Abstract
Arsenic (As) resistant indigenous bacteria with discrete minimum inhibitory concentration values for arsenate [As(V)] and arsenite [As(III)] were isolated from the paddy fields of different regions of Chhattisgarh, India, following enrichment culture technique. Evaluation of the plant growth promoting (PGP) properties of the isolates revealed that two rod-shaped Gram-positive bacteria viz., ARP2 and ART2 acquired various PGP traits, including phosphate solubilization, production of siderophore, indole acetic acid, ammonia, and exopolysaccharide. Both the isolates significantly increased (40–80%) the root length of Oryza sativa L. even under As-exposure. Sequencing of 16S rRNA gene identified these isolates as Bacillus nealsonii strain ARP2 and Bacillus tequilensis strain ART2, respectively. Isolate ARP2 exhibited arsenate reductase activity thereby rapidly reduced As(V) into As(III), achieving a reduction rate of 37.5 μM min−1. Alike, strain ART2 was capable of oxidizing As(III) into As(V) via arsenite oxidase enzyme, and revealed the oxidation rate of 21.8 μM min−1. Quantitative estimation of As through atomic absorption spectrophotometer revealed that the isolates ARP2 and ART2 removed 93 ± 0.2% and 77 ± 0.14% of As(V) and As(III), respectively, from As-containing culture media. The FTIR analysis showed the interaction of As with the cell membrane and was further confirmed by SEM and TEM techniques, which marked the increase in cell volume owing to successive accumulation of As. The As-resistant and PGP properties of above two isolates demonstrates their potentiality for sustainable bioremediation of As, and establishment of flora in As-rich environment.
Similar content being viewed by others
References
Abbas SZ, Riaz M, Ramzan N, Zahid MT, Shakoori FR, Rafatullah M (2015) Isolation and characterization of arsenic resistant bacteria from waste water. Braz J Microbiol 45:1309–1315
Abdel-Lateef AM, Mohamed RA, Mahmoud HH (2013) Determination of arsenic (III) and (V) species in some environmental samples by atomic absorption spectrometry. Adv Chem Sci 2:110–113
Alexander DB, Zuberer DA (1991) Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol Fert Soils 12:39–45
Anderson CR, Cook GM (2004) Isolation and characterization of arsenate reducing bacteria from arsenic contaminated sites in New Zealand. Curr Microbiol 48:341–347
Anderson GL, Williams J, Hille R (1992) The purification and characterization of arsenite oxidase from Alcaligenes faecalis, a molybdenum containing hydroxylase. J Biol Chem 267:23674–23682
Ascar L, Ahumada I, Richter P (2008) Influence of redox potential (Eh) on the availability of arsenic species in soils and soils amended with biosolid. Chemosphere 72:1548–1552
Banerjee S, Datta S, Chattyopadhyay D, Sarkar P (2011) Arsenic accumulating and transforming bacteria isolated from contaminated soil for potential use in bioremediation. J Environ Sci Health Part A 46:1736–1747
Biswas R, Sarkar A (2018) Characterization of arsenite-oxidizing bacteria to decipher their role in arsenic bioremediation. Prep Biochem Biotechnol 11:1–8
Cruz K, Guézennec J, Barkay T (2017) Binding of Hg by bacterial extracellular polysaccharide: a possible role in Hg tolerance. Appl Microbiol Biotechnol 101:5493–5503
Dey U, Chatterjee S, Mondal NK (2016) Isolation and characterization of arsenic-resistant bacteria and possible application in bioremediation. Biotechnol Rep (Amst) 10:1–7
Dye DW (1962) The inadequacy of the usual determinative tests for the identification of Xanthomonas sp. Nat Sci 5:393–416
Fiske CH, Subbarow Y (1925) A colorimetric determination of phosphorus. J Biol Chem 66:375–400
Garelick H, Jones H, Dybowska A, Valsami-Jones E (2008) Arsenic pollution sources. Rev Environ Contam Toxicol 197:17–60
Ghosh P, Rathinasabapathi B, Teplitski M, Ma LQ (2015) Bacterial ability in AsIII oxidation and AsV reduction: Relation to arsenic tolerance, P uptake, and siderophore production. Chemosphere 138:995–1000
Gordon SA, Weber RP (1951) Colorimetric estimation of indole acetic acid. Plant Physiol 26:192–195
Gouda S, Kerry RG, Das G, Paramithiotis S, Shin HS, Patra JK (2018) Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbiol Res 206:131–140
Hare V, Chowdhary P, Baghel VS (2017) Influence of bacterial strains on Oryza sativa grown under arsenic tainted soil: accumulation and detoxification response. Plant Physiol Biochem 119:93–102
Hartmann M, Berditsch M, Hawecker J, Ardakani MF, Gerthsen D, Ulrich AS (2010) Damage of the bacterial cell envelope by antimicrobial peptides gramicidin and PGLa as revealed by transmission and scanning electron microscopy. Antimicrob Agents Chemother 54:3132–3142
Harun-Or-Rashid M, Kim HJ, Yeom SI, Yu HA, Manir MM, Moon SS, Kang YJ, Chung YR (2018) Bacillus velezensis YC7010 enhances plant defenses against grown planthopper through transcriptomic and metabolic changes in Rice. Front Plant Sci 9:1904
He H, Ye Z, Yang D, Yan J, Xiao L, Zhong T, Yuan M, Cai X, Fang Z, Jing Y (2013) Characterization of endophytic Rahnella sp. JN6 from Polygonum pubescens and its potential in promoting growth and Cd, Pb, Zn uptake by Brassica napus. Chemosphere 90:1960–1965
Huang GH, Tian HH, Liu HY, Fan XW, Liang Y, Li YZ (2013) Characterization of plant-growth-promoting effects and concurrent promotion of heavy metal accumulation in the tissues of the plants grown in the polluted soil by Burkholderia strain LD-11. Int J Phytoremed 15:991–1009
Kruger MC, Bertin PN, Heipieper HJ, Arsène-Ploetze F (2013) Bacterial metabolism of environmental arsenic mechanisms and biotechnological applications. Appl Microbiol Biotechnol 97:3827–3841
Li Y, Wang Q, Wang L, He LY, Sheng XF (2016) Increased growth and root Cu accumulation of Sorghum sudanense by endophytic Enterobacter sp. K3–2: Implications for Sorghum sudanense biomass production and phytostabilization. Ecotoxicol Environ Saf 124:163–168
Liao VH, Chu YJ, Su YC, Hsiao SY, Wei CC, Liu CW, Liao CM, Shen WC, Chang FJ (2011) Arsenite-oxidizing and arsenate-reducing bacteria associated with arsenic-rich groundwater in Taiwan. J Contam Hydrol 123:20–29
Lièvremont D, Bertin PN, Lett MC (2009) Arsenic in contaminated waters: biogeochemical cycle, microbial metabolism and biotreatment processes. Biochimie 91:1229–1237
Mallick I, Hossain ST, Sinha S, Mukherjee SK (2014) Brevibacillus sp. KUMAs2, a bacterial isolate for possible bioremediation of arsenic in rhizosphere. Ecotoxicol Environ Saf 107:236–244
Mandal BK, Suzuki KT (2002) Arsenic round the world: a review. Talanta 58:201–235
Naureen A, Rehman A (2016) Arsenite oxidizing multiple metal resistant bacteria isolated from industrial effluent: their potential use in wastewater treatment. World J Microbiol Biotechnol 32:133
Nookongbut P, Kantachote D, Krishnan K, Megharaj M (2017) Arsenic resistance genes of As-resistant purple nonsulfur bacteria isolated from As-contaminated sites for bioremediation application. J Basic Microbiol 57:316–324
Olanrewaju OS, Glick BR, Babalola OO (2017) Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol 33:197
Pandey N, Bhatt R (2015) Arsenic resistance and accumulation by two bacteria isolated from a natural arsenic contaminated site. J Basic Microbiol 55:1275–1286
Pandey N, Bhatt R (2016) Role of soil associated Exiguobacterium in reducing arsenic toxicity and promoting plant growth in Vigna radiata. Eur J Soil Biol 75:142–150
Pandey N, Keshavkant S (2019) Characterization of arsenic resistant plant-growth promoting indigenous soil bacteria isolated from Center-East regions of India. J Basic Microbiol. https://doi.org/10.1002/jobm.201800658
Patel PC, Goulhen F, Boothman C, Gault AG, Charnock JM, Kalia K, Lloyd JR (2007) Arsenate detoxification in a Pseudomonad hypertolerant to arsenic. Arc Microbiol 187:171–183
Paul D, Kazy SK, Banerjee TD, Gupta AK, Pal T, Sar P (2015) Arsenic biotransformation and release by bacteria indigenous to arsenic contaminated groundwater. Bioresour Technol 188:14–23
Płociniczak T, Sinkkonen A, Romantschuk M, Sułowicz S, Piotrowska-Seget Z (2016) Rhizospheric bacterial strain Brevibacterium casei MH8a colonizes plant tissues and enhances Cd, Zn, Cu phytoextraction by White Mustard. Front Plant Sci 7:101
Rajkumar M, Ma Y, Freitas H (2013) Improvement of Ni phytostabilization by inoculation of Ni resistant Bacillus megaterium SR28C. J Environ Manag 128:973–980
Rosen BR, Liu ZJ (2009) Transport pathways for arsenic and selenium: a mini review. Environ Int 35:512–515
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol 4:406–425
Shagol CC, Krishnamoorthy R, Kim K, Sundaram S, Sa T (2014) Arsenic-tolerant plant-growth-promoting bacteria isolated from arsenic-polluted soils in South Korea. Environ Sci Pollut Res Int 21:9356–9365
Tsai SL, Singh S, Chen W (2009) Arsenic metabolism by microbes in nature and the impact on arsenic remediation. Curr Opin Biotechnol 20:659–667
Vishnoi N, Dixit S, Singh DP (2016) Differential pattern of arsenic binding by the cell wall in two arsenite tolerant Bacillus strains isolated from arsenic contaminated soil. Cell Mol Biol 62:3
Wang G, Huang Y, Li J (2011) Bacteria live on arsenic analysis of microbial arsenic metabolism—a review. Wei Sheng Wu Xue Bao 51:154–160
Wu YH, Feng SX, Li B, Mi XM (2010) The characteristics of Escherichia coli adsorption of arsenic (III) from aqueous solution. World J Microbiol Biotechnol 26:249–256
Wu D, Zhang Z, Gao Q, Ma Y (2018) Isolation and characterization of aerobic, culturable, arsenic-tolerant bacteria from lead-zinc mine tailing in southern China. World J Microbiol Biotechnol 34:177
Yamamura S, Amachi S (2014) Microbiology of inorganic arsenic: From metabolism to bioremediation. J Biosci Bioeng 118:1–9
Yang R, Luo C, Chen Y, Wang G, Xu Y, Shen Z (2013) Copper-resistant bacteria enhance plant growth and copper phytoextraction. Int J Phytoremed 15:573–584
Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol 181:777–794
Acknowledgements
The authors are thankful to the Microbial Type Culture Collection and Gene Bank, Chandigarh, for 16S rRNA sequencing. We extend our gratitude to Dr. Amit Dubey, Scientist 'D', Chhattisgarh Council of Science & Technology, Raipur, for HG-AAS facilities. Advanced Instrumentation Research Facility (AIRF) of JNU, New Delhi is equally acknowledged for SEM and TEM analysis.
Funding
The study was supported by the Science and Engineering Research Board, New Delhi, through National Post-Doctoral Fellowship (Sanction No: PDF/2016/002813, dated 16.08.2017) and the project of Chhattisgarh Council of Science & Technology, Raipur (Sanction No: 2819/CCOST/MRP/2017, dated 27.11.2017).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Pandey, N., Manjunath, K. & Sahu, K. Screening of plant growth promoting attributes and arsenic remediation efficacy of bacteria isolated from agricultural soils of Chhattisgarh. Arch Microbiol 202, 567–578 (2020). https://doi.org/10.1007/s00203-019-01773-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-019-01773-2