, Volume 74, Issue 12, pp 1711–1720 | Cite as

Oxidative and antioxidative responses to antimony stress by endophytic fungus Aspergillus tubingensis isolated from antimony accumulator Hedysarum pallidum Desf.

  • Ouissem Meghnous
  • Laid Dehimat
  • Patrick Doumas
  • Mounia Kassa-Laouar
  • Fawzia Mosbah
  • Oualida RachedEmail author
Original Article


Antimony (Sb) is a toxic metalloid whose pollution has become a serious problem. However, studies on fungal endophytes resistant to antimony are virtually nonexistent. An endophytic fungal strain was isolated for the first time from the roots of Hedysarum pallidum Desf. which is a Sb accumulator Fabacea growing on mine cuttings. Experiments with high Sb increased concentrations (0, 5, 10, 20 and 30 mM Sb) were performed in order to assess the strain potential in contaminated environments bioremediation and to understand its Sb tolerance strategy. The isolated strain was identified as Aspergillus tubingensis MH189391 by morphological characteristics and phylogenetic analysis. It exhibited a minimum inhibitory concentration (MIC) of 500 mM Sb, i.e. 60,880 mg L−1, and maintained high amounts of biomass up to 30 mM Sb, i.e. 3652.8 mg L−1 of Sb. A stimulation of A. tubingensis growth and its antioxidant responses was observed at the level of 5 mM Sb, i.e. 609 mg L−1. Hydrogen peroxide (H2O2) and malondialdehyde (MDA) contents increased significantly (p < 0.05) with Sb treatments. Oxidative stress induced significant increases (p < 0.05) in antioxidant biomarkers such as proline, catalase (CAT), and superoxide dismutase (SOD), but it resulted in a significant decrease of peroxidase (POD) and ascorbate peroxidase (APX) activities. Proline, CAT, SOD, H2O2 and MDA were significantly (p < 0.05) and positively correlated, which highlights their coactions in oxidative stress fighting. Results indicate that Aspergillus tubingensis has developed an important adaptation to excessive Sb concentrations and that it could be used in antimony-contaminated environments bioremediation.


Metalloid Antioxidants Endophyte Fungus Mine cuttings 



Ascorbate peroxidase






Minimum inhibitory concentration


Probability value


Polymerase chain reaction




Correlation coefficient


Reactive oxygen species


Standard error of the mean




Superoxide dismutase



We would like to thank the Ministry of Higher Education and Scientific Research of Algeria for the financial support and the head of INRA Montpellier (France) for allowing us to achieve some of this work within its premises.

Compliance with ethical standards

Conflict of interest

No potential conflict of interest or financial disclosure for all authors. All persons gave their informed consent prior to their inclusion in the study.


  1. Bacal CJO, Yu ET (2017) Cellulolytic activities of a novel Fomitopsis sp. and Aspergillus tubingensis isolated from Philippine mangroves. Philipp J Sci 146:403–410Google Scholar
  2. Benhamdi A, Bentellis A, Rached O, Du Laing G, Mechakra A (2014) Effects of antimony and arsenic on antioxidant enzyme activities of two Steppic plant species in an old antimony mining area. Biol Trace Elem Res 158:96–104. CrossRefPubMedGoogle Scholar
  3. Bentellis A, Azzoug R, El Hadef El Okki M, Rached O (2014) Trace elements pollution from an abandoned mine and factors affecting Antimony concentrations in the Dahimine Wadi Bank soils (Northeast Algeria). Carpath J Earth Env 9:95–106Google Scholar
  4. Chakraborty S, Mukherjee A, Das TK (2012) Biochemical characterization of a lead-tolerant strain of Aspergillus foetidus: an implication of bioremediation of lead from liquid media. Int Biodeterior Biodegradation 84:134–142. CrossRefGoogle Scholar
  5. Chakraborty S, Mukherjee A, Khuda-Bukhsh AR, Das TK (2014) Cadmium-induced oxidative stress tolerance in cadmium resistant Aspergillus foetidus: its possible role in cadmium bioremediation. Ecotox Environ Safe 106:46–53. CrossRefGoogle Scholar
  6. Chance B, Maehly AC (1955) Assay of catalases and peroxidases. Methods Enzymol 2:764–775. CrossRefGoogle Scholar
  7. Choi J, Détry N, Kim KT, Asiegbu FO, Valkonen JPT, Lee YH (2014) fPoxDB: fungal peroxidase database for comparative genomics. BMC Microbiol 14:117. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Clemente R (2013) Antimony. In: Alloway BJ (ed) Heavy metals in soils: trace metals and metalloids in soils and their bioavailability, 3rd edn. Springer, Dordrecht, pp 497–506CrossRefGoogle Scholar
  9. Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environ Exp Bot 109:212–228. CrossRefGoogle Scholar
  10. Deng Z, Cao L, Huang H, Jiang X, Wang W, Shi Y, Zhang R (2011) Characterization of Cd and Pb-resistant fungal endophyte Mucor sp. CBRF59 isolated from rapes (Brassica chinensis) in metal contaminated soils. J Hazard Mater 185:717–724. CrossRefPubMedGoogle Scholar
  11. Devi KA, Pandey G, Rawat AKS, Sharma GD, Pandey P (2017) The endophytic symbiont—Pseudomonas aeruginosa stimulates the antioxidant activity and growth of Achyranthes aspera L. Front Microbiol 8:1–14. CrossRefGoogle Scholar
  12. Feng R, Liao G, Guo J, Wang R, Xu Y, Ding Y, Mo L, Fan Z, Li N (2016) Responses of root growth and antioxidative systems of paddy rice exposed to antimony and selenium. Environ Exp Bot 122:29–38. CrossRefGoogle Scholar
  13. Huang HB, Feng XJ, Liu L, Chen Bin LYJ, Ma L, She Z-G, Lin YC (2010) Three dimeric Naphtho-γ-Pyrones from the mangrove endophytic fungus Aspergillus tubingensis isolated from Pongamia pinnata. Planta Med 76:1888–1891CrossRefGoogle Scholar
  14. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  15. Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Beneficial role of bacterial endophytes in heavy metal phytoremediation. J Environ Manag 174:14–25. CrossRefGoogle Scholar
  16. Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474. CrossRefGoogle Scholar
  17. Mubarak H, Chai LY, Mirza N, Yang ZH, Pervez A, Tariq M, Shaheen S, Mahmood Q (2015) Antimony (Sb) - pollution and removal techniques –critical assessment of technologies. Toxicol Environ Chem 97:1–22. CrossRefGoogle Scholar
  18. Mukherjee A, Das D, Mondal SK, Biswas R, Das TK, Boujedaini N, Khuda-Bukhsh AR (2010) Tolerance of arsenate-induced stress in Aspergillus niger, a possible candidate for bioremediation. Ecotox Environ Safe 73:172–182. CrossRefGoogle Scholar
  19. Nakano Y, Asada K (1980) Spinach chloroplasts scavenge hydrogen peroxide on illumination. Plant Cell Physiol 21:1295–1307. CrossRefGoogle Scholar
  20. Pierart A, Shahid M, Séjalon-Delmas N, Dumat C (2015) Antimony bioavailability: knowledge and research perspectives for sustainable agricultures. J Hazard Mater 289:219–234. CrossRefPubMedGoogle Scholar
  21. Qayyum S, Khan I, Maqbool F, Zhao Y, Gu Q, Peng C (2016) Isolation and characterization of heavy metal resistant fungal isolates from industrial soil in China. Pak J Zool 48:1241–1247Google Scholar
  22. Raj S, Mohan S (2016) Impact on proline content of Jatropha curcas in fly ash amended soil with respect to heavy metals. J Pharm Pharm 8:244–247Google Scholar
  23. Teng Y, Du X, Wang T, Mi C, Yu H, Zou L (2018) Isolation of a fungus Pencicillium sp. with zinc tolerance and its mechanism of resistance. Arch Microbiol 200:159–169. CrossRefPubMedGoogle Scholar
  24. Tsikas D (2017) Assessment of lipid peroxidation by measuring malondialdehyde (MDA) and relatives in biological samples: analytical and biological challenges. Anal Biochem 524:13–30. CrossRefPubMedGoogle Scholar
  25. Zhang L, Xiao S, Li W, Feng W, Li J, Wu Z, Gao X, Liu F, Shao M (2011) Overexpression of a Harpin-encoding gene hrf1 in rice enhances drought tolerance. J Exp Bot 62:4229–4238. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Zhou X, Sun C, Zhu P, Liu F (2018) Effects of antimony stress on photosynthesis and growth of Acorus calamus. Front Plant Sci 9:1–9. CrossRefGoogle Scholar
  27. Zouari M, Ben Ahmed C, Zorrig W, Elloumi N, Rabhi M, Delmail D, Ben Rouina B, Labrousse P, Ben Abdallah F (2016) Exogenous proline mediates alleviation of cadmium stress by promoting photosynthetic activity, water status and antioxidative enzymes activities of young date palm (Phoenix dactylifera L.). Ecotox Environ Safe 128:100–108. CrossRefGoogle Scholar

Copyright information

© Institute of Molecular Biology, Slovak Academy of Sciences 2019

Authors and Affiliations

  1. 1.Biology and Environment Laboratory, Faculty of Nature and Life SciencesMentouri UniversityConstantineAlgeria
  2. 2.Mycology, Biotechnology and Microbial Activity LaboratoryMentouri UniversityConstantineAlgeria
  3. 3.BPMP, CNRS, INRA, Montpellier SupAgroUniversity of MontpellierMontpellierFrance
  4. 4.Biotechnology High National School Taoufik KhaznadarAli Mendjeli University CityConstantineAlgeria

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