Profiling of heavy metal(loid)-resistant bacterial community structure by metagenomic-DNA fingerprinting using PCR–DGGE for monitoring and bioremediation of contaminated environment

Abstract

Frequent exposure of microbes to hazardous metalloids/heavy metals in contaminated environment results in the development of heavy metal(loid)-resistance properties. The study attempted to assess the profile of elevated arsenic (As), cadmium (Cd) and mercury (Hg)—resistant bacterial community structures of sludge (S1, India), sludge and sediment (S2 and S3, Japan) and sediment (S4, Vietnam) samples by metagenomic-DNA fingerprinting using polymerase chain reaction-denaturing gradient gel electrophoresis (PCR–DGGE) for monitoring and bioremediation of hazardous metal(loid) contamination in environment. The results revealed that As-resistant bacteria were dominant compared to Cd- and Hg-resistant bacteria with higher species diversity (Lysinibacillus sp., Uncultured soil bacterium clone, Staphylococcus sciuri, Bacillus fastidiosus, Bacillus niacini, Clostridium sp. and Bacillus sp.) in S1 and S4 than that of S2 and S3 samples. The occurrence of dominant As-resistant bacteria may indicate arsenic contamination in the investigated coastal habitats of India, Japan and Vietnam. The As-, Cd- and Hg-resistant bacteria/bacterial consortiums showed appreciable uptake ability of respective metal(loid) (0.042–0.125 mg As/l, 0.696–0.726 mg Cd/l and 0.34–0.412 mg Hg/l). Therefore, it might be concluded that the profiling of metalloids/heavy metal-resistant bacterial community structure by metagenomic-DNA fingerprinting using PCR–DGGE could be used to explore high metal(loid)-resistant bacteria for applying in metal(loid) bioremediation and as an indicator for monitoring hazardous metal(loid) contamination in environment.

Keywords

Metal(loid) / Resistant / Metagenomics / Bacterial diversity / Environmental contamination / Bioremediation

References

[1] Abbas SZ, Riaz M, Ramzan N, Zahid MT, Shakoori FR, Rafatullah M. Isolation and characterization of arsenic resistant bacteria from wastewater. Braz J Microbiol, 2014, 45: 1309-1315

[2] Abbas SZ, Rafatullah M, Ismail N, Lalung J. Isolation and characterization of Cd-resistant bacteria from industrial wastewater. Desalin Water Treat, 2015, 56: 1037-1046

[3] Altimira F, Yáñez C, Bravo G, González M, Rojas LA, Seeger M. Characterization of copper–resistant bacteria and bacterial communities from copper–polluted agricultural soils of central Chile. BMC Microbiol, 2012, 12: 193

[4] Bhakta JN. Rathoure AK, Dhatwalia VK. Microbial response against metal toxicity. Toxicity and waste management using bioremediation, 2016 PA IGI Global 75-96

[5] Bhakta JN. Bhakta JN. Metal toxicity in microorganism. Handbook of research on inventive bioremediation techniques, 2017 PA IGI Global 1-23

[6] Bhakta JN, Munekage Y. Role of ecosystem components in Cd removal process of aquatic ecosystem. Ecol Eng, 2008, 32: 274-280

[7] Bhakta JN, Munekage Y. Mercury removal by some soils of Japan from aquatic environment. Environ Eng Manag J, 2010, 9(4): 503-510

[8] Bhakta JN, Ohnishi K, Munekage Y, Iwasaki K. Isolation and probiotic characterization of arsenic–resistant lactic acid bacteria for uptaking arsenic. Int J Chem Biol Eng, 2010, 3: 4

[9] Bhakta JN, Munekage Y, Ohnishi K, Jana BB. Isolation and identification of cadmium and lead resistant lactic acid bacteria for applying as metal removing probiotic. Int J Environ Sci Technol, 2012, 9: 433-440

[10] Bhakta JN, Ohnishi K, Munekage Y, Iwasaki K, Wei M. Characterization of lactic acid bacteria–based probiotics as heavy metals sorbents. J Appl Microbiol, 2012, 112: 1193-1206

[11] Bhakta JN, Munekage Y, Ohnishi K, Jana BB, Balcazar JL. Isolation and characterization of cadmium and arsenic absorbing bacteria for bioremediation. Water Air Soil Pollut, 2014, 225(10): 2151

[12] Bidstrup PC. Toxicity of mercury and its compounds, 1964 Amsterdam Elsevier

[13] Campbell JH, Clark JS, John CZ. PCR–DGGE comparison of bacterial community structure in fresh and archived soils sampled along a Chihuahuan Desert elevational gradient. Microb Ecol, 2009, 57(2): 261-266

[14] Carpio IE, Machado-Santelli G, Sakata SK, Ferreira Filho SS, Rodrigues DF. Copper removal using a heavy-metal resistant microbial consortium in a fixed-bed reactor. Water Res, 2014, 62: 156-166

[15] Carpio IEM, Franco DC, Sato MIZ, Sakata S, Pellizari VH, Ferreira Filho SS, Rodrigues DF. Biostimulation of metal-resistant microbial consortium to remove zinc from contaminated environments. Sci Total Environ, 2016, 550: 670-675

[16] Curtis TP, Sloan WT. Prokaryotic diversity and its limits: microbial community structure in nature and implications for microbial ecology. Curr Opin Microbiol, 2004, 7: 221-226

[17] Dinsdale EA, Edwards RA, Hall D Functional metagenomic profiling of nine biomes. Nature, 2008, 452: 629-632

[18] Figueiredo NL, Canário J, O’Driscoll NJ, Duarte A, Carvalho C. Aerobic Mercury-resistant bacteria alter Mercury speciation and retention in the Tagus Estuary (Portugal). Ecotoxicol Environ Saf, 2016, 124: 60-67

[19] Gadd GM. Heavy metal accumulation by bacteria and other microorganisms. Experientia, 1990, 46: 834-840

[20] Giller K, Witter E, McGrath SP. Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem, 1998, 30: 1389-1414

[21] Gupta UC, Gupta SC. Trace element toxicity relationships to crop production and livestock and human health: implications for management. Commun Soil Sci Plant Anal, 1998, 29(11–14): 1491-1522

[22] Handelsman J. Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev, 2004, 68: 669-685

[23] Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM. Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem Biol, 1998, 5: R245-R249

[24] Hoover J, Gonzales M, Shuey C, Barney Y, Lewis J. Elevated arsenic and uranium concentrations in unregulated water sources on the Navajo Nation, USA. Expo Health, 2017, 9: 113-124

[25] Jafari SA, Cheraghi S. Mercury removal from aqueous solution by dried biomass of indigenous Vibrio parahaemolyticus PG02: kinetic, equilibrium, and thermodynamic studies. Int Biodeterior Biodegrad, 2014, 92: 12-19

[26] Kumar S, Krishnani KK, Bhushan B, Brahmane MP (2015) Metagenomics: retrospect and prospects in high throughput age. Biotech Res Int 2015, Article ID 121735, p 13. https://dx.doi.org/10.1155/2015/121735

[27] Kunin V, Copeland A, Lapidus A, Mavromatis K, Hugenholtz P. A bioinformatician’s guide to metagenomics. Microbiol Mol Biol Rev, 2008, 72: 557-578

[28] Kvasnova S, Hamarová L, Pristaš P. Zinc bioaccumulation by microbial consortium isolated from nickel smelter sludge disposal site. Nova Biotechnol Chim, 2017, 16: 48-53

[29] Li Z, Xu J, Tang C, Wu J, Muhammad A, Wang H. Application of 16S rRNA PCR amplification and DGGE fingerprinting for detection of shift microbial community diversity in Cu–, Zn– and Cd–contaminated paddy soil. Chemosphere, 2006, 62: 1374-1380

[30] Lim KT, Shukor MY, Wasoh H (2014) Physical, chemical, and biological methods for the removal of arsenic compounds. BioMed Res Int 2014, Article ID 503784, p 9. https://dx.doi.org/10.1155/2014/503784

[31] Logue JB, Bürgmann H, Robinson CT. Progress in the ecological genetics and biodiversity of freshwater bacteria. Bioscience, 2008, 58: 103-113

[32] Martínez-Alonso M, Escolano J, Montesinos E, Gaju N. Diversity of the bacterial community in the surface soil of a pear orchard based on 16S rRNA gene analysis. Int Microbiol, 2010, 13(3): 123-134

[33] Min-sheng H, Jing P, Le-ping Z. Removal of heavy metals from aqueous solutions using bacteria. J Shanghai Univ, 2001, 5(3): 253-259

[34] O’Brien S, Buckling A. Hijacking the social lives of microbial populations to clean up heavy metal contamination. EMBO Rep, 2015, 16: 1241-1245

[35] Pettit RK. Soil DNA libraries for anticancer drug discovery. Cancer Chemother Pharmacol, 2004, 54: 1-6

[36] Qing H, Min-Na D, Hong-Yan Q, Xiang-Ming X, Guo-Qiang Z, Min Y. Detection, isolation, and identi cation of cadmium–resistant bacteria based on PCR–DGGE. J Environ Sci, 2007, 19: 1114-1119

[37] Ranjard L, Echairi A, Nowak V, Lejon D, Nouaim R, Chaussod R. Field and microcosm experiments to evaluate the effects of agricultural Cu treatment on the density and genetic structure of microbial communities in two different soils. FEMS Microbiol Ecol, 2006, 58: 303-315

[38] Ruiz-Barba JL, Maldonado A, Jiménez-Díaz R. Small–scale total DNA extraction from bacteria and yeast for PCR applications. Anal Biochem, 2005, 347: 333-335

[39] Saranya K, Sundaramanickam A, Shekhar S, Swaminathan S, Balasubramanian T (2017) Bioremediation of mercury by Vibrio fluvialis screened from industrial effluents. BioMed Res Int, Article ID 6509648, 6 pages. https://dx.doi.org/10.1155/2017/6509648

[40] Schmeisser C, Steele H, Streit WR. Metagenomics, biotechnology with non–culturable microbes. Appl Microbiol Biotechnol, 2007, 75: 955-962

[41] Signes-Pastor AJ, Carey M, Vioque J, Navarrete-Mun˜oz EM, Rodrıguez-Dehli C, Tardon A, Begon˜a-Zubero M, Santa-Marina L, Vrijheid M, Casas M, Llop S, Gonzalez-Palacios S, Meharg AA. Urinary arsenic speciation in children and pregnant women from Spain. Expo Health, 2017, 9: 105-111

[42] Singh PK, Singh AL, Kumar A, Singh MP. Mixed bacterial consortium as an emerging tool to remove hazardous trace metals from coal. Fuel, 2012, 102: 227-230

[43] Sinha A, Pant KK, Khare SK. Studies on mercury bioremediation by alginate immobilized mercury tolerant Bacillus cereus cells. Int Biodeterior Biodegrad, 2012, 71: 1-8

[44] Smalla K, Oros-Sichler M, Milling A, Heuer H, Baumgarte S, Becker R, Neuber G, Kropf S, Ulrich A, Tebbe CC. Bacterial diversity of soils assessed by DGGE, T-RFLP and SSCP fingerprints of PCR–amplified 16S rRNA gene fragments: do the different methods provide similar results?. J Microbiol Methods, 2007, 69(3): 470-479

[45] Streit WR, Schmitz RA. Metagenomics—the key to the uncultured microbes. Curr Opin Microbiol, 2004, 7: 492-498

[46] Torsvik V, Ovreas L. Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol, 2002, 5: 240-245

[47] Umar AF, Tahir F, Agbo EB. Polymerase chain reaction-denaturing gradient gel electrophoresis (PCR–DGGE) profile of bacterial community from agricultural soils in Bauchi, North-East Nigeria. Adv Microbiol, 2017, 7: 480-486

[48] Wang Y, Shi J, Wang H, Lin Q, Chen X, Chen Y. The influence of soil heavy metals pollution on soil microbial biomass, enzyme activity, and community composition near a copper smelter. Ecotoxicol Environ Saf, 2007, 67: 75-81

[49] Watts MP, Khijniak TV, Boothman C, Lloyd JR (2015) Treatment of alkaline Cr(VI)-contaminated leachate with an alkaliphilic metal-reducing bacterium. Appl Environ Microbiol 81(16): eScholarID:268368

[50] Wei G, Fan L, Zhu W, Fu Y, Yu J, Tang M. Isolation and characterization of the heavy metal resistant bacteria CCNWRS33–2 isolated from root nodule of Lepedeza cuneata in gold mine tailings in China. J Hazard Mater, 2009, 162: 50-56

[51] Yao X-F, Zhang J-M, Tian L, Guob J-H. The effect of heavy metal contamination on the bacterial community structure at Jiaozhou Bay, China. Braz J Microbiol, 2017, 48: 71-78

Funding

Japan Society for the promotion of Science (JSPS) (FY2009 JSPS)