grants numbers 37691 and 48328), and the Ministerio de Ciencia, Tecnología e Innovación (MinCiencias) of Colombia (grant number 110180863795/CT-190-2019). The Ministerio de Ambiente y Desarrollo Sostenible de Colombia (MinAmbiente) is acknowledged for the permits to collect and access national genetic resources (Contrato de Acceso a Recursos Genéticos y sus Productos Derivados No. 121 de 2016—Otrosí No. 17).
Funding
This work was supported by the Dirección de Investigación y Extensión sede Bogotá (DIEB) at the Universidad Nacional de Colombia (grant numbers 37691 and 48328), and the Ministerio de Ciencia, Tecnología e Innovación (MinCiencias) of Colombia (gran number 110180863795/CT-190–2019).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Juan C. Diez-Marulanda carried out the experiments while Pedro F. B. Brandão supervised the project. The first draft of the manuscript was written by Juan C. Diez-Marulanda, and Pedro F. B. Brandão commented and reviewed the manuscript before submission. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethical approval
Not applicable.
Consent to participate
Not applicable.
Consent to publish
Not applicable.
Competing interests
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Responsible Editor: Gerald Thouand
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
Diez-Marulanda, J.C., Brandão, P.F.B. Potential use of two Serratia strains for cadmium remediation based on microbiologically induced carbonate precipitation and their cadmium resistance. Environ Sci Pollut Res 31, 5319–5330 (2024). https://doi.org/10.1007/s11356-023-31062-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-023-31062-x