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Characterization of Rhodotorula mucilaginosa RSRod01 Isolated from Trifolium sp. Root Nodules Growing at a Pb-Zn Mine Site

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Abstract

New advance in plant–microorganism interactions research revealed the ability of plants to affect the composition of root-associated microbial communities, selecting for the microorganisms required for their growth in different ecosystems under stress conditions. Yeasts can play important roles in promoting plant growth; however, little information is available in this regard. In this study, we evaluated the ability of Rhodotorula mucilaginosa RSRod01 strain isolated from the root nodules of Trifolium sp. collected from a Pb-Zn mine soil to promote plant growth in vitro by producing a siderophore and extracellular enzymes, and exhibiting antifungal activity, as well as its tolerance to heavy metals and salinity. The results showed that the isolate possessed important plant growth-promoting (PGP) traits, including the capacity to grow at 4% salt concentration and resistance to high levels of heavy metals. Resistance to heavy metals decreased in the following row: Pb2+ > Cu2+ > Co2+ > Zn2+ = Ni2+ > Cd2+> Cr6+.

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REFERENCES

  1. Aibeche, C., Selami, N., Zitouni-Haouar, F.E., Oeunzar, K., Addou, A., Kaid-Harche, M., and Djabeur, A., Bioremediation potential and lead removal capacity of heavy metal-tolerant yeasts isolated from Dayet Oum Ghellaz Lake water (northwest of Algeria), Int. Microbiol., 2022, vol. 25, pp. 61−73.

    Article  CAS  PubMed  Google Scholar 

  2. Akhtyamova, N. and Sattarova, R.K., Endophytic yeast Rhodotorula rubra strain TG-1: antagonistic protection activities, Biochem. Physiol., 2013, vol. 2, p. 1000104. Ali, S.S. and Vidhale, N.N., Bacterial siderophore and their application: a review, Int. J. Curr. Microbiol. Appl. Sci., 213, vol. 2, pp. 303−312.

  3. Amari, T., Ghnaya, T., and Abdelly, C., Nickel, cadmium and lead phytotoxicity and potential of halophytic plants in heavy metal extraction, South. Afric. J. Bot., 2017, vol. 111, pp. 99−110.

    Article  CAS  Google Scholar 

  4. Ayangbenro, A.S. and Babalola, O.O., A new strategy for heavy metal polluted environments: A review of microbial biosorbents, Int. J. Environ. Res. Public Health, 2017, vol. 14, p. 94.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Baldrian, P., Interactions of heavy metals with white-rot fungi, Enzyme Microb. Technol., 2003, vol. 32, pp. 78−91.

    Article  CAS  Google Scholar 

  6. Bhojiya, A.A. and Joshi, H., Heavy metal tolerance pattern of Pseudomonas putida isolated from heavy metal contaminated soil of Zawar, Udaipur (India), Int. J. Innov. Knowl. Concepts, 2017, vol. 2, pp. 58–64.

    Google Scholar 

  7. Botha, A., The importance and ecology of yeasts in soil, Soil Biol. Biochem., 2011, vol. 43, pp. 1–8.

    Article  CAS  Google Scholar 

  8. Calvente, V., De Orellano, M.E., Sansone, G., Benuzzi, D., and De Tosetti, M.I.S., Effect of nitrogen source and pH on siderophore production by Rhodotorula strains and their application to biocontrol of phytopathogenic moulds, J. Ind. Microbiol. Biotechnol., 2001, vol. 26, pp. 226−229.

    Article  CAS  PubMed  Google Scholar 

  9. Carrim, A.J.I., Barbosa, E.C., and Vieira, J.D.G., Enzymatic activity of endophytic bacterial isolates of Jacaranda decurrens Cham. (Carobinhado-campo), Braz. Arch. Biol. Technol., 2006, vol. 49, pp. 353−359.

    Article  Google Scholar 

  10. Cho, D.H. and Kim, E.Y., Characterization of Pb+ 2 bioadsorption from aqueous solution by Rhodotorula glutinis, Bi-oproc. Biosyst. Eng., 2003, vol. 25, pp. 271−277.

    Article  CAS  Google Scholar 

  11. Del Busso Zampieri, B., Bartelochi Pinto, A., Schultz, L., De Oliveira, M.A., De Oliveira, A.J.F., and Zampieri, B.D.B., Diversity and distribution of heavy metal-resistant bacteria in polluted sediments of the Araça Bay, São Sebastião (SP), and the relationship between heavy metals and organic matter concentrations, Microb. Ecol., 2016, vol. 72, pp. 1−13.

    Google Scholar 

  12. Etesami, H. and Beattie, G.A., Plant-microbe interactions in adaptation of agricultural crops to abiotic stress conditions, in Probiotics and Plant Health, Singapore: Springer, 2017, pp. 163−200.

    Google Scholar 

  13. Fahraeus, G., The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique, J. Gen. Microbiol., 1957, vol. 16, pp. 374−381.

    CAS  PubMed  Google Scholar 

  14. Freimoser, F.M., Rueda-Mejia, M.P., Tilocca, B., and Migheli, Q., Biocontrol yeasts: mechanisms and applications, World J. Microbiol. Biotechnol., 2019, vol. 10, p. 154.

    Article  Google Scholar 

  15. Fu, S.F., Sun, P.F., Lu, H.Y., Wei, J.Y., Xiao, H.S., Fang, W.T., Cheng, B.Y., and Chou, J.Y., Plant growth-promoting traits of yeasts isolated from the phyllosphere and rhizosphere of Drosera spatulata Lab, Fungal. Biol., 2016, vol. 120, pp. 433−448.

    Article  CAS  PubMed  Google Scholar 

  16. Gerhardt, P., Murray, R.G.E., Costilow, R.N., Nester, E.W., Wood, W.A., Krieg, N.R., and Phillips, G.B., Manual of Methods for General Bacteriology, Washington: Amer. Soc. Microbiol., 1981.

    Google Scholar 

  17. Gerlagh, M., Goossen-van de Geijn, H., Fokkema, N., and Vereijken, P., Long term biosanitation by application of Coniothyrium minitans on Sclerotinia sclerotiorum, infected crops, Phytopathology, 1999, vol. 89, pp. 141−147.

    Article  CAS  PubMed  Google Scholar 

  18. Grujić, S., Vasić, S., Čomić, L., Ostojić, A., and Radojević, I., Heavy metal tolerance and removal potential in mixed-species biofilm, Water Sci. Technol., 2017, vol. 76, pp. 806−812.

    Article  PubMed  Google Scholar 

  19. Guo, H., Luo, S., Chen, L., Xiao, X., Xi, Q., Wei, W., Zeng, G., Liu, C., Wan, Y., Chen, J., and He, Y., Bioremediation of heavy metals by growing hyperaccumulator endophytic bacterium Bacillus sp. L14, Bioresour. Technol., 2010, vol. 101, pp. 8599–8605.

    Article  CAS  PubMed  Google Scholar 

  20. Gupta, P., Samant, K., and Sahu, A., Isolation of cellulose-degrading bacteria and determination of their cellulolytic potential. Int. J. Microbiol., 2012, vol. 2012, art. 578925.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Hong, S.G., Lee, K.H., and Bae, K.S., Diversity of yeasts associated with natural environments in Korea, J. Microbiol., 2002, vol. 40, pp. 55−62.

    CAS  Google Scholar 

  22. Hong, S.G., Lee, K.H., and Kwak, J., Diversity of yeasts associated with Panax ginseng, J. Microbiol., 2006, vol. 44, pp. 674−679.

    CAS  PubMed  Google Scholar 

  23. Ilyas, S., Rehman, A., Varela, A.C., and Sheehan, D., Redox proteomics changes in the fungal pathogen Trichosporon asahii on arsenic exposure: identification of protein responses to metal-induced oxidative stress in an environmentally-sampled isolate, PLoS One, 2014, vol. 9, p. 7.

    Article  Google Scholar 

  24. Jiang, B., Wang, Q., Zhao, Y., Li, L., and Hu, X., Biosorption mechanism of Zn2+ and Cd2+ by a Rhodotorula mucilaginosa, J. Pure Appl. Microbiol., 2013, vol. 7, pp. 1963–1969.

    CAS  Google Scholar 

  25. Jin, C.S., Deng, R.J., Ren, B.Z., Hou, B.L., and Hursthouse, A.S., Enhanced biosorption of Sb(III) onto living Rhodotorula mucilaginosa strain DJHN070401: optimization and mechanism, Curr. Microbiol., 2020, vol. 77, pp. 2071–2083.

    Article  CAS  PubMed  Google Scholar 

  26. Joubert, P.M. and Doty, S.L., Endophytes of forest trees, in Endophytic Yeasts: Biology, Ecology and Applications, Berlin, 2018, pp. 3–14.

    Google Scholar 

  27. Kavitha, S., Adish, K.S., Yogalakshmi, K.N., Kaliappan, S., and Banu, J.R., Effect of enzyme secreting bacterial pretreatment on enhancement of aerobic digestion potential of waste activated sludge interceded through EDTA, Bioresor. Technol., 2013, vol. 150, pp. 210–219.

  28. Kuang, J., Hou, Y.P., Wang, J.X., and Zhou, M.G., Sensitivity of Sclerotinia sclerotiorum to fludioxonil: in vitro determination of baseline sensitivity and resistance risk, Crop Protection, 2011, vol. 30, pp. 876−882.

    Article  CAS  Google Scholar 

  29. Li, J., Jiang, Z., Chen, S., Wang, T., Jiang, L., Wang, M., Wang, S., and Li, Z., Biochemical changes of polysaccharides and proteins within EPS under Pb(II) stress in Rhodotorula mucilaginosa, Ecotoxicol. Environ. Saf., 2019, vol. 174, pp. 484–490.

    Article  CAS  PubMed  Google Scholar 

  30. Lopez-Fernandez, M., Moll, H., and Merroun, M.L., Reversible pH dependent curium (III) biosorption by the bentonite yeast isolate Rhodotorula mucilaginosa BII-R8, J. Hazard. Mater., 2019, vol. 370, pp. 156–163.

    Article  CAS  PubMed  Google Scholar 

  31. Luo, C., Liu, C., Wang, Y., Liu, X., Li, F., Zhang, G., and Li, X., Heavy metal contamination in soils and vegetables near an e-waste processing site, south China, J. Hazard. Mater., 2011, vol. 186, pp. 481–490.

    Article  CAS  PubMed  Google Scholar 

  32. Martínez-Rodríguez del, J.C., De la Mora-Amutio, M., Plascencia-Correa, L.A., Audelo-Regalado, E., Guar-dado, F.R., Hernández-Sánchez, E., Peña-Ramírez, Y.J., Escalante, A., Beltrán-García, M.J., and Ogura, T., Cultivable endophytic bacteria from leaf bases of Agave tequilana and their role as plant growth promoters, Braz. J. Microbiol., 2015, vol. 45, pp. 1333–1339.

    Google Scholar 

  33. Merdas, B., Contribution to the geological study of the mineralizations of the Hammam N’bail region (North East Algeria), Dissertation, USTHB, Alger, 2006.

  34. Morath, S.U., Hung, R., and Bennett, J.W., Fungal volatile organic compounds: a review with emphasis on their biotechnological potential, Fungal Biol., 2012, vol. 26, pp. 73–83.

    Article  Google Scholar 

  35. Nimsi, K.A., Manjusha, K., Kathiresan, K., and Arya, H., Plant growth-promoting yeasts (PGPY), the latest entrant for use in sustainable agriculture: a review, J. Appl. Microbiol., 2023, vol. 134, p. lxac088.

    Article  PubMed  Google Scholar 

  36. Petkova, M., Petrova, S., Spasova-Apostolova, V., and Naydenov, M., Tobacco plant growth-promoting and antifungal activities of three endophytic yeast strains, Plants (Basel), 2022, vol. 11, p. 751.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Pikovskaya, R.I., Mobilization of phosphorus in soil in connection with the vital activity of some microbial species, Mikrobiologiya, 1948, vol. 17, pp. 362−370.

    CAS  Google Scholar 

  38. Prista, C., Soeiro, A., Vesely, P., Almagro, A., Ramos, J., and Loureiro-Dias, M.C., Genes from Debaryomyces hansenii increase salt tolerance in Saccharomyces cerevisiae W303, FEMS Yeast Res., 2022, vol. 2, pp. 151−157.

    Google Scholar 

  39. Poorniammal, R. and Prabhu, S., plant growth promoting activity and biocontrol potential of soil yeast, Int. J. Agric. Environ. Biotechnol., 2022, vol. 15, pp. 75−80.

    Google Scholar 

  40. Rajkumar, M., Ae, N., Prasad, M.N., and Freitas, H., Potential of siderophore-producing bacteria for improving heavy metal phytoextraction, Trends. Biotechnol., 2010, vol. 28, pp. 142−149.

    Article  CAS  PubMed  Google Scholar 

  41. Rahal, S. and Chekireb, D., Diversity of rhizobia and non-rhizobia endophytes isolated from root nodules of Trifolium sp. growing in lead and zinc mine site Guelma, Algeria, Arch. Microbiol., 2021, vol. 203, pp. 3839–3849.

    Article  CAS  PubMed  Google Scholar 

  42. Ramos-Garza, J., Bustamante-Brito, R., De Paz, G.A., Medina-Canales, G.M., Vásquez-Murrieta, M.S., Wang, E.T., and Rodríguez-Tovar, A.V., Isolation and characterization of yeasts associated with plants growing in heavy-metal- and arsenic-contaminated soils, Can. J. Microbiol., 2016, vol. 62, pp. 307–319.

    Article  CAS  PubMed  Google Scholar 

  43. Raspor, P., Batic, M., Jamnik, P., Josic, D., Milic, R., Pas, M., Recek, M., Rezic-dereani, V., and Skrt, M., The influence of chromium compounds on yeast physiology, Acta Microbiol. Immunol., 2000, vol. 47, pp. 143−173.

    Article  CAS  Google Scholar 

  44. Rehman, A.U., Nazir, S., Irshad, R., Tahir, K., Ur Rehman, K., Ul Islam, R., and Wahab, Z., Toxicity of heavy metals in plants and animals and their uptake by magnetic iron oxide nanoparticles, J. Mol. Liquids, 2021, vol. 321, p. 114455.

    Article  Google Scholar 

  45. Salgado, A., Oliver, A.L.S., Matia-González, A.M., Sotelo, J., Zarco-Fernández, S., Muñoz-Olivas, R., Cámara, C., and Rodríguez-Gabriel, M.A., Response to arsenate treatment in Schizosaccharomyces pombe and the role of its arsenate reductase activity, PLoS One, 2012, vol. 7, p. e43208.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Schalk, I.J., Hannauer, M., and Braud, A., New roles for bacterial siderophores in metal transport and tolerance, Environ. Microbiol., 2011, vol. 13, pp. 2844–2854.

    Article  CAS  PubMed  Google Scholar 

  47. Schulz, B. and Boyle, C., The endophytic continuum, Mycol. Res., 2005, vol. 109, pp. 661−686.

    Article  PubMed  Google Scholar 

  48. Schwyn, B. and Neilands, J.B., Universal chemical assay for the detection and determination of siderophores, Anal. Biochem., 1987, vol. 160, pp. 47−56.

    Article  CAS  PubMed  Google Scholar 

  49. Sierra, G., A simple method for the detection of lipolytic activity of micro-organisms and some observations on the influence of the contact between cells and fatty substrates, Antonie Van Leeuwenhoek, 1957, vol. 23, pp. 15−22.

    Article  CAS  PubMed  Google Scholar 

  50. Somasegaran, P. and Hoben, H.J., Handbook for Rhizobia, Methods in Legume-Rhizobium Technology, New York, 1994, pp. 240−258.

    Book  Google Scholar 

  51. Sun, P.F., Fang, W.T., Shin, L.Y., Wei, J.Y., Fu, S.F., and Chou, J.Y., Indole-3-acetic acid-producing yeasts in the phyllosphere of the carnivorous plant Drosera indica L., PLoS One, 2014, vol. 9, p. e114196.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Sun, G.L., Reynolds, E.E., and Belcher, A.M., Using yeast to sustainably remediate and extract heavy metals from waste waters, Nat. Sustain., 2020, vol. 3, pp. 303–311.

    Article  Google Scholar 

  53. Vejan, P., Abdullah, R., Khadiran, T., Ismail, S., and Nasrulhaq Boyce, A., Role of plant growth promoting rhizobacteria in agricultural sustainability–a review, Molecules, 2016, vol. 21, p. 573.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Vessey, J.K., Plant growth promoting rhizobacteria as biofertilizers, Plant and Soil, 2003, vol. 255, pp. 571–586.

    Article  CAS  Google Scholar 

  55. Villegas, L.B., Amoroso, M.J., and De Figueroa, L.I.C., Copper tolerant yeasts isolated from polluted area of Argentina, J. Basic Microbiol., 2005, vol. 45, pp. 381–391.

    Article  CAS  PubMed  Google Scholar 

  56. White, T.J., Bruns, T.D., Lee, S.B., and Taylor, J.W., Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, in PCR Protocols: A Guide to Methods and Applications, Innis, M.A., Gelfand, D.H., Sninsky, J.J., and White, T.J., Eds., San Diego: Academic, 1990.

  57. Yurkov, A.M., Yeasts of the soil—obscure but precious, Yeast, 2018, vol. 35, pp. 369−378.

    Article  CAS  PubMed  Google Scholar 

  58. Zhang, D., Spadaro, D., Garibaldi, A., and Gullino, M.L., Selection and evaluation of new antagonists for their efficacy against postharvest brown rot of peaches, Postharvest Biol. Technol., 2010, vol. 55, pp. 174–181.

    Article  CAS  Google Scholar 

  59. Zhang, H., Huang, T., and Chen, S., Ignored sediment fungal populations in water supply reservoirs are revealed by quantitative PCR and 454 pyrosequencing, BMC Microbiol., 2015, vol. 15, p. 44.

    Article  PubMed  PubMed Central  Google Scholar 

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ACKNOWLEDGMENTS

This work was supported by the General Directorate for Scientific Research and Technological development (GDSRTD) (Algeria). We are grateful to Benjamin Gourion for hosting Sarah Rahal in Laboratory Des Interactions plants Micro-organismes (LIPM, Toulouse, France), for the help in the experiments and his extremely useful advice throughout this research. The authors would like to thank also Claire Benezech for her help and advice.

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Rahal, S., Menaa, B. & Chekireb, D. Characterization of Rhodotorula mucilaginosa RSRod01 Isolated from Trifolium sp. Root Nodules Growing at a Pb-Zn Mine Site. Microbiology 92, 860–867 (2023). https://doi.org/10.1134/S0026261723600891

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