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Removal of Phenanthrene by some microalga species and study of antioxidative compounds in Nostoc calcicola ISC 89

  • Soils, Sec 3 • Remediation and Management of Contaminated or Degraded Lands • Research Article
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Abstract

Purpose

The accumulation of polycyclic aromatic hydrocarbons (PAHs) can cause adverse effects on the environment and human health. Microalgae species have the ability to remove and degrade PAHs. The present research provides novel insights to discover microalgae responses against phenanthrene (as a PAH) through an antioxidant defense response underlying reactive oxygen species detoxification and scavenging.

Materials and methods

This research was carried out to investigate the phenanthrene (PHE) removal by five microalgal species, namely, Scenedesmus sp. ISC 94, Chlorella sp. ISC 23, Nostoc calcicola ISC 89, Anabaena sp. ISC 88, and Leptolyngbya fragilis ISC 108. Screening of microalgal species for the PHE removal was done based on GC analysis and growth parameters under control conditions (without PHE) and at 0.1% PHE.

Results and discussion

The results showed that the tolerance of N. calcicola ISC 89 to PHE was more significant than other species under the studied condition. Antioxidant enzyme activity, total lipid, proline, and phenolic acid content increased significantly in PHE-treated N. calcicola ISC 89. It was also observed that there was a decrease in malondialdehyde (MDA) and H2O2 contents with an increase of specific growth rate and dry weight in the tolerant species.

Conclusions

This research can provide new insights into the mechanism of N. calcicola ISC 89 tolerance against PHE-induced oxidative damage. Overall, this study suggests that N. calcicola ISC 89 can be used to remediate PAH-contaminated regions.

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Abbreviations

PAHs:

Polycyclic aromatic hydrocarbons

PHE:

Phenanthrene

BBM:

Bold’s basal medium

FW:

Fresh weight

DW:

Dry weight

OD:

Optical density

SGR:

Specific growth rate

ACECR:

Academic Center of Education Culture and Research

MDA:

Malondialdehyde

PBP:

Phycobiliprotein

APC:

Allophycocyanin

PE:

Phycoerythrin

PC:

Phycocyanin

TCA:

Trichloroacetic acid

TBA:

Thiobarbituric acid

NBT:

Nitrobluetetrazolium

ROS:

Reactive oxygen species

CarCarotenoid:

ChlChlorophyll

SOD:

Superoxide dismutase

CAT:

Catalase

APX:

Ascorbate peroxidase

PPO:

Polyphenol oxidase

POX:

Peroxidase

TAL:

Tyrosine ammonia-lyase

PAL:

Phenylalanine ammonia-lyase

H2O2 :

Hydrogen peroxide

TP:

Total phenolic

TPA:

Total phenolic acid

TF:

Total flavonoid

References

  • Abbas SH, Ismail IM, Mostafa TM, Sulaymon AH (2014) Biosorption of heavy metals: a review. J Chem Sci Technol 3:74–102

    Google Scholar 

  • Abeles FB, Biles CL (1991) Characterization of peroxidases in lignifying peach fruit endocarp. Plant Physiol 95:269–273

    Article  CAS  Google Scholar 

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Al-Hawas G, Shukry W, Azzoz M, Al-Moaik R (2012) The effect of sublethal concentrations of crude oil on the metabolism of Jojoba (Simmodsia chinensis) seedlings. Int Res J Plant Sci 3:54–62

    Google Scholar 

  • Amirlatifi F, Soltani N, Saadatmand S, Shokravi S, Dezfulian M (2013) Crude oil-induced morphological and physiological responses in cyanobacterium Microchaete tenera ISC13. Int J Environ Res 7:1007–1014

    CAS  Google Scholar 

  • Anyanwu IN, Semple KT (2015) Biodegradation of phenanthrene-nitrogen-containing analogues in soil. Water Air Soil Pollut 28:1

    Google Scholar 

  • Aydaş SB, Ozturk S, Aslım B (2013) Phenylalanine ammonia lyase (PAL) enzyme activity and antioxidant properties of some cyanobacteria isolates. Food Chem 136:164–169

    Article  Google Scholar 

  • Baoune H, Aparicio JD, Pucci G, El Hadj-Khelil AO, Polti MA (2019) Bioremediation of petroleum-contaminated soils using Streptomyces sp. Hlh1. J Soil Sediment 19:2222–2230

    Article  CAS  Google Scholar 

  • Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bi YF, Miao SS, Lu YC, Qiu CB, Zhou Y, Yang H (2012) Phytotoxicity, bioaccumulation and degradation of isoproturon in green algae. J Hazard Mater 243:242–249

    Article  CAS  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Brányiková I, Maršálková B, Doucha J, Brányik T, Bišová K, Zachleder V, Vítová M (2011) Microalgae-novel highly efficient starch producers. Biotechnol Bioeng 108:766–776

    Article  Google Scholar 

  • Carrieri D, Momot D, Brasg IA, Ananyev G, Lenz O, Bryant DA, Dismukes GC (2010) Boosting autofermentation rates and product yields with sodium stress cycling: application to production of renewable fuels by cyanobacteria. Appl Environ Microbiol 76:6455–6462

    Article  CAS  Google Scholar 

  • Chamovitz D, Sandmann G, Hirschberg J (1993) Molecular and biochemical characterization of herbicide-resistant mutants of cyanobacteria reveals that phytoene desaturation is a rate-limiting step in carotenoid biosynthesis. J Biol Chem 268:17348–17353

    Article  CAS  Google Scholar 

  • Chan SMN, Luan T, Wong MH, Tam NFY (2006) Removal and biodegradation of polycyclic aromatic hydrocarbons by Selenastrum capricornutum. Environ Toxicol Chem 25:1772–1779

    Article  CAS  Google Scholar 

  • Chang CC, Yang MH, Wen HM, Chern JC (2002) Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J Food Drug Anal 10:178–182

    CAS  Google Scholar 

  • Debelius B, Forja J, Del Valls A, Lubián L (2008) Effect of linear alkylbenzene sulfonate (LAS) and atrazine on marine microalgae. Mar Poll Bull 57:559–568

    Article  CAS  Google Scholar 

  • Del Vento S, Dachs J (2002) Prediction of uptake dynamics of persistent organic pollutants by bacteria and phytoplankton. Environ Toxicol Chem 21:2099–2107

    Article  Google Scholar 

  • Demeter MA, Lemire JA, Mercer SM, Turner RJ (2017) Screening selectively harnessed environmental microbial communities for biodegradation of polycyclic aromatic hydrocarbons in moving bed biofilm reactors. Bioresour Technol 228:116–124

    Article  CAS  Google Scholar 

  • Dogbo D, Gogbeu S, N’zue B, Ya K, Zohouri G, Mamyrbekova-Bekro J, Bekro YA (2012) Comparative activities of phenylalanine ammonia-lyase and tyrosine ammonia-lyase and phenolic compounds accumulated in cassava elicited cell. Afr Crop Sci J 20:85–94

    Google Scholar 

  • Dubois M, Gilles K, Hamilton J, Rebers P, Smith F (1951) A colorimetric method for the determination of sugars. Nature 168:167–167

    Article  CAS  Google Scholar 

  • Echeveste P, Agustí S, Dachs J (2010) Cell size dependent toxicity thresholds of polycyclic aromatic hydrocarbons to natural and cultured phytoplankton populations. Environ Pollut 158:299–307

    Article  CAS  Google Scholar 

  • El-Sheekh MM, Ghareib M, Abou-El-Souod G (2012) Biodegradation of phenolic and polycyclic aromatic compounds by some algae and cyanobacteria. J Bioremediat Biodegrad 3

  • Fan CW, Reinfelder JR (2003) Phenanthrene accumulation kinetics in marine diatoms. Environ Sci Technol 37:3405–3412

    Article  CAS  Google Scholar 

  • Fatma T, Khan M, Choudhary M (2007) Impact of environmental pollution on cyanobacterial proline content. J Appl Phycol 19:625–629

    Article  Google Scholar 

  • Fayeulle A, Veignie E, Schroll R, Munch JC, Rafin C (2019) PAH biodegradation by telluric saprotrophic fungi isolated from aged PAH-contaminated soils in mineral medium and historically contaminated soil microcosms. J Soil Sediment 19:3056–3067

    Article  CAS  Google Scholar 

  • Ghanbarzadeh M, Niknam V, Soltani N, Ebrahimzadeh H (2019) Leptolyngbya fragilis ISC 108 is the most effective strain for dodecane biodegradation in contaminated soils. Int J Phytoremediat 21:908–920

    Article  CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I Occurrence in higher plants. Plant Physiol 59:309–314

    Article  CAS  Google Scholar 

  • González-Aguilar G, Tiznado-Hernandez M, Zavaleta-Gatica R, Martınez-Téllez M (2004) Methyl jasmonate treatments reduce chilling injury and activate the defense response of guava fruits. Biochem Biophys Res Commun 313:694–701

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hong YW, Yuan DX, Lin QM, Yang TL (2008) Accumulation and biodegradation of phenanthrene and fluoranthene by the algae enriched from a mangrove aquatic ecosystem. Mar Poll Bull 56:1400–1405

    Article  CAS  Google Scholar 

  • Jebara S, Jebara M, Limam F, Aouani ME (2005) Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities in common bean (Phaseolus vulgaris) nodules under salt stress. J Plant Physiol 162:929–936

    Article  CAS  Google Scholar 

  • Ji NK, Barot M, Khan SR (2013) Some intermediate bio-transformants during biodegradation of high molecular weight phenanthrene and fluoranthene by cyanobacterial species–Aulosira Fertilissima Ghose. Int J Appl Sci Biotechnol 1:97–105

    Article  Google Scholar 

  • Ji MK, Yun HS, Hwang BS, Kabra AN, Jeon BH, Choi J (2016) Mixotrophic cultivation of Nephroselmis sp. using industrial wastewater for enhanced microalgal biomass production. Ecol Eng 95:527–533

    Article  Google Scholar 

  • Jia X, He Y, Jiang D, Liu C, Lu W (2019) Construction and analysis of an engineered Escherichia coli-Pseudomonas aeruginosa co-culture consortium for phenanthrene bioremoval. Biochem Eng J 148:214–223

    Article  CAS  Google Scholar 

  • Kumar MS, Muralitharan G, Thajuddin N (2009) Screening of a hypersaline cyanobacterium, Phormidium tenue, for the degradation of aromatic hydrocarbons: naphthalene and anthracene. Biotechnol Lett 31:1863–1866

    Article  CAS  Google Scholar 

  • Kumar JN, Amb MK, Bora A (2010) Chronic response of Anabaena fertilissima Rao, CB on growth, metabolites and enzymatic activities by chlorophenoxy herbicide. Pest Biochem Physiol 98:168–174

    Article  Google Scholar 

  • Leganés F, Sánchez-Maeso E, Fernández-Valiente E (1987) Effect of indoleacetic acid on growth and dinitrogen fixation in cyanobacteria. Plant Cell Physiol 28:529–533

    Google Scholar 

  • Lei A, Hu Z, Wong Y, Tam NF (2006) Antioxidant responses of microalgal species to pyrene. J Appl Phycol 18:67–78

    Article  CAS  Google Scholar 

  • Lei AP, Hu ZL, Wong YS, Tam NF (2007) Removal of fluoranthene and pyrene by different microalgal species. Bioresour Technol 98:273–280

    Article  CAS  Google Scholar 

  • Liang Y, Sarkany N, Cui Y (2009) Biomass and lipid productivities of Chlorella vulgaris under autotrophic, heterotrophic and mixotrophic growth conditions. Biotechnol Lett 31:1043–1049

    Article  CAS  Google Scholar 

  • Lin CC, Kao CH (2000) Effect of NaCl stress on H2O2 metabolism in rice leaves. Plant Growth Regul 30:151–155

    Article  CAS  Google Scholar 

  • MacDonald MJ, D’Cunha GB (2007) A modern view of phenylalanine ammonia lyase. Biochem Cell Biol 85:273–282

    Article  CAS  Google Scholar 

  • Liu J, Zhang J, Zhan C, Liu H, Zhang L, Hu T, Xing X, Qu C (2019) Polycyclic aromatic hydrocarbons (PAHs) in urban street dust of Huanggang, central China: status, sources and human health risk assessment. Aerosol Air Qual Res 19:221–223

    Article  CAS  Google Scholar 

  • Liu H, Tan X, Guo J, Liang X, Xie Q, Chen S (2020) Bioremediation of oil-contaminated soil by combination of soil conditioner and microorganism. J Soil Sediment 20:2121–2129

    Article  CAS  Google Scholar 

  • Macfie S, Tarmohamed Y, Welbourn P (1994) Effects of cadmium, cobalt, copper, and nickel on growth of the green alga Chlamydomonas reinhardtii: the influences of the cell wall and pH. Arch Environ Contamin Toxicol 27:454–458

    Article  CAS  Google Scholar 

  • Marker A (1972) The use of acetone and methanol in the estimation of chlorophyll in the presence of phaeophytin. Freshw Biol 2:361–385

    Article  Google Scholar 

  • Matkowski A, Zielińska S, Oszmiański J, Lamer-Zarawska E (2008) Antioxidant activity of extracts from leaves and roots of Salvia miltiorrhiza Bunge, S. przewalskii Maxim., and S. verticillata L. Bioresour Technol 99:7892–7896

    Article  CAS  Google Scholar 

  • Mei X, Lin DH, Xu Y, Wu YY, Tu YY (2009) Effects of phenanthrene on chemical composition and enzyme activity in fresh tea leaves. Food Chem 115:569–573

    Article  CAS  Google Scholar 

  • Modiri S, Sharafi H, Alidoust L, Hajfarajollah H, Haghighi O, Azarivand A, Zamanzadeh Z, Zahiri HS, Vali H, Noghabi KA (2015) Lipid production and mixotrophic growth features of cyanobacterial strains isolated from various aquatic sites. Microbiol 161:662–673

    Article  CAS  Google Scholar 

  • Mohanty P, Matysik J (2001) Effect of proline on the production of singlet oxygen. Amino Acids 21:195–200

    Article  Google Scholar 

  • Neethu S, Midhun SJ, Radhakrishnan E, Jyothis M (2021) Microbially synthesized nanomaterials for remediation of contaminated soil and water environment. Microbe Mediated Remediation of Environmental Contaminants. Elsevier, pp 157–176

  • Nirmal Kumar J, Patel JG, Kumar RN, Khan SR (2014) Chronic response of three different cyanobacterial species on growth, pigment, and metabolic variations to the high molecular weight polycyclic aromatic hydrocarbon–pyrene. Polycycl Aromat Compd 34:143–160

    Article  CAS  Google Scholar 

  • Odukoya J, Lambert R, Sakrabani R (2019) Understanding the impacts of crude oil and its induced abiotic stresses on agrifood production: a review. Horticulturae 5:47

    Article  Google Scholar 

  • Panah B, Najafi F, Soltani N, Nejad R, Babaei S (2015) Biodegradation ability and physiological responses of cyanobacterium Leptolyngbya sp. ISC 25 under naphthalene treatment. Algologia 25:125–134

    Article  Google Scholar 

  • Patel JG, Kumar JN, Khan SR (2015) Consequences of environmentally hazardous polycyclic aromatic hydrocarbon-anthracene treatment on cyanobacteria. Int J Appl Sci Biotechnol 3:381–386

    Article  CAS  Google Scholar 

  • Peng W, Li X, Xiao S, Fan W (2018) Review of remediation technologies for sediments contaminated by heavy metals. J Soils Sediments 18:1701–1719

    Article  CAS  Google Scholar 

  • Perez-Garcia O, Bashan Y (2015) Microalgal heterotrophic and mixotrophic culturing for bio-refining: From metabolic routes to techno-economics. Algal Biorefineries 2:61–131

    Article  Google Scholar 

  • Podkuiko L (2013) The effects of two crude oil solutions to phytoplankton species. In: Tartu Ülikool

  • Raymond J, Rakariyatham N, Azanza J (1993) Purification and some properties of polyphenoloxidase from sunflower seeds. Phytochemistry 34:927–931

    Article  CAS  Google Scholar 

  • Roelofs D, Bicho RC, de Boer TE, Castro-Ferreira MP, Montagne-Wajer K, van Gestel CA, Soares AM, van Straalen NM, Amorim MJ (2016) Mechanisms of phenanthrene toxicity in the soil invertebrate, Enchytraeus Crypticus. Environ Toxicol Chem 35:2713–2720

    Article  CAS  Google Scholar 

  • Román RB, Alvarez-Pez J, Fernández FA, Grima EM (2002) Recovery of pure B-phycoerythrin from the microalga Porphyridium cruentum. J Biotechnol 93:73–85

    Article  Google Scholar 

  • Safafar H, Van Wagenen J, Møller P, Jacobsen C (2015) Carotenoids, phenolic compounds and tocopherols contribute to the antioxidative properties of some microalgae species grown on industrial wastewater. Mar Drugs 13:7339–7356

    Article  CAS  Google Scholar 

  • Safonova E, Kvitko K, Kuschk P, Möder M, Reisser W (2005) Biodegradation of phenanthrene by the green alga Scenedesmus obliquus ES-55. Eng Life Sci 5:234–239

    Article  CAS  Google Scholar 

  • Sharma I (2020) Bioremediation techniques for polluted environment: concept, advantages, limitations, and prospects. Trace Metals in the environment-new approaches and recent advances: IntechOpen

  • 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

  • Singh D, Khattar J, Nadda J, Singh Y, Garg A, Kaur N, Gulati A (2011) Chlorpyrifos degradation by the cyanobacterium Synechocystis sp. strain PUPCCC 64. Environ Sci Pollut Res Int 18:1351–1359

    Article  CAS  Google Scholar 

  • Song H, Wang YS, Sun CC, Wu ML, Peng YL, Deng C, Li QP (2011) Effects of polycyclic aromatic hydrocarbons exposure on antioxidant system activities and proline content in Kandelia candel. Oceanol Hydrobiol Stud 40: 9-18

    Article  CAS  Google Scholar 

  • Subashchandrabose SR, Ramakrishnan B, Megharaj M, Venkateswarlu K, Naidu R (2013) Mixotrophic cyanobacteria and microalgae as distinctive biological agents for organic pollutant degradation. Environ Int 51:59–72

    Article  CAS  Google Scholar 

  • Tao W, Lin J, Wang W, Huang H, Li S (2020) Biodegradation of aliphatic and polycyclic aromatic hydrocarbons by the thermophilic bioemulsifier-producing Aeribacillus pallidus strain SL-1. Ecotoxicol Environ Saf 189:109994

    Article  CAS  Google Scholar 

  • Torabi S, Niknam V (2011) Effects of iso-osmotic concentrations of NaCl and mannitol on some metabolic activity in calluses of two Salicornia species. In Vitro Cell Dev Biol Plant 47:734–742

    Article  CAS  Google Scholar 

  • Trabelsi N, Megdiche W, Ksouri R, Falleh H, Oueslati S, Soumaya B, Hajlaoui H, Abdelly C (2010) Solvent effects on phenolic contents and biological activities of the halophyte Limoniastrum monopetalum leaves. LWT-Food Sci Technol 43:632–639

    Article  CAS  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

  • Xu J, Duan X, Yang J, Beeching JR, Zhang P (2013) Enhanced reactive oxygen species scavenging by overproduction of superoxide dismutase and catalase delays postharvest physiological deterioration of cassava storage roots. Plant Physiol 161:1517–1528

    Article  CAS  Google Scholar 

  • Yun J, Rocic P, Pung YF, Belmadani S, Carrao ACR, Ohanyan V, Chilian WM (2009) Redox-dependent mechanisms in coronary collateral growth: the “redox window” hypothesis. Antioxid Redox Signal 11:1961–1974

    Article  CAS  Google Scholar 

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Acknowledgements

The funding and facilities for this research were provided equally by the Academic Center for Education, Culture, and Research (ACECR) of Iran and University of Tehran.

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Correspondence to Vahid Niknam.

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Ghanbarzadeh, M., Niknam, V., Soltani, N. et al. Removal of Phenanthrene by some microalga species and study of antioxidative compounds in Nostoc calcicola ISC 89. J Soils Sediments 22, 109–119 (2022). https://doi.org/10.1007/s11368-021-03065-z

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