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Characterization of cadmium-resistant Klebsiella pneumoniae MCC 3091 promoted rice seedling growth by alleviating phytotoxicity of cadmium

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Abstract

Cadmium (Cd) phytotoxicity in agricultural land is a major global concern now-a-days resulting in very poor yield. Plant growth-promoting rhizobacteria (PGPR)-mediated bioremediation is one of the convenient strategies for detoxification of Cd from the soil and for plant growth promotion under Cd stress. The selected strain K5 was identified as Klebsiella pneumoniae based on MALDI-TOF MS ribosomal protein and 16S rDNA sequence-based homology. The strain possessed several PGP traits viz. IAA production (3413 μg/mL), phosphate solubilization (80.25 ppm), ACC deaminase activity (40 ng α-ketobutyrate/mg protein/h), N2 fixation ability (1.84 μg N2 fixed/h), etc. and has the highest Cd resistance (4000 μg/mL) among Cd-resistant PGPR so far reported. This strain efficiently accumulated Cd and remained viable under Cd stress as confirmed by AAS-TEM-EDX analysis and viability test, respectively. The significant (p < 0.05) positive effect of the strain was reflected in various plant growth parameters like increased seed germination (50 to 90%), root length (5-fold), shoot length (about 2-fold), root fresh weight (> 2-fold), and shoot fresh weight (1.23-fold) under Cd stress compared with uninoculated set. Moreover, the positive impact of this strain on antioxidant enzyme activity (CAT, MDA, SOD) and several other biochemical parameters (proline, α-amylase, protease, total sugar, total protein, chlorophyll content) were also measured that favors plant growth promotion under Cd stress. Besides, the K5 strain also decreased stress-ethylene level under Cd stress and reduction of Cd accumulation in seedling (> 1.5-fold) was conducive to alleviate Cd phytotoxicity. Hence, K. pneumoniae strain K5 can be used as a phytostimulating and Cd-bioremediating biofertilizer for sustainable agriculture in heavy metal-contaminated sites.

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Abbreviations

PGPR:

Plant growth-promoting rhizobacteria

PGP traits:

Plant growth-promoting traits

GC:

Gas chromatography

ACC:

1-aminocyclopropane-1-carboxylic acid

CAT:

Catalase

MDA:

Malondialdehyde

SOD:

Superoxide dismutase

ROS:

Reactive oxygen species

MAP kinase:

Mitogen-activated protein kinase

MALDI-TOF MS:

Matrix-assisted laser desorption/ionization mass spectrometry

TEM:

Transmission electron microscopy

EDX:

Energy dispersive X-ray spectroscopy

References

  • Abbas SZ, Rafatullah M, Ismail N et al (2014) Isolation, identification, characterization, and evaluation of cadmium removal capacity of Enterobacter species. J Basic Microbiol 54:1–9. https://doi.org/10.1002/jobm.201400157

    Article  Google Scholar 

  • Aebi H (1984) Catalase in vitro. In: Methods in enzymology. vol 105. Academic Press, Inc. ISBN 0.12-182005-X

  • Ahmad I, Akhtar MJ, Zahir ZA et al (2014) Cadmium-tolerant bacteria induce metal stress tolerance in cereals. Environ Sci Pollut Res 21:11054–11065. https://doi.org/10.1007/s11356-014-3010-9

    Article  CAS  Google Scholar 

  • Ahmad I, Akhtar MJ, Asghar HN et al (2016) Differential effects of plant growth-promoting rhizobacteria on maize growth and cadmium uptake. J Plant Growth Regul 35:303–315. https://doi.org/10.1007/s00344-015-9534-5

    Article  CAS  Google Scholar 

  • Alkorta I, Hernández-Allica J, Becerril JM et al (2004) Chelate-enhanced phytoremediation of soils polluted with heavy metals. Rev Environ Sci Biotechnol 3:55–70

    Article  CAS  Google Scholar 

  • Andrews JM (2001) Determination of minimum inhibitory concentrations. J Antimicrob Chemother 48:5–16

    Article  CAS  Google Scholar 

  • Aoshima K (2016) Itai-itai disease: renal tubular osteomalacia induced by environmental exposure to cadmium-historical review and perspectives. Soil Sci Plant Nutr. https://doi.org/10.1080/00380768.2016.1159116

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  Google Scholar 

  • Asari S, Tarkowsk D, Rolčík J, Novák O et al (2016) Analysis of plant growth-promoting properties of Bacillus amyloliquefaciens UCMB5113 using Arabidopsis thaliana as hostplant. Planta. https://doi.org/10.1007/s00425-016-2580-9

  • Bal H, Nayak L, Das S et al (2012) Isolation of ACC deaminase producing PGPR from rice rhizosphere and evaluating their plant growth promoting activity under salt stress. Plant Soil. https://doi.org/10.1007/s11104-012-1402-5

  • Bates LS (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Belimov AA, Dietz KJ (2000) Effect of associative bacteria on element composition of barley seedlings grown in solution culture at toxic cadmium concentrations. Microbiol Res 155:113–121

    Article  CAS  Google Scholar 

  • Belimov AA, Hontzeas N, Safronova VI et al (2005) Cadmium-tolerant plant growth-promoting bacteria 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

    Article  CAS  Google Scholar 

  • Benson HJ (1990) Microbiological application—a lab manual in general microbiology, 5th edn. W. C. Brown Publishers, Dubuque

    Google Scholar 

  • Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. W J Microbiol Biotechnol 28:1327–1350. https://doi.org/10.1007/s11274-011-0979-9

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538

  • Cappuccino JG, Sherman N (2013) Biochemical activities of microorganisms. In: Microbiology, A Laboratory Manual. The Benjamin/Cummings Publishing Co., California

  • Chen Y, Chao Y, Li Y et al (2016) Survival strategies of the plant-associated bacterium Enterobacter sp. strain EG16 under cadmium stress. Appl Environ Microbiol 82:1734–1744. https://doi.org/10.1128/AEM.03689-15

    Article  CAS  Google Scholar 

  • Chmielowska-Bąk J, Lefèvre I, Lutts S et al (2014) Effect of cobalt chloride on soybean seedlings subjected to cadmium stress. Acta Soc Bot Pol 83:201–207. https://doi.org/10.5586/asbp.2014.027

    Article  Google Scholar 

  • Chunhabundit R (2016) Cadmium exposure and potential health risk from foods in contaminated area, Thailand. Toxicol Res 32:65–72. https://doi.org/10.5487/TR.2016.32.1.065

    Article  CAS  Google Scholar 

  • Cocozza C, Trupiano D, Lustrato G et al (2015) Challenging synergistic activity of poplar-bacteria association for the Cd phytostabilization. Environ Sci Pollut Res 22:19546–19561. https://doi.org/10.1007/s11356-015-5097-z

    Article  CAS  Google Scholar 

  • Dilworth MJ (1966) Acetylene reduction by nitrogen-fixing preparations from Clostridium pasteurianum. Bichemicaet Biophysicaacta 127:285–294

    CAS  Google Scholar 

  • Dimkpa CO, Svatos A, Dabrowska P et al (2008) Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere 74:19–25

    Article  CAS  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK et al (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Ekmekci Y, Tanyolaç D,  Ayhan B (2009) A crop tolerating oxidative stress induced by excess lead : maize. Acta Physiol Plant 31:319–330. https://doi.org/10.1007/s11738-008-0238-3

  • FAO (2003). Nutritional contribution of rice and impact of biotechnology and biodiversity in rice-consuming countries. Food and Agriculture Organization of the United Nations, Rome Italy .http://www.fao.org/docrep/006/Y4751E/y4751e05.htm

  • Fick GN, Qualset CO (1975) Genetic control of endosperm amylase activity and gibberellic acid Reoponses in standard-height and short-statured wheats. Proc Nat Acad Sci USA 72:892–895

    Article  CAS  Google Scholar 

  • Fiske CH, Subbarow Y (1925) The colorimetric determination of phosphorus. LXVI 2:375–400

    Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases. Plant Physiol 59:309–314

    Article  CAS  Google Scholar 

  • Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7. https://doi.org/10.1016/j.femsle.2005.07.030

    Article  CAS  Google Scholar 

  • Grichko VP, Filby B, Glick BR (2000) Increased ability of transgenic plants expressing the bacterial enzyme ACC deaminase to accumulate Cd Co, Cu, Ni, Pb, and Zn. J Biotechnol 81:45–53

    Article  CAS  Google Scholar 

  • Guo J, Chi J (2014) Effect of Cd-tolerant plant growth-promoting rhizobiumon plant growth and Cd uptake by Lolium multiflorum lam. And Glycine max (L.) merr. in Cd-contaminated soil. Plant Soil 375:205–214. https://doi.org/10.1007/s11104-013-1952-1

    Article  CAS  Google Scholar 

  • Gyaneshwar P, Kumar GN, Parekh LJ et al (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93

    Article  CAS  Google Scholar 

  • Ha J, Gélabert A, Spormann AM et al (2010) Role of extracellular polymericsubstances in metal ion complexation on Shewanellaoneidensis: batch uptakethermodynamic modeling, ATR-FTIR, and EXAFS study. Geochim Cosmochim Acta 74:1–15

    Article  CAS  Google Scholar 

  • Haneef I, Faizan S, Perveen R et al (2014) Impact of bio-fertilizers and different levels of cadmium on the growth, biochemical contents and lipid peroxidation of Plantago ovata Forsk. Saudi J Biol Sci 21:305–310. https://doi.org/10.1016/j.sjbs.2013.12.005

    Article  CAS  Google Scholar 

  • Hayat S, Hayat Q, Alyemeni MN et al (2012) Role of proline under changing environments. Plant Signal Behavior 7:1456–1466. https://doi.org/10.4161/psb.21949

    Article  CAS  Google Scholar 

  • Heath L, Packer L (1968) Photoperoxidation in isolated chloroplasts of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Hseu Z, Chen Z, Tsai C et al (2002) Digestion methods for total heavy metals in sediments and soils. Water Air Soil Pollut 141:189–205

  • Kamran MA, Eqani SAMAS, Bibi S et al (2016) Bioaccumulation of nickel by E. sativa and role of plant growth promoting rhizobacteria (PGPRs) under nickel stress. Ecotoxicol Environ Safety 126:256–263. https://doi.org/10.1016/j.ecoenv.2016.01.002

    Article  CAS  Google Scholar 

  • Kartik VP, Jinal HN, Amaresan N (2016) Characterization of cadmium-resistant bacteria for its potential in promoting plant growth and cadmium accumulation in Sesbania bispinosa root. Int J Phytorem 18:1061–1066. https://doi.org/10.1080/15226514.2016.1183576

    Article  CAS  Google Scholar 

  • Kenney JP (2010) Metal adsorption to bacterial cells and their products. Universityof Notre, Dame

    Google Scholar 

  • Khan AA, Faust MA (1967) Effect of growth retardants on a-amylase production in germinating barley seed. Physiol Plant 20:673–681

    Article  CAS  Google Scholar 

  • Kidrič M, Kos J, Sabotič J (2014) Proteases and their endogenous inhibitors in the plant response to abiotic stress. Botanica Serbica 38:139–158

    Google Scholar 

  • Kumar S, Stecher G, Tamura K (2015) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  Google Scholar 

  • Lorck H, Veterinary R (1948) Production of hydrocyanic acid by bacteria. Physiol Plant 1:1–6

    Article  Google Scholar 

  • Moreira H, Marques APGC, Franco AR et al (2014) Phytomanagement of Cd-contaminated soils using maize (Zea mays L.) assisted by plant growth-promoting rhizobacteria. Env Sci Pollut Res 21:9742–9753. https://doi.org/10.1007/s11356-014-2848-1

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.1002/jobm.201400723

    Article  CAS  Google Scholar 

  • Pandey N, Bhatt R (2016) Role of soil associated Exiguobacterium in reducing arsenic toxicity and promoting plant growth in Vigna radiata. Euro J Soil Biol 75:142–150 https://doi.org/10.1016/j.ejsobi.2016.05.007

    Article  CAS  Google Scholar 

  • Pandey S, Saha P, Barai PK et al (2010) Characterization of a Cd2+-resistant strain of Ochrobactrum sp. isolated from slag disposal site of an iron and steel factory. Curr Microbiol 61:106–111. https://doi.org/10.1007/s00284-010-9583-8

    Article  CAS  Google Scholar 

  • Pandey S, Ghosh PK, Ghosh S et al (2013) Role of heavy metal resistant Ochrobactrum sp. and Bacillus spp. strains in bioremediation of a rice cultivar and their PGPR like activities. J Microbiol 51:11–17. https://doi.org/10.1007/s12275-013-2330-7

    Article  CAS  Google Scholar 

  • Park J, Bolan N, Megharaj M et al (2010) Isolation of phosphate-solubilizing bacteria and characterization of their effects on lead immobilization. Pedologist 53:67–75

    CAS  Google Scholar 

  • Pikovskaya RI (1948) Mobilization of phosphorus in soil connection with the vital activity of some microbial species. Microbiologiya 17:362–370

    CAS  Google Scholar 

  • Pishchik VN, Vorobyev NI, Chernyaeva II et al (2002) Experimental and mathematical simulation of plant growth promoting rhizobacteria and plant interaction under cadmium stress. Plant Soil 243:173–186

    Article  CAS  Google Scholar 

  • Prapagdee B, Khonsue N (2015) Bacterial-assisted cadmium phytoremediation by Ocimum gratissimum L. in polluted agricultural soil: a field trial experiment. Int J Environ Sci Technol 12:3843–3852. https://doi.org/10.1007/s13762-015-0816-z

    Article  CAS  Google Scholar 

  • Pulcrano G, Iula DV, Vollaro A et al (2013) Rapid and reliable MALDI-TOF mass spectrometry identification of Candida non-albicans isolates from bloodstream infections. J Microbiol Methods 94:262–266. https://doi.org/10.1016/j.mimet.2013.07.001

    Article  CAS  Google Scholar 

  • Quartacci MF, Argilla A, Baker AJM et al (2006) Phytoextraction of metals from a multiply contaminated soil by Indian mustard. Chemosphere 63:918–925

    Article  CAS  Google Scholar 

  • Rosa M, Prado C, Podazza G et al (2009) Soluble sugars—metabolism, sensing and abiotic stress a complex network in the life of plants. Plant Signal Behav 4:388–393

    Article  CAS  Google Scholar 

  • Safronova VI, Stepanok VV, Engqvist GL et al (2006) Root-associated bacteria containing 1-aminocyclopropane-1-carboxylate deaminase improve growth and nutrient uptake by pea genotypes cultivated in cadmium supplemented soil. Biol Fert Soil 42:267–272

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) In: molecular cloning a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal CAS assay for the detection and determination of siderophores. Anal Biochem. https://doi.org/10.1016/0003-2697(87)90612-9

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:1–26. https://doi.org/10.1155/2012/217037

    Article  Google Scholar 

  • Shrivastava UP, Kumar A (2013) Characterization and optimization of 1-aminocyclopropane-1-carboxylate deaminase (ACCD) activity in different rhizospheric PGPR along with Microbacterium sp. strain ECI-12A. Int J Appl Sci Biotechnol 1:11–15

    CAS  Google Scholar 

  • Singh RP, Jha PN (2016) The multifarious PGPR Serratia marcescens CDP-13 augments induced systemic resistance and enhanced salinity tolerance of wheat (Triticum aestivum L.) PLoS One (6):11, e0155026. https://doi.org/10.1371/journal.pone.0155026

  • Singh R, Pathak B, Fulekar MH (2015) Characterization of PGP traits by heavy metals tolerant Pseudomonas putida and Bacillus safensis strain isolated from rhizospheric zone of weed (Phyllanthus urinaria) and its efficiency in Cd and Pb removal. Int J Curr Microbiol Appl Sci 4:954–975

    Google Scholar 

  • Snell FD, Snell CT (1971) Colorimetric methods of analysis. Van Nostard Reinford Co., New York

    Google Scholar 

  • Tran TA, Popova LP (2013) Functions and toxicity of cadmium in plants: recent advances and future prospects. Turk J Bot 37:1–13

    CAS  Google Scholar 

  • Wan Y, Luo S, Chen J et al (2012) Effect of endophyte-infection on growth parameters and cd-induced phytotoxicity of Cd-hyperaccumulator Solanum nigrum L. Chemosphere 89:743–750. https://doi.org/10.1016/j.chemosphere.2012.07.005

    Article  CAS  Google Scholar 

  • Yang Y, Zhang F, Li H et al (2009) Accumulation of cadmium in the edible parts of six vegetable species grown in Cd-contaminated soils. J Environ Manage 90:1117–1122. https://doi.org/10.1016/j.jenvman.2008.05.004

    Article  CAS  Google Scholar 

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Acknowledgements

The first author is thankful to the Department of Science and Technology, New Delhi, Government of India, for awarding the DST-INSPIRE fellowship (Reg. No.:IF150197).

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Authors and Affiliations

  1. Microbiology Laboratory, Department of Botany, The University of Burdwan, Burdwan, WB, PIN 713104, India

    Krishnendu Pramanik, Soumik Mitra, Anumita Sarkar, Tithi Soren & Tushar Kanti Maiti

  2. Department of Botany, Government General Degree College, Singur, WB, PIN 712409, India

    Anumita Sarkar

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  1. Krishnendu Pramanik
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  2. Soumik Mitra
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  3. Anumita Sarkar
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Correspondence to Tushar Kanti Maiti.

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Pramanik, K., Mitra, S., Sarkar, A. et al. Characterization of cadmium-resistant Klebsiella pneumoniae MCC 3091 promoted rice seedling growth by alleviating phytotoxicity of cadmium. Environ Sci Pollut Res 24, 24419–24437 (2017). https://doi.org/10.1007/s11356-017-0033-z

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