Abstract
The metal tolerant plant growth-promoting bacteria (MT-PGPB) adapt different strategies to cope up with the metal stressed soil and improve the growth of plants in such areas. The present study was therefore, designed to isolate MT-PGPBs from the coal dumping area of Dudhnoi, Goalpara, Assam, India. In this study, a total of 10 bacterial strains were obtained from the coal dumping area and 21 from reference forest soil using nutrient agar media. Among them, four bacterial strains (Bacillus toyonensis DD1, B. mycoides DD2, B. velezensis DD9 and B. flexus DD10) obtained from the coal dumping area could tolerate two or more heavy metals (Zn, Fe, Pb, Ni, Cu, Cd, Cr). Besides, these metal tolerating bacterial isolates were evaluated for their plant growth-promoting activities like production of indole-3-acetic acid, siderophore, ACC deaminase activity, and phosphate solubilization. The results showed that three isolates were capable of solubilizing phosphate, produced IAA, and showed ACC deaminase activity, while all 4 isolates produced siderophore. Hence, these four bacterial isolates might help in microbe assisted phytoremediation in the future.
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.
Code availability
Not applicable.
Abbreviations
- MT-PGPB:
-
Metal tolerant plant growth-promoting bacteria
- FE-SEM:
-
Field emission scanning electron microscopy
- MC:
-
Moisture content
- TOC:
-
Total organic carbon
- TN:
-
Total nitrogen
- AvP:
-
Available phosphorus
- AvK:
-
Available potassium
- AAS:
-
Atomic absorption spectrophotometry
- NA:
-
Nutrient agar
- CFU:
-
Colony forming unit
- MIC:
-
Minimum inhibitory concentration
- IAA:
-
Indole-3-Acetic Acid
- ACC:
-
Deaminase, 1-aminocyclopropane-1-carboxylate deaminase
- CAS:
-
Chrome azurol S
- LB:
-
Luria-Bertani
- CTAB:
-
Cetyl trimethylammonium bromide
References
Afzal AM, Rasool MH, Waseem M, Aslam B (2017) Assessment of heavy metal tolerance and biosorptive potential of Klebsiella variicola isolated from industrial effluents. AMB Expr 7:184. https://doi.org/10.1186/s13568-017-0482-2
Ahemad M (2015) Phosphate-solubilizing bacteria-assisted phytoremediation of metalliferous soils: a review. 3 Biotech 5:111–121. https://doi.org/10.1007/s13205-014-0206-0
Ahemad M (2019) Remediation of metalliferous soils through the heavy metal resistant plant growth promoting bacteria: paradigms and prospects. Arab J Chem 12(7):1365–1377. https://doi.org/10.1016/j.arabjc.2014.11.020
Anonymous (2011) Methods manual, soil testing in India, Department of Agriculture & Cooperation, Ministry of Agriculture. Government of India, New Delhi
Barman D, Dkhar MS (2018) Plant growth-promoting potential of endophytic bacteria isolated from Costus speciosus in tropical deciduous forest of Eastern Himalaya. Proc Natl Acad Sci India Sect B Biol Sci 89:841–852. https://doi.org/10.1007/s40011-018-0998-5
Barman D, Jha DK, Bhattacharjee K (2020) Metalotolerant bacteria: insights into bacteria thriving in metal contaminated areas. In: Singh RP, Manchanda G, Maurya IK, Wei Y (eds) Microbial versatility in varied environments. Springer Nature, Singapore, pp 135–166
Bashan Y, Wolowelsky J (1987) Soil samplers for quantifying microorganisms. Soil Sci 143:132–138
Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth promoting rhizobacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250. https://doi.org/10.1016/j.soilbio.2004.07.033
Benmalek Y, Fardeau ML (2016) Isolation and characterization of metal-resistant bacterial strain from wastewater and evaluation of its capacity in metal-ions removal using living and dry bacterial cells. Int J Environ Sci Technol 13:2153–2162. https://doi.org/10.1007/s13762-016-1048-6
Bhattacharjee K, Banerjee S, Joshi SR (2012) Diversity of Streptomyces spp. in Eastern Himalayan region – computational RNomics approach to phylogeny. Bioinformation 8(12):548–554. https://doi.org/10.6026/97320630008548
Bhattacharjee K, Banerjee S, Bawitlung L, Krishnappa D, Joshi SR (2014) A study on parameters optimization for degradation of endosulfan by bacterial consortia isolated from contaminated soil. Proc Natl Acad Sci India Sect B Biol Sci 84:657. https://doi.org/10.1007/s40011-013-0223-5
Bhattacharjee K, Kumar S, Palepu NR, Patra PK, Rao KM, Joshi SR (2017) Structure elucidation and in silico docking studies of a novel furopyrimidine antibiotics synthesized by endolithic bacterium Actinomadura sp. AL2. World J Microbiol Biotechnol 33:178. https://doi.org/10.1007/s11274-017-2343-1
Bian ZF, Lei SG, Inyang HI, Chang LQ, Zhang RC, Zhou CJ, He X (2009) Integrated method of RS and GPR for monitoring the changes in the soil moisture and groundwater environment due to underground coal mining. Environ Geol 57:131–142. https://doi.org/10.1007/s00254-008-1289-x
Bray RH, Kurtz LT (1945) Determination of total, organic and available forms of phosphorus in soils. Soil Sci 59(1):39–46
Briffa J, Sinagra E, Blundell R (2020) Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon 6:e04691. https://doi.org/10.1016/j.heliyon.2020.e04691
Cengiz S, Karaca AC, Cakir I, Uner HB, Sevindik A (2004) SEM-EDS analysis and discrimination of forensic soil. Forensic Sci Int 141:33–37. https://doi.org/10.1016/j.forsciint.2003.12.006
Chabukdhara M, Singh OP (2016) Coal mining in northeast India: an overview of environmental issues and treatment approaches. Int J Coal Sci Technol 3:87–96. https://doi.org/10.1007/s40789-016-0126-1
Domingues VS, de Souza Monteiro A, Julio ADL, Queiroz ALL, dos Santos VL (2020) Diversity of metal-resistant and tensoactive-producing culturable heterotrophic bacteria isolated from a copper mine in Brazilian amazonia. Sci Rep 10:6171. https://doi.org/10.1038/s41598-020-62780-8
Dutta M, Khare P, Chakravarty S, Saikia D, Saikia BK (2018) Physico-chemical and elemental investigation of aqueous leaching of high sulfur coal and mine overburden from Ledo coalfield of Northeast India. Int J Coal Sci Technol 5:265–281. https://doi.org/10.1007/s40789-018-0210-9
Ezeokoli OT, Bezuidenhout CC, Maboeta MS, Khasa DP, Adeleke RA (2020) Structural and functional differentiation of bacterial communities in post-coal mining reclamation soils of South Africa: bioindicators of soil ecosystem restoration. Sci Rep 10:1759. https://doi.org/10.1038/s41598-020-58576-5
Franco-Duarte R, Cernakova L, Kadam S, Kaushik KS, Salehi B, Bevilacqua A, Corbo MR, Antolak H, Dybka-Stępien K, Leszczewicz M, Relison Tintino S, Alexandrino de Souza VC, Sharifi-Rad J, Coutinho H, Martins N, Rodrigues CF (2019) Advances in chemical and biological methods to identify microorganisms-from past to present. Microorganisms 7(5):130. https://doi.org/10.3390/microorganisms7050130
Gupta K, Chatterjee C, Gupta B (2012) Isolation and characterization of heavy metal tolerant Gram-positive bacteria with bioremedial properties from municipal waste rich soil of Kestopur canal (Kolkata), West Bengal, India. Biologia 65:827–836. https://doi.org/10.2478/s11756-012-0099-5
Hassen A, Saidi N, Cherif M, Boudabous A (1998) Resistance of environmental bacteria to heavy metal. Bioresource Technol 64:7–15. https://doi.org/10.1016/S0960-8524(97)00161-2
Holt JG, Krieg NR, PHA S, Staley JT, Williams ST (1994) Bergey’s manual of determinative bacteriology, 9th edn. Lippincott Williams & Wilkins, Baltimore
Jain D, Kour R, Bhojiya AA, Meena RH, Singh A, Mohanty SR, Rajpurohit D, Ameta KD (2020) Zinc tolerant plant growth promoting bacteria alleviates phytotoxic effects of zinc on maize through zinc immobilization. Sci Rep 10:13865. https://doi.org/10.1038/s41598-020-70846-w
Jing XB, He N, Zhang Y, Cao YR, Xu H (2012) Isolation and characterization of heavy-metal-mobilizing bacteria from contaminated soils and their potential in promoting Pb, Cu, and Cd accumulation by Coprinus comatus. Can J Microbiol 58:45–53. https://doi.org/10.1139/w11-110
Johnson LF, Curl EA (1972) Methods for research on the ecology of soil-borne plant pathogens. Burgess Publishing Co, Minneapolis
Juwarkar AA, Jambhulkar HP (2008) Phytoremediation of coal mine spoil dump through integrated biotechnological approach. Bioresource Technol 99(11):4732–4741. https://doi.org/10.1016/j.biortech.2007.09.060
Karami A, Shamsuddin ZH (2010) Phytoremediation of heavy metals with several efficiency enhancer methods. Afr J Biotechnol 9:3689–3698. https://doi.org/10.5897/AJB09.854
Khan SR, Singh SK, Rastogi N (2017) Heavy metal accumulation and ecosystem engineering by two common mine site-nesting ant species: implications for pollution-level assessment and bioremediation of coal mine soil. Environ Monit Assess 189:195. https://doi.org/10.1007/s10661-017-5865-y
Khanna K, Jamwal VL, Gandhi SG, Ohri P, Bhardwaj R (2019) Metal resistant PGPR lowered Cd uptake and expression of metal transporter genes with improved growth and photosynthetic pigments in Lycopersicon esculentum under metal toxicity. Sci Rep 9:5855. https://doi.org/10.1038/s41598-019-41899-3
Lazar V, Cernat R, Balotescu C, Cotar A, Coipan E, Cojocaru C (2002) Correlation between multiple antibiotic resistance and heavy-metal tolerance among some E.coli strains isolated from polluted waters. Bacteriol Virusol Parazitol Epidemiol 47(3–4):155–160
Lenart A, Wolny-Koladka K (2013) The effect of heavy metal concentration and soil pH on the abundance of selected microbial groups within ArcelorMittal Poland steelworks in Cracow. Bull Environ Contam Toxicol 90:85–90. https://doi.org/10.1007/s00128-012-0869-3
Lima de Silva AA, de Carvalho MA, de Souza SA, Dias PM, da Silva Filho RG, de Meirelles Saramago CS, de Melo Bento CA, Hofer E (2012) Heavy metal tolerance (Cr, Ag and Hg) in bacteria isolated from sewage. Braz J Microbiol 43(4):1620–1631. https://doi.org/10.1590/S1517-838220120004000047
Ma Y, MNV P, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258. https://doi.org/10.1016/j.biotechadv.2010.12.001
Ma K, Zhang Y, Ruan M, Guo J, Chai T (2019) Land subsidence in a coal mining area reduced soil fertility and led to soil degradation in arid and semi-arid regions. Int J Environ Res Public Health 16(20):3929. https://doi.org/10.3390/ijerph16203929
Maharana JK, Patel AK (2013) Physico-chemical characterization and mine soil genesis in age series coal mine overburden spoil in chronosequence in a dry tropical environment. J Phylogenet Evol Biol 1(1):1–7. https://doi.org/10.4172/2329-9002.1000101
Makdoh K, Kayang H (2015) Soil physico-chemical properties in coal mining areas of Khliehriat, East Jaintia Hills District, Meghalaya, India. Int Res J Environ Sci 4(10):69–76
Maurya A, Kesharwani L, Mishra MK (2018) Analysis of heavy metal in soil through atomic absorption spectroscopy for forensic consideration. Int J Res Appl Sci Eng Technol 6:1188–1192. https://doi.org/10.22214/ijraset.2018.6173
Mesa V, Navazas A, González-Gil R, González A, Weyens N, Lauga B, JLR G, Sánchez J, Pelaez AI (2017) Use of endophytic and rhizosphere bacteria to improve phytoremediation of arsenic-contaminated industrial soils by autochthonous Betula celtiberica. Appl Environ Microbiol 83(8):e03411–e03416. https://doi.org/10.1128/AEM.03411-16
Mishra J, Singh R, Arora NK (2017) Alleviation of heavy metal stress in plants and remediation of soil by rhizosphere microorganisms. Front Microbiol 8:1706. https://doi.org/10.3389/fmicb.2017.01706
Nath S, Paul P, Roy R, Bhattacharjee S, Deb B (2019) Isolation and identification of metal-tolerant and antibiotic-resistant bacteria from soil samples of Cachar district of Assam, India. SN Appl Sci 1:727. https://doi.org/10.1007/s42452-019-0762-3
Ojuederie OB, Babalola OO (2017) Microbial and plant-assisted bioremediation of heavy metal polluted environments: a review. Int J Environ Res Public Health 14:1504. https://doi.org/10.3390/ijerph14121504
Paul D, Sinha SN (2015) Isolation and characterization of a phosphate solubilizing heavy metal tolerant bacterium from River Ganga, West Bengal, India. Songklanakarin J Sci Technol 37:651–657
Piper CS (1966) Soil and plant analysis. Hans, Bombay
Rajkumar M, Freitas H (2008) Effects of inoculation of plant growth promoting bacteria on Ni uptake by Indian mustard. Bioresour Technol 99:3491–3498. https://doi.org/https://doi.org/10.1016/j.biortech.2007.07.046
Rajkumar M, Ae N, MNV P, 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
Rani MJ, Hemambika B, Hemapriya J, Kannan VR (2010) Comparative assessment of heavy metal removal by immobilized and dead bacterial cells: a biosorption approach. Afr J Environ Sci Technol 4:077–083
Samanta A, Bera P, Khatun M, Sinha C, Pal P, Lalee A, Mandal A (2012) An investigation on heavy metal tolerance and antibiotic resistance properties of bacterial strain Bacillus sp. isolated from municipal waste. J Microbiol Biotech Res 2(1):178–189
Sun W, Xiao E, Krumins V, Dong Y, Li B, Deng J, Wang Q, Xiao T, Liu J (2019) Comparative analyses of the microbial communities inhabiting coal mining waste dump and an adjacent acid mine drainage creek. Microb Ecol 78(3):651–664. https://doi.org/10.1007/s00248-019-01335-5
Tirry N, Joutey NT, Sayel H, Kouchou A, Bahafid W, Asri M, Ghachtouli NE (2018) Screening of plant growth promoting traits in heavy metals resistant bacteria: prospects in phytoremediation. J Genet Eng Biotechnol 16:613–619. https://doi.org/10.1016/j.jgeb.2018.06.004
Tomova I, Stoilova-Disheva M, Lazarkevich I, Vasileva-Tonkova E (2015) Antimicrobial activity and resistance to heavy metals and antibiotics of heterotrophic bacteria isolated from sediment and soil samples collected from two Antarctic islands. Front Life Sci 8:348–357. https://doi.org/10.1080/21553769.2015.1044130
Toth SJ, Prince AL (1949) Estimation of cation exchange capacity and exchangeable calcium, potassium, and sodium contents of soils by flame photometer techniques. Soil Sci 67:439–445
Tripathi N, Singh RS, Chaulya SK (2012) Dump stability and soil fertility of a coal mine spoil in Indian dry tropical environment: a long-term study. Environ Manage 50(4):695–706. https://doi.org/10.1007/s00267-012-9908-4
Ullah A, Heng S, MFH M, Fahad S, Yang X (2015) Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: a review. Environ Exp Bot 117:28–40. https://doi.org/10.1016/j.envexpbot.2015.05.001
Upadhyay N, Verma S, Singh AP, Devi S, Vishwakarma K, Kumar N, Pandey A, Dubey K, Mishra R, Tripathi DK et al (2016) Soil ecophysiological and microbiological indices of soil health: a study of coal mining site in Sonbhadra, Uttar Pradesh. J Soil Sci Plant Nutr 6:778–800. https://doi.org/10.4067/S0718-95162016005000056
Ural N (2021) The significance of scanning electron microscopy (SEM) analysis on the microstructure of improved clay: an overview. Open Geosci 13:197–218. https://doi.org/10.1515/geo-2020-0145
Wagi S, Ahmed A (2019) Bacillus spp.: potent microfactories of bacterial IAA. PeerJ 7:e7258. https://doi.org/10.7717/peerj.7258
Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and proposed modification of the chromic acid titration method. Soil Sci 37(1):29–38
Wilson K (2001) Preparation of genomic DNA from bacteria. Curr Protoc Mol Biol 56(1):2.4.1–2.4.5. https://doi.org/10.1002/0471142727.mb0204s56
World Coal Association, Coal Facts (2011) http://www.worldcoal.org/ resources/coal statistics
Yaseen S, Pal A, Singh S, Skinder BM (2015) Soil quality of agricultural fields in the vicinity of selected mining areas of Raniganj coalfield India. J Environ Anal Toxicol 5:3. https://doi.org/10.4172/2161-0525.1000269
Yilmaz EI (2003) Metal tolerance and biosorption capacity of Bacillus circulans strain EB1. Res Microbiol 154:409–415. https://doi.org/10.1016/S0923-2508(03)00116-5
Yu X, Li Y, Zhang C, Liu H, Liu J, Zheng W, Kang X, Leng X, Zhao K, Gu Y, Zhang X, Xiang Q, Chen Q (2014) Culturable heavy metal-resistant and plant growth promoting bacteria in V-Ti magnetite mine tailing soil from Panzhihua, China. PLoS ONE 9(9):e106618. https://doi.org/10.1371/journal.pone.0106618
Acknowledgments
The authors are highly thankful to the Head, Department of Botany, Gauhati University, Guwahati for providing the required instrumentation facilities under UGC-SAP and DST-FIST. The first author gratefully acknowledges the financial support provided by the Department of Biotechnology, Govt. of India under the DBT-RA Program in Biotechnology and Life Sciences.
Funding
This study was partially supported by the Department of Biotechnology, Government of India under the DBT-RA Program in Biotechnology and Life Sciences. The funders had no role in study design, data collection, and analysis, decision to publish, or preparation of the manuscript.
Author information
Authors and Affiliations
Contributions
DB and DKJ designed the research. DB and ID performed the experiments. DB and DKJ analyzed the data. DB drafted the manuscript. DB and DKJ finalized the manuscript. All authors read and critically reviewed the manuscript.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
All authors have read and approved the final manuscript.
Conflicts of interest/Competing interests
The authors declare that they have no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary material
ESM 1
Docx
Rights and permissions
About this article
Cite this article
Barman, D., Dutta, I. & Jha, D.K. Heavy metal resistant bacteria from coal dumping site with plant growth promoting potentials. Biologia 77, 533–545 (2022). https://doi.org/10.1007/s11756-021-00963-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11756-021-00963-y