Alleviation of Cadmium Stress in Rice Seedlings Inoculated with Enterobacter tabaci 4M9 (CCB-MBL 5004)

Main Article Content

Saidu Abdullahi
Hazzeman Haris
Kamarul Zaman Zarkasi
Amir Hamzah Ghazali

Abstract

The growth of crop plants is greatly affected by the increased toxicity of metals. Luckily, certain beneficial bacteria can potentially reduce the effects of metal stress and promote the growth of the host plants. Many species of bacteria were reported as heavy metal tolerant and plant growth promoting, with very little or no report available concerning Enterobacter tabaci as heavy metal tolerant plant growth promoting. The present study aimed to evaluate the potential of Cadmium (Cd) tolerant Enterobacter tabaci 4M9 (CCB-MBL 5004) to alleviate heavy metals stress and enhance the growth of rice seedlings grown under Cd stress conditions. Rice seedlings were grown in Yoshida medium supplemented with different concentrations of Cd and inoculated with 4M9. The results showed that the inoculum tested successfully reduced oxidative stress in the seedlings by reducing the electrolyte leakage (EL) and increasing catalase (CAT) and superoxide dismutase (SOD) activities in the inoculated seedlings compared to the control counterparts. The results also revealed a significant increase in plant growth, biomass, and chlorophyll content of inoculated rice seedlings compared to the control. In general, the Cd tolerant E. tabaci 4M9 confers heavy metal alleviation and thereby improves the growth and survival of rice seedlings under Cd stress conditions. Therefore, the findings stated the potential of 4M9 for alleviating heavy metal stress and promoting the development of inoculated rice seedlings if accidentally grown under Cd-contaminated conditions.

Article Details

How to Cite
Alleviation of Cadmium Stress in Rice Seedlings Inoculated with Enterobacter tabaci 4M9 (CCB-MBL 5004). (2024). Tropical Life Sciences Research, 35(1), 107–121. https://doi.org/10.21315/tlsr2024.35.1.6
Section
Original Article

References

Abdullahi S, Haris H, Zarkasi K Z and Amir H G. (2021). Beneficial bacteria associated with Mimosa pudica and potential to sustain plant growth-promoting traits under heavy metals stress. Bioremediation Journal 25(1): 1–21. https://doi.org/10.1080/10889 868.2020.1837724

Ahmad I, Akhtar M J, Zahir Z A, Naveed M, Mitter B and Sessitsch A. (2014). Cadmium-tolerant bacteria induce metal stress tolerance in cereals. Environmental Science and Pollution Research 21: 11054–11065. https://doi.org/10.1007/s11356-014-3010-9

Ajmal A W, Saroosh S, Mulk S, Hassan M N, Yasmin H, Jabeen Z, Nosheen A, Shah S M U, Naz R and Hasnain Z. (2021). Bacteria isolated from wastewater irrigated agricultural soils adapt to heavy metal toxicity while maintaining their plant growth promoting traits. Sustainability 13(14): 7792. https://doi.org/10.3390/su13147792

Azeem M A, Shah F H, Ullah A, Ali K, Jones D A, Khan M E H and Ashraf A. (2022). Biochemical characterization of halotolerant Bacillus safensis PM22 and its potential to enhance growth of maize under salinity stress. Plants 11(13): 1721. https://doi.org/10.3390/plants11131721

Caverzan A, Casassola A and Brammer S P. (2016). Reactive oxygen species and antioxidant enzymes involved in plant tolerance to stress. In A K Shanker and C Shanker (eds.). Abiotic and biotic stress in plants: Recent advances and future perspectives. London: IntechOpen. https://doi.org/10.5772/61368 (accessed on 11 November 2022).

Das J and Sarkar P. (2018). Remediation of arsenic in mung bean (Vigna radiata) with growth enhancement by unique arsenic-resistant bacterium Acinetobacter iwoffii. Science of the Total Environment 624: 1106–1118. https://doi.org/10.1016/j. scitotenv.2017.12.157

Dharni S, Srivastava A K, Samad A and Patra D D. (2014). Impact of plant growth-promoting Pseudomonas monteilii PsF84 and Pseudomonas plecoglossicida PsF610 on metal uptake and production of secondary metabolite (monoterpenes) by rose-scented geranium (Pelargonium graveolens cv. bourbon) grown on tannery sludge. Chemosphere 117: 433–439. https://doi.org/10.1016/j.chemosphere.2014.08.001

Etesami H. (2018). Bacterial mediated alleviation of heavy metal stress and decreased accumulation of metals in plant tissues: Mechanisms and future prospects. Ecotoxicology and Environment Safety 147: 175–191. https://doi.org/10.1016/j.ecoenv.2017.08.032

Farh M E A, Kim Y J, Sukweenadhi J, Singh P and Yang D C. (2017). Aluminum-resistant, plant growth-promoting bacteria induce overexpression of aluminum stress-related genes in Arabidopsis thaliana and increase the ginseng tolerance against aluminum stress. Microbiological Research 200: 45–52. https://doi.org/10.1016/j. micres.2017.04.004

Gontia-mishra I, Sapre S, Sharma A and Tiwari S. (2016). Alleviation of mercury toxicity in wheat by the interaction of mercury-tolerant plant growth-promoting rhizobacteria. Journal of Plant Growth Regulation 35: 1000–1012. https://doi.org/10.1007/s00344-016-9598-x

Hassan M J, Raza M A, Rehman S U, Ansar M, Gitari H, Khan I, Wajid M, Ahmed M, Shah G A, Peng Y and Li Z. (2020). Effect of cadmium toxicity on growth, oxidative damage, antioxidant defense system and cadmium accumulation in two sorghum cultivars. Plants 9(11): 1575. https://doi.org/10.3390/plants9111575

Hiscox J D and Israelstam G F. (1978). A method for the extraction of chlorophyll from leaf tissue without maceration. Canadian Journal of Botany 57(12): 1332–1334. https://doi.org/10.1139/b79-163

Islam F, Yasmeen T, Ali Q, Mubin M, Ali S, Arif M S, Hussain S, Riaz M and Abbas F. (2016). Copper-resistant bacteria reduces oxidative stress and uptake of copper in lentil plants: potential for bacterial bioremediation. Environmental Science and Pollution Research 23: 220–233. https://doi.org/10.1007/s11356-015-5354-1

Ismael M A, Elyamine A M, Moussa M G, Cai M, Zhao X and Hu C. (2019). Cadmium in plants: Uptake, toxicity, and its interactions with selenium fertilizers. Metallomics 11(2): 255–277. https://doi.org/10.1039/c8mt00247a

Jabeen Z, Irshad F, Habib A, Hussain N, Sajjad M, Mumtaz S, Rehman S, Haider W and Hassan M N. (2022). Alleviation of cadmium stress in rice by inoculation of Bacillus cereus. Peer J 10: e13131. https://doi.org/10.7717/peerj.13131

Khalid S, Shahid M, Niazi N K, Murtaza B, Bibi I and Dumat C. (2017). A comparison of technologies for remediation of heavy metal contaminated soils. Journal of Geochemical Exploration 182(Part B): 247–268. https://doi.org/10.1016/j.gexplo.2016.11.021

Khan A R, Ullah I, Khan A L, Park G S, Waqas M, Hong S J, Jung B K, Kwak Y, Lee I J and Shin J H. (2015a). Improvement in phytoremediation potential of Solanum nigrum under cadmium contamination through endophytic-assisted Serratia sp. RSC-14 inoculation. Environmental Science and Pollution Research 22: 14032–14042. https://doi.org/10.1007/s11356-015-4647-8

Khan M U, Sessitsch A, Harris M, Fatima K, Imran A, Arslan M, Shabir G, Khan Q M and Afzal M. (2015b). Cr-resistant rhizo- and endophytic bacteria associated with Prosopis juliflora and their potential as phytoremediation enhancing agents in metal-degraded soils. Frontiers in plant Science 5: 1–10. https://doi.org/10.3389/fpls.2014.00755

Kim Y H, Khan A L, Waqas M and Lee I J. (2017). Silicon regulates antioxidant activities of crop plants under abiotic-induced oxidative stress: A review. Frontiers in Plant Science 8: 1–7. https://doi.org/10.3389/fpls.2017.00510

Kour D, Kaur T, Devi R, Yadav A, Singh M, Joshi D, Singh J, Suyal D C, Kumar A, Rajput V D, et al. (2021). Beneficial microbiomes for bioremediation of diverse contaminated environments for environmental sustainability: Present status and future challenges. Environmental Science and Pollution Research 28: 24917– 24939. https://doi.org/10.1007/s11356-021-13252-7

Ma Y, Rajkumar M, Zhang C and Freitas H. (2016). Beneficial role of bacterial endophytes in heavy metal phytoremediation. Journal of Environmental Management 174: 14–25. https://doi.org/10.1016/j.jenvman.2016.02.047

Mallick I, Bhattacharyya C, Mukherji S, Dey D, Sarkar S C, Mukhopadhyay U K and Ghosh A. (2018). Effective rhizoinoculation and biofilm formation by arsenic immobilizing halophilic plant growth-promoting bacteria (PGPB) isolated from mangrove rhizosphere: A step towards arsenic rhizoremediation. Science of the Total Environment 610–611: 1239–1250. https://doi.org/10.1016/j.scitotenv.2017.07.234

Marquez J E, Pourret O, Faucon M P, Weber S, Hoàng T B H and Martinez R E. (2018). Effect of cadmium, copper, and lead on the growth of rice in the coal mining region of Quang Ninh, Cam-Pha (Vietnam). Sustainability 10(6): 1758. https://doi.org/10.3390/su10061758

Mosa K A, Ismail A and Helmy M. (2017). Introduction to plant stresses. In: Plant stress tolerance. SpringerBriefs in Systems Biology. Cham: Springer, 1–19. https://doi.org/10.1007/978-3-319-59379-1_1

Ndeddy Aka R J and Babalola O O. (2016). Effect of bacterial inoculation of strains of Pseudomonas aeruginosa, Alcaligenes feacalis and Bacillus subtilis on germination, growth, and heavy metal (Cd, Cr, and Ni) uptake of Brassica juncea. International Journal of Phytoremediation 18(2): 200–209. https://doi.org/10.1080/15226514.2015.1073671

Ojuederie O B and Babalola O O. (2017). Microbial and plant-assisted bioremediation of heavy metal polluted environments: A review. International Journal of Environmental Research and Public Health 14(12): 1504. https://doi.org/10.3390/ijerph14121504

Rizvi A and Khan M S. (2017). Biotoxic impact of heavy metals on growth, oxidative stress and morphological changes in root structure of wheat (Triticum aestivum L.) and stress alleviation by Pseudomonas aeruginosa strain CPSB1. Chemosphere 185: 942–952. https://doi.org/10.1016/j.chemosphere.2017.07.088

Rossatto T, do Amaral M N, Benitez L C, Vighi I L, Braga E J B, de Magalhães Júnior A M, Maia M A C and da Silva Pinto L. (2017). Gene expression and activity of antioxidant enzymes in rice plants, cv. BRS AG, under saline stress. Physiology and Molecular Biology of Plants 23(4): 865–875. https://doi.org/10.1007/s12298-017-0467-2

Singh R P, Pandey D M, Jha P N, Ma Y. (2022). ACC deaminase producing rhizobacterium Enterobacter cloacae ZNP-4 enhance abiotic stress tolerance in wheat plant. PLoS ONE 17(5): e0267127. https://doi.org/10.1371/journal.pone.0267127

Swapnil I G, Anubha S and Sharad S. (2016). Alleviation of mercury toxicity in wheat by the interaction of mercury-tolerant plant growth promoting rhizobacteria. Journal of Plant Growth Regulation 35: 1000–1012. https://doi.org/10.1007/s00344-016-9598-x

Tchounwou P B, Yedjou C G, Patlolla A K and Sutton D J. (2012). Heavy metal toxicity and the environment. In: A Luch (eds). Molecular, clinical and environmental toxicology. Experientia Supplementum: 101. Springer, Basel. https://doi.org/10.1007/978-3-7643-8340-4_6

Thomas J and Archana G (2023). Differential influence of heavy metals on plant growth promoting attributes of beneficial microbes and their ability to promote growth of Vigna radiata (mung bean). Biocatalysis and Agricultural Biotechnology 47(2023): 102592. https://doi.org/10.1016/j.bcab.2022.102592

Tiwari S and Lata C (2018). Heavy metal stress, signaling, and tolerance due to plant-associated microbes: An overview. Frontiers in Plant Science 9: 1–12. https://doi.org/10.3389/fpls.2018.00452

Xie X, He Z, Chen N, Tang Z, Wang Q and Cai Y. (2019). The roles of environmental factors in regulation of oxidative stress in plant. BioMed Research International 2019: 21–27. https://doi.org/10.1155/2019/9732325

Yin K, Wang Q, Lv M and Chen L. (2019). Microorganism remediation strategies towards heavy metals. Chemical Engineering Journal 360: 1553–1563. https://doi.org/10.1016/j.cej.2018.10.226

Yoshida S, Forno D A, Cock J H and Gomez K A. (1976). Laboratory manual for physiological studies of rice. https://pdf.usaid.gov/pdf_docs/PNAAE519.pdf (accessed on 24 March 2022).

Zafar-ul-Hye M, Naeem M, Danish S, Khan M J, Fahad S, Datta R, Brtnicky M, Kintl A, Hussain G S and El-Esawi M A. (2020). Effect of cadmium-tolerant rhizobacteria on growth attributes and chlorophyll contents of bitter gourd under cadmium toxicity. Plants 9(10): 1386. https://doi.org/10.3390/plants9101386

Zhao H, Guan J, Liang Q, Zhang X, Hu H and Zhang J. (2021). Effects of cadmium stress on growth and physiological characteristics of Sassafras seedlings. Scientific Reports 11(1): 9913. https://doi.org/10.1038/s41598-021-89322-0