Abstract
In this study, chromium (Cr)-tolerant bacteria were test for their efficiency in alleviating Cr stress in Cicer arietinum plants. On the basis of 16S rRNA gene analysis, the isolates were identified belonging to genus Stenotrophomonas maltophilia, Bacillus thuringiensis B. cereus, and B. subtilis. The strains produced a considerable amount of indole-3-acetic acid in a medium supplemented with tryptophan. The strains also showed siderophore production (S2VWR5 and S3VKR17), phosphorus production (S1VKR11, S3VKR2, S3VKR16, and S2VWR5), and potassium solubilization (S3VKR2, S2VWR5, and S3VKR17). Furthermore, the strains were evaluated in pot experiments to assess the growth promotion of C. arietinum in the presence of chromium salts. Bacterization improved higher root and shoot length considerably to 6.25%–60.41% and 11.3%–59.6% over the control. The plants also showed increase in their fresh weight and dry weight in response to inoculation with Cr-tolerant strains. The accumulation of Cr was higher in roots compared to shoots in both control and inoculated plants, indicating phytostabilization of Cr by C. arietinum. However, phytostabilization was found to be improved manifold in inoculated plants. Apart from the plant attributes, the amendment of soil with Cr and Cr-tolerant bacteria significantly increased the content of total chlorophyll and carotenoids, suggesting the inoculant’s role in protecting plants from deleterious effects. This work suggests that the combined activity of Cr-tolerant and plant growth–promoting (PGP) properties of the tested strains could be exploited for bioremediation of Cr and to enhance the C. arietinum cultivation in Cr-contaminated soils.
Similar content being viewed by others
References
Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26:1–20
Aleksandrov VG, Blagodyr RN, Iiiev IP (1967) Liberation of phosphoric acid from apatite by silicate bacteria. Mikrobiol Zh (Kiev) 29:111–114
Altschul SF, Maddan TL, Schaffer AA, Zang J, Zang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programmes. Nucleic Acids Res 25:3389–3402
Andrades-Moreno L, Del Castillo I, Parra R, Doukkali B, Redondo-Gómez S, Pérez-Palacios P, Caviedes MA, Pajuelo E, Rodríguez-Llorente ID (2014) Prospecting metal-resistant plant-growth promoting rhizobacteria for rhizoremediation of metal contaminated estuaries using Spartina densiflora. Environ Sci Pollut Res 21:3713–3721
Arnon DI (1949) Copper enzymes in isolated chloroplast: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15
Azevedo H, Glória Pinto CG, Fernandes J, Loureiro S, Santos C (2005) Cadmium effects on sunflower growth and photosynthesis. J Plant Nutr 28:2211–2220
Bahadur A, Afzal A, Ahmad R, Nasir F, Khan A, Suthar V, Jan G, Batool A, Zia MA (2016) Mahmood-ul-Hassan M (2016) Influence of metal-resistant rhizobacteria on the growth of Helianthus annuus L. in Cr(VI)-contaminated soil. Water Air Soil Pollut 227:467
Brick JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indole acetic acid production by bacteria immobilized on nitrocellulose membrane. Appl Environ Microbiol 57:535–538
Bruno LB, Karthik C, Ma Y, Kadirvelu K, Freitas H, Rajkumar M (2020) Amelioration of chromium and heat stresses in Sorghum bicolor by Cr6+ reducing thermotolerant plant growth promoting bacteria. Chemosphere 244:125521
Chatterjee S, Sau GB, Mukherjee SK (2009) Plant growth promotion by hexavalent chromium reducing bacterial strain, Cellulosimicrobium cellulans KUCr3. World J Microbiol Biotechnol 25:1829–1836
Chung J, Nerenberg R, Rittmann BE (2006) Bio-reduction of soluble chromate using a hydrogen based membrane biofilm reactor. Water Res 40:1634–1642
Das S, Jeana JS, Choua ML, Rathod J, Liua CC (2016) Arsenite-oxidizing bacteria exhibiting plant growth promoting traits isolated from the rhizosphere of Oryza sativa L.: implications for mitigation of arsenic contamination in paddies. J Hazard Mater 302:10–18
Feldman FJ, Purdy WC (1965) The atomic absorption spectroscopy of chromium. Anal Chim Acta 33:273–278
Fitz WJ, Wenzel WW (2002) Arsenic transformations in the soil rhizosphere plant system: fundamentals and potential application to phytoremediation. J Biotechnol 99:259–278
Gil-Cardeza ML, Ferri A, Cornejo P, Gomez E (2014) Distribution of chromium species in a Cr-polluted soil: presence of Cr(III) in glomalin related protein fraction. Sci Total Environ 493:828–833
Gupta P, Kumar V, Usmani Z, Rani R, Chandra A, Gupta VK (2020) Implications of plant growth promoting Klebsiella sp. CPSB4 and Enterobacter sp. CPSB49 in luxuriant growth of tomato plants under chromium stress. Chemosphere 240:124944
Hemambika B, Balasubramanian V, Rajesh Kannan V, Arthur James R (2013) Screening of chromium-resistant bacteria for plant growth-promoting activities. Soil Sediment Contam 22:717–736
Jiang CY, Sheng XF, Qian M, Wang QY (2008) Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal polluted soil. Chemosphere 72:157–164
Jing YX, Yan JL, He HD, Yang DJ, Xiao L, Zhong T, Yuan M, Cai XD, Li SB (2014) Characterization of bacteria in the rhizosphere soils of Polygonum pubescens and their potential in promoting growth and Cd, Pb, Zn uptake by Brassica napus. Int J Phytoremediation 16:321–333
Karthik C, Elangovan N, Kumar TS, Govindharaju S, Barathi S, Oves M, Arulselvi PI (2017) Characterization of multifarious plant growth promoting traits of rhizobacterial strain AR6 under chromium (VI) stress. Microbiol Res 204:65–71
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 Phytoremediation 18:1061–1066
Khan MU, Sessitsch A, Harris M, Fatima K, Imran A, Arslan MG, Shabir G, Khan QM, Afzal M (2015) Cr-resistant rhizo and endophytic bacteria associated with Prosopis juliflora and their potential as phytoremediation enhancing agents in metal-degraded soils. Front Plant Sci 5:755
Ma Y, Rajkumar M, Luo YM, Freitas H (2011) Inoculation of endophytic bacteria on host and non-host plants—effects on plant growth and Ni uptake. J Hazard Mater 196:230–237
Maqbool Z, Asghar HN, Shahzad T, Hussain S, Riaz M, Ali S, Arif MS, Maqsood M (2015) Isolating, screening and applying chromium reducing bacteria to promote growth and yield of okra (Hibiscus esculentus L) in chromium contaminated soils. Ecotoxicol Environ Saf 114:343–349
Mengoni A, Schat H, Vangronsveld J (2010) Plants as extreme environments? Ni-resistant bacteria and Ni-hyperaccumulators of serpentine flora. Plant Soil 331:5–16
Porra R, Thompson W, Kriedemann P (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394
Rajkumar M, Nagendran R, Lee KJ, Lee WH, Kim SZ (2006) Influence of plant growth promoting bacteria and Cr6+ on the growth of Indian mustard. Chemosphere 62:741–748
Rajkumar M, Ae N, Prasad MN, Freitas H (2010) Potential of siderophore producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149
Rajkumar M, Ma Y, Freitas H (2013) Improvement of Ni phytostabilization by inoculation of Ni resistant Bacillus megaterium SR28C. J Environ Manage 128:973–980
Reichman S (2014) Probing the plant growth-promoting and heavy metal tolerance characteristics of Bradyrhizobium japonicum CB1809. Eur J Soil Biol 63:7–13
Romeh AA, Khamis MA, Metwally SM (2016) Potential of Plantago major L for phytoremediation of lead-contaminated soil and water. Water Air Soil Pollut 227:9
Roychowdhury R, Mukherjee P, Roy M (2016) Identification of chromium resistant bacteria from dry fly ash sample of Mejia MTPS thermal power plant, West Bengal, India. Bull Environ Contam Toxicol 96:210–216
Sagar S, Dwivedi A, Yadav S, Tripathi M, Kaistha SD (2012) Hexavalent chromium reduction and plant growth promotion by Staphylococcus arlettae strain Cr11. Chemosphere 86:47–852
Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56
Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phyto extraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194
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 21:9356–9365
Subrahmanyam G, Sharma RK, Naresh Kumar G, Archana G (2018) Vigna radiata GM4 plant growth enhancement and root colonization by a multi-metal resistant plant growth promoting bacterium in Cr (VI) amended soils. Pedosphere 28:144–156
Tariq SR, Shah MH, Shaheen N, Jaffar M, Khalique A (2008) Statistical source identification of metals in ground water exposed to industrial contamination. Environ Monit Assess 138:159–165
Thacker U, Parikh R, Shouche Y, Madamwar D (2006) Hexavalent chromium reduction by Providencia sp. Process Biochem 41:1332–1337
Turgay OC, Görmez A, Bilen S (2012) Isolation and characterization of metal resistant-tolerant rhizosphere bacteria from the serpentine soils in Turkey. Environ Monit Assess 184:515–526
Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S (2009) Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot 60:2677–2688
Verma SC, Ladha JK, Tripathi AK (2001) Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J Biotechnol 91:127–141
Wani PA, Khan MS, Zaidi A (2008) Chromium-reducing and plant growth promoting Mesorhizobium improves chickpea growth in chromium-amended soil. Biotechnol Lett 30:159–163
Weyens N, Lelie DVD, Taghavi S, Vangronsveld J (2009) Phytoremediation: plant-endophyte partnerships take the challenge. Curr Opin Biotechnol 20:248–254
Xia S, Song Z, Jeyakumar P, Shaheen SM, Rinklebe J, Ok YS, Bolan N, Wang H (2019) A critical review on bioremediation technologies for Cr(VI)-contaminated soils and wastewater. Crit Rev Env Sci Tec 49:1027–1078
Zahoor M, Irshad M, Rahman H, Qasim M, Afridi SG, Qadir M, Hussain A (2017) Alleviation of heavy metal toxicity and phytostimulation of Brassica campestris L. by endophytic Mucor sp. MHR-7. Ecotoxicol Environ Saf 142:139–149
Zhang YF, He LY, Chen ZJ, Wang QY (2011) Characterization of ACC deaminase producing endophytic bacteria isolated from copper-tolerant plants and their potential in promoting the growth and copper accumulation of Brassica napus. Chemosphere 83:57–62
Zhu LJ, Guan DX, Luo J, Rathinasabapathi B, Ma LQ (2014) Characterization of arsenic-resistant endophytic bacteria from hyperaccumulators Pteris vittata and Pteris multifida. Chemosphere 113:9–16
Acknowledgments
The authors thank the management of the Uka Tarsadia University for providing research promotion scheme fund to carry out the work. They also thank GSBTM for 16S rRNA gene sequencing; Mahuva Sugar Factory, Mahuva, for physicochemical studies; and Dr. N. B. Patel, Head of the Sophisticated Scientific Instrumentation Center (SSIC), VNSGU, Surat, for providing access to AAS facilities.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
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
Shreya, D., Jinal, H.N., Kartik, V.P. et al. Amelioration effect of chromium-tolerant bacteria on growth, physiological properties and chromium mobilization in chickpea (Cicer arietinum) under chromium stress. Arch Microbiol 202, 887–894 (2020). https://doi.org/10.1007/s00203-019-01801-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-019-01801-1