Assessment and bioremediation of mercury pollutants by highly mercury-resistant bacteria immobilized in biochar from small-scale artisanal gold mining areas

Authors

  • Dewi Nursaidah Rohmah Graduate Program of Biology, Faculty of Biology, Universitas Gadjah Mada
  • Endah Retnaningrum Microbiology Laboratory, Faculty of Biology, Universitas Gadjah Mada http://orcid.org/0000-0001-7936-4920

DOI:

https://doi.org/10.15243/jdmlm.2023.102.4061

Keywords:

bacteria immobilization, Escherichia fergusonii, polyphasic identification, river sediment, toxicity profile

Abstract

Small-scale gold mining activities in Indonesia still use amalgamation techniques, which have the potential to cause mercury (Hg) pollution and affect the quality and number of microorganisms. Mercury-resistant bacteria can survive and adapt to mercury-exposed environments and can be developed as bioremediation agents. The bioremediation activity of these bacteria can be increased through immobilization using biochar. The results of observations of physicochemical qualities in three samples in the mining area, showed significant differences. The TOC in the rhizosphere soil sample of Calliandra calothyrsus L. showed the significantly highest value at 14.5%, and the pH of the three samples indicated acidity and exhibited no difference (p<0.05). The highest concentration measured in the tailing sample was 9.9 ng/g (p<0.05). The number of heterotrophic bacteria in the rhizosphere soil was the highest at 7.2 × 108 CFU/g. On the other hand, the number of mercury-resistant bacteria in the tailing sample showed the highest value of 6.3 × 103 CFU/g. In the selection based on the toxicity profile of 30 mercury-resistant bacteria obtained, the highest results were observed in the LMP1B5 bacterial isolate from the river sediment, with 50% effective concentration (EC50) and minimum inhibitory concentration (MIC) values of 225 and 250 mg/L, respectively. Polyphasic identification based on phenotypic and genotypic characteristics using the 16S rRNA gene showed that the bacterial isolate was identified as Escherichia fergusonii. The growth and mercury removal activity of E. fergusonii LMP1B5 increased by 21% and 52%, respectively, after the immobilization with biochar. Thus, immobilized E. fergusonii LMP1B5 was effective in removing mercury pollutants.

Author Biography

Dewi Nursaidah Rohmah, Graduate Program of Biology, Faculty of Biology, Universitas Gadjah Mada

Biology Departemnt

References

Abu-Dieyeh, M.H., Alduroobi, H.M. and Al-Ghouti, M.A. 2019. Potential of mercury-tolerant bacteria for bio-uptake of mercury leached from discarded fluorescent lamps. Journal of Environmental Management 237:217-227, doi:10.1016/j.jenvman.2019.02.066.

Al-Ansari, M.M. 2022. Biodetoxification mercury by using a marine bacterium Marinomonas sp.RS3 and its merA gene expression under mercury stress. Environmental Research 205:112452, doi:10.1016/ j.envres.2021.112452.

Andriyanto, A., Wilopo, W. and Retnaningrum, E. 2020. The performance of a fixed-bed anaerobic bioreactor using sulfate-reducing bacterial consortium from Sikidang crater sediments. Indonesian Journal of Chemistry 20:190-199, doi:10.22146/ijc.45164.

Bera, S. and Mohanty, K. 2020. Areca nut (Areca catechu) husks and Luffa (Luffa cylindrica) sponge as microbial immobilization matrices for efficient phenol degradation. Journal of Water Process Engineering 33:100999, doi:10.1016/j.scitotenv.2022.155563.

Bouabidi, Z.B., El-Naas, M.H. and Zhang, Z. 2019. Immobilization of microbial cells for the biotreatment of wastewater: A review. Environmental Chemistry Letters 17:241-257, doi:10.1007/s10311-018-0795-7.

Bowman, K.L., Lamborg, C.H. and Agather, A.M. 2020. A global perspective on mercury cycling in the ocean. Science of the Total Environment 710:136166, doi:10.1016/j.scitotenv.2019.136166.

Brenner, D.J. Krieg, N.R. and Staley, J.R. 2005. Bergey's Manual Systematic Bacteriology, Springer, New York, US.

Carneiro, L.M., Zucchi, M. do Rosário Zucchi, M., de Jesus, T.B., Júnior, da Silva, J.B. and Hadlich, G.M. 2021. δ13C, δ15N and TOC/TN as indicators of the origin of organic matter in sediment samples from the estuary of a tropical river. Marine Pollution Bulletin 172:11285, doi:10.1016/j.marpolbul.2021.112857.

Chen, H., Zhang, J., Tang, L., Su, M., Tian, D., Zhang, L., Li, Z. and Hu, S. 2019. Enhanced Pb immobilization via the combination of biochar and phosphate solubilizing bacteria. Environment International 127:395-401, doi:10.1016/j.envint.2019.03.068.

Cilia, V., Lafay, B. and Christen, R. 1996. Sequence heterogeneities among 16S ribosomal RNA sequences, and their effect in phylogenetic analyses at the species level. Molecular Biology and Evolution 13:451-461, doi:10.1093/oxfordjournals.molbev.a025606.

Dash, H.R., Sahu, M., Mallick, B. and Das, S. 2017. Functional efficiency of MerA protein among diverse mercury resistant bacteria for efficient use in bioremediation of inorganic mercury. Biochimie 142:207-215, doi:10.1016/j.biochi.2017.09.016.

Farsi, R.M., Alharbi, N.M., Basingab, F.S., Nass, N.M., Qattan, S.Y., Hassoubah, S.A., Alrahimi, J.S. and Alaidaroos, B.A. 2021. Biodegradation of picric acid (2,4,6-trinitrophenol, TNP) by free and immobilized marine Enterococcus thailandicus isolated from the red sea, Saudi Arabia. Egyptian Journal of Aquatic Research 47:307-312, doi:10.1016/j.ejar.2021.05.002.

Fu, X., Qiao, Y., Xue, J., Cheng, D., Chen, C., Bai, Y. and Jiang, Q. 2021. Analyses of community structure and role of immobilized bacteria system in the bioremediation process of diesel pollution seawater. Science of the Total Environment 799:149439, doi:10.1016/j.scitotenv.2021.149439.

Heiri, O., Lotter, A.F. and Lemcke, G. 2001. Loss on ignition as a method for estimating organic and carbonate content in sediments: Reproducibility and comparability of results. Journal of Paleolimnology 25:101-110, doi:10.1023/A:1008119611481.

Hillis, D.M. and Bull, J.J. 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42:182-192, doi:10.1093/sysbio/42.2.182.

Hossain, M.I., Mizan, M.F.R., Ashrafudoulla, M., Nahar, S., Joo, H.J., Jahid, I.K., Park, S.H., Kim, K.S. and Ha, S.D. 2020. Inhibitory effects of probiotic potential lactic acid bacteria isolated from kimchi against Listeria monocytogenes biofilm on lettuce, stainless-steel surfaces, and MBECâ„¢ biofilm device. LWT 118, doi:10.1016/j.lwt.2019.108864.

Huang, J., Liu, C., Price, G.W., Li, Y. and Wang, Y. 2021. Identification of a novel heavy metal resistant Ralstonia strain and its growth response to cadmium exposure. Journal of Hazardous Materials 416:125942, doi:10.1016/j.jhazmat.2021.125942.

Hutamadi, Widi, B.N. and Suprapto, S.J. 2007. Review of the small-scale gold mining practices at Cineam, Tasikmalaya Regency, West Java, Indonesia. Buletin Sumber Daya Geologi 2(1):1-9, doi:10.47599/bsdg.v2i1.196.

Huys, G., Cnockaert, M., Janda, J.M. and Swings, J. 2003. Escherichia albertii sp. nov., a diarrhoeagenic species isolated from stool specimens of Bangladeshi Children. International Journal of Systematic and Evolutionary Microbiology 53:807-810, doi:10.1099/ijs.0.02475-0.

Jesionowski, T., Zdarta, J. and Krajewska, B. 2014. Enzyme immobilization by adsorption: a.review. Adsorption 20:801-821. doi:10.1007/s10450-014-9623-y.

Jiang, L., Zhang, R., Zhang, L., Zheng, R. and Zhong, M. 2021. Improving the regulatory health risk assessment of mercury-contaminated sites. Journal of Hazardous Materials 402:123493, doi:10.1016/ j.jhazmat.2020.123493.

Joshi, G., Meena, B., Verma, P., Nayak, J., Vinithkumar, N.V. and Dharani, G. 2021 Deep-sea mercury resistant bacteria from the Central Indian Ocean: A potential candidate for mercury bioremediation. Marine Pollution Bulletin 169:112549, doi:10.1016/j.marpolbul.2021.112549.

Karna, R.R., Luxton, T., Bronstein, K.E., Redmon, J.H. and Scheckel, K.G. 2017. State of the science review: Potential for beneficial use of waste by-products for in situ remediation of metal-contaminated soil and sediment. Critical Reviews in Environmental Science and Technology 47:65-129, doi:10.1080/10643389.2016.1275417.

Kumari, S., Amit, Jamwal, R., Mishra, N. and Singh, D.K. 2020. Recent developments in environmental mercury bioremediation and its toxicity: A review. Environmental Nanotechnology, Monitoring and Management 13:100283, doi:10.1016/j.enmm.2020.100283.

Liu, H., Xu, F., Xie, Y., Wang, C., Zhang, A., Li, L. and Xu, H. 2018. Effect of modified coconut shell biochar on availability of heavy metals and biochemical characteristics of soil in multiple heavy metals contaminated soil. Science of the Total Environment 645:702-709, doi:10.1016/j.scitotenv.2018.07.115.

Liu, S., Jin, D., Lan, R., Wang, Y., Meng, Q., Dai, H., Lu, S., Hu, S. and Xu, J. 2015. Escherichia marmotae sp. nov., isolated from faeces of Marmota himalayana. International Journal. International Journal of Systematic and Evolutionary Microbiology 65:2130-2134, doi:10.1099/ijs.0.000228.

Lo, K.H., Lu, C.-W., Lin, W.-H., Chien, C.-C., Chen, S.-C. and Kao, C.-M. 2020. Enhanced reductive dechlorination of trichloroethene with immobilized Clostridium butyricum in silica gel. Chemosphere 238:124596, doi:10.1016/j.chemosphere.2019.124596.

Lu, J., Peng, W., Lv, Y., Jiang, Y., Xu, B., Zhang, W., Zhou, J., Dong, W., Xin, F. and Jiang, M. 2020. Application of cell immobilization technology in microbial cocultivation systems for biochemicals production. Industrial and Engineering Chemistry Research 59:17026-17034, doi:10.1021/acs.iecr.0c01867.

Mahbub, K.R., Krishnan, K., Naidu, R. and Megharaj, M. 2016. Mercury resistance and volatilization by Pseudoxanthomonas sp. SE1 isolated from soil. Environmental Technology and Innovation 6:94-104, doi:10.1016/j.eti.2016.08.001.

Mahbub, K.R., Krishnan, K., Naidu, R. and Megharaj, M. 2017. Mercury remediation potential of a mercury resistant strain Sphingopyxis sp. SE2 isolated from contaminated soil. Journal of Environmental Sciences 51:128-137, doi:10.1016/j.jes.2016.06.032.

Mantey, J., Nyarko, K.B., Owusu-Nimo, F., Awua, K.A., Bempah, C.K., Amankwah, R.K., Akatu, W.E. and Appiah-Effah, E. 2020. Mercury contamination of soil and water media from different illegal artisanal small-scale gold mining operations (galamsey). Heliyon 6:e04312, doi:10.1016/j.heliyon.2020.e04312.

Mantey, J., Owusu-Nimo, F., Nyarko, K.B. and Aubynn, A. 2017. Operational dynamics of “Galamsey†within eleven selected districts of western region of Ghana. Journal of Mining and Environment 8:11-34, doi:10.22044/jme.2016.627.

Narváez, D.M., Groot, H., Diaz, S.M., Palma, R.M., Muñoz, N., Cros, M.P. and Hernández-Vargas, H.-V. 2017. Oxidative stress and repetitive element methylation changes in artisanal gold miners occupationally exposed to mercury. Heliyon 3:e00400, doi:10.1016/j.heliyon.2017.e00400.

Paradis, S., Boissinot, M., Paquette, N., Bélanger, S.D., Martel, E.A., Boudreau, D.K., Picard, F.J., Ouellette, M., Roy, P.H. and Bergeron, M.G. 2005. Phylogeny of the Enterobacteriaceae based on genes encoding elongation factor Tu and F-ATPase β-subunit. International Journal of Systematic and Evolutionary Microbiology 55:2013-2025, doi:10.1099/ijs.0.63539-0.

Pinto, L. de. C.M., Dórea, J.G., Bernardi, J.V.E. and Gomes, L.F. 2019. Mapping the evolution of mercury (Hg) research in the Amazon (1991â»2017): A scientometric analysis (1991–2017). International Journal of Environmental Research and Public Health 16:1111, doi:10.3390/ijerph16071111.

Priyadarshanee, M., Chatterjee, S., Rath, S., Dash, H.R. and Das, S. 2022. Cellular and genetic mechanism of bacterial mercury resistance and their role in biogeochemistry and bioremediation. Journal of Hazardous Materials 423:126985, doi:10.1016/j.jhazmat.2021.126985.

Rahim, A.R.A., Mohsin, H.M., Thanabalan, M., Rabat, N.E., Saman, N., Mat, H. and Johari, K. 2020. Effective carbonaceous desiccated coconut waste adsorbent for application of heavy metal uptakes by adsorption: Equilibrium, kinetic and thermodynamics analysis. Biomass and Bioenergy 142:105805, doi:10.1016/j.biombioe.2020.105805.

Rajasulochana, P. and Preethy, V. 2016. Comparison on efficiency of various techniques in treatment of waste and sewage water–A comprehensive review. Resource-Efficient Technologies 2:175-184, doi:10.1016/j.reffit.2016.09.004.

Rani, L., Srivastav, A.L. and Kaushal, J. 2021. Bioremediation: An effective approach of mercury removal from the aqueous solutions. Chemosphere 280:130654, doi:10.1016/j.chemosphere.2021.130654.

Retnaningrum, E. and Wilopo, W. 2016. Performance and bacterial composition of anodic biofilms in microbial fuel cell using dairy wastewater. AIP Conference: Towards The Sustainable Use of Biodiversity In a Changing Environment: From Basic to Applied Research: Proceeding of the 4th International Conference on Biological Science 1744 (1):020018, doi:10.1063/1.4953492.

Retnaningrum, E. and Wilopo, W. 2017. Removal of sulphate and manganese on synthetic wastewater in sulphate reducing bioreactor using Indonesian natural zeolite. Indonesian Journal of Chemistry 17:203-210, doi:10.22146/ijc.22710.

Retnaningrum, E., Wilopo, W. and Warmada, I.W. 2021. Enhancement of manganese extraction in a biochar-enriched bioleaching column with a mixed culture of indigenous bacteria. Biodiversitas Journal of Biological Diversity 22:2949, doi:10.13057/biodiv/d220560.

Rohmah, D.N. and Retnaningrum, E. 2021. Activity and characterization of mercury-reducing bacteria from traditional gold mining in Cineam, Tasikmalaya. Final Research Project of Graduate Student. Universitas Gadjah Mada, Yogyakarta, Indonesia (in Indonesian).

Schlaberg, R., Simmon, K.E. and Fisher, M.A. 2012. A systematic approach for discovering novel, clinically relevant bacteria. Emerging Infectious Diseases 18:422-430, doi:10.3201/eid1803.111481.

Sharma, S. and Malaviya, P. 2016. Bioremediation of tannery wastewater by chromium resistant novel fungal consortium. Ecological Engineering 91:419-425, doi:10.1016/j.ecoleng.2016.03.005.

Wang, R.F., Cao, W.W. and Cerniglia, C.E. 1997. Phylogenetic analysis and identification of Shigella spp. By Molecular Probes. Molecular and Cellular Probes 11:427-432, doi:10.1006/mcpr.1997.0136.

Wang, Z., Wang, Y., Zhao, P., Chen, L., Yan, C., Yan, Y. and Chi, Q. 2015. Metal release from contaminated coastal sediments under changing pH conditions: Implications for metal mobilization in acidified oceans. Marine Pollution Bulletin 101:707-715, doi:10.1016/j.marpolbul.2015.10.026.

Xiong, B., Zhang, Y., Hou, Y., Arp, H.P.H., Reid, B.J. and Cai, C. 2017. Enhanced biodegradation of PAHs in historically contaminated soil by M. gilvum inoculated biochar. Chemosphere 182:316-324, doi:10.1016/j.chemosphere.2017.05.020.

Xu, J., Cao, Z., Zhang, Y., Yuan, Z., Lou, Z., Xu, X. and Wang, X. 2018. A review of functionalized carbon nanotubes and graphene for heavy metal adsorption from water: Preparation, application, and mechanism. Chemosphere 195:351-364, doi:10.1016/j.chemosphere.2017.12.061.

Yarza, P., Spröer, C., Swiderski, J., Mrotzek, N., Spring, S., Tindall, B.J., Gronow, S., Pukall, R., Klenk, H.P., Lang, E., Verbarg, S., Crouch, A., Lilburn, T., Beck, B., Unosson, C., Cardew, S., Moore, E.R., Gomila, M., Nakagawa, Y., Janssens, D., De Vos, P., Peiren, J., Suttels, T., Clermont, D., Bizet, C., Sakamoto, M., Iida, T., Kudo, T., Kosako, Y., Oshida, Y., Ohkuma, M., R Arahal, D., Spieck, E., Pommerening Roeser, A., Figge, M., Park, D., Buchanan, P., Cifuentes, A., Munoz, R., Euzéby, J.P., Schleifer, K.H., Ludwig, W., Amann, R., Glöckner, F.O. and Rosselló-Móra, R. 2013. Sequencing Orphan Species Initiative (SOS): Filling THE GAPS in the 16S rRNA Gene sequence database for all species with validly published names. Systematic and Applied Microbiology 36:69-73, doi:10.1016/j.syapm.2012.12.006.

Youngwilai, A., Kidkhunthod, P., Jearanaikoon, N., Chaiprapa, J., Supanchaiyamat, N., Hunt, A.J., Ngernyen, Y., Ratpukdi, T., Khan, E. and Siripattanakul-Ratpukdi, S. 2020. Simultaneous manganese adsorption and biotransformation by Streptomyces violarus strain SBP1 cell-immobilized biochar. Science of the Total Environment 713:136708, doi:10.1016/j.scitotenv.2020.136708.

Zhang, M. and Wang, H. 2016. Preparation of immobilized sulfate reducing bacteria (SRB) granules for effective bioremediation of acid mine drainage and bacterial community analysis. Minerals Engineering 92:63-71, doi:10.1016/j.mineng.2016.02.008.

Zolnikov, T.R. and Ramirez-Ortiz, D. 2018. A systematic review on the management and treatment of mercury in artisanal gold mining. Science of the Total Environment 633:816-824.

Żur, J., Wojcieszyńska, D. and Guzik, U. 2016. Metabolic responses of bacterial cells to immobilization. Molecules 21:1-15, doi:10.3390/molecules21070958.

Downloads

Submitted

13-08-2022

Accepted

07-10-2022

Published

01-01-2023

How to Cite

Rohmah, D. N., & Retnaningrum, E. (2023). Assessment and bioremediation of mercury pollutants by highly mercury-resistant bacteria immobilized in biochar from small-scale artisanal gold mining areas. Journal of Degraded and Mining Lands Management, 10(2), 4061–4072. https://doi.org/10.15243/jdmlm.2023.102.4061

Issue

Section

Research Article