Abstract
In the present study, the potential of a microalga, Chlorella vulgaris, was assessed for the bioremediation of fluoranthene (FLT), a four ring polycyclic aromatic hydrocarbon (PAH). With an initial cell density of C. vulgaris (OD680 = 0.100), 54–58% of 25 μM FLT was removed from the growth medium within 3 days and almost 90–94% after 7 days of incubation. Enzymatic studies confirmed that the enzyme involved in FLT metabolism was catechol 2,3, dioxygenase (C2,3D) which increased almost 2 times in 5 μM FLT and 2.4 times in 25 μM FLT inoculated culture. Activity of dehydrogenase and superoxide dismutase (SOD) was significantly reduced, while peroxidase (POD) activity was induced very prominently in FLT inoculated cultures. Changes in growth, physiological parameters and biochemical compositions of the algae with 5 μM and 25 μM FLT were also analyzed and compared to control. The analysis showed that parameters including growth rate, biomass, chlorophyll, carbohydrate and protein contents, were negatively affected by the higher concentration of FLT, whereas the lipid and carotenoids content significantly increased. To our knowledge, this is the first report to suggest the role of C2,3D pathway for the metabolism of FLT in a eukaryotic algae.
Similar content being viewed by others
References
Aksmann A, Tukaj Z (2008) Intact anthracene inhibits photosynthesis in algal cells: a fluorescence induction study on Chlamydomonas reinhardtii cw92 strain. Chemosphere 74:26–32. https://doi.org/10.1016/j.chemosphere.2008.09.064
Ashok A, Kottuparambil S, Høj L, Negri AP, Duarte CM, Agustǐ S (2020) Accumulation of 13C-labelled phenanthrene in phytoplankton and transfer to corals resolved using cavity ring-down spectroscopy. Ecotoxicol Environ Saf 196:110511. https://doi.org/10.1016/j.ecoenv.2020.110511
Beauchamp CO, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287. https://doi.org/10.1016/0003-2697(71)90370-8
Cao B, Geng A, Loh K-C (2008) Induction of ortho- and meta- cleavage pathways in Pseudomonas in biodegradation of high benzoate concentration: MS identification of catabolic enzymes. Appl Microbiol Biotechnol 81:99–107. https://doi.org/10.1007/s00253-008-1728-3
Cemiglia CE, Gibson DT, Van Baalen C (1982) Naphthalene metabolism by diatoms isolated from Kachemak Bay Region of Alaska. J Gen Microbial 128:987–990. https://doi.org/10.1099/00221287-128-5-987
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. https://doi.org/10.1897/05-354R.1
Choudhary R, Saroha AE, Swarnkar PL (2011) Effect of abscisic acid and hydrogen peroxide on antioxidant enzymes in Syzygium cumini plant. J Food Sci Tech 49:649–652. https://doi.org/10.1007/s13197-011-0464-3
Croxton AN, Wikfors GH, Schulterbrandt-Gragg III RD (2015) The use of flow cytometric applications to measure the effects of PAHs on growth, membrane integrity, and relative lipid content of the benthic diatom. Mar Pollut Bull 91:160–165. https://doi.org/10.1016/j.marpolbul.2014.12.010
Dere S, Gunes T, Sivaci R (1998) Spectrophotometric determination of chlorophyll—a, b and total carotenoid contents of some algae species using different solvents. Turk J Bot 22:13–17
El-Sheekh MM, Ghareib MM, EL-Souod GW (2012) Biodegradation of Phenolic and polycyclic aromatic compounds by some algae and cyanobacteria. J Bioremed Biodegrad 3:1. https://doi.org/10.4172/2155-6199.1000133
George B, Pancha I, Desai C, Chokshi K, Paliwal C, Ghosh T, Mishra S (2014) Effects of different media composition, light intensity and photoperiod on morphology and physiology of freshwater microalgae Ankistrodesmus falcatus—a potential strain for bio-fuel production. Bioresour Technol 171:367–374. https://doi.org/10.1016/j.biortech.2014.08.086
Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15. https://doi.org/10.1016/j.jhazmat.2009.03.137
Hong Y-W, Yuan DX, Lin Q-M, Yang T-L (2008) Accumulation and biodegradation of phenanthrene and fluoranthene by the algae enriched from a mangrove aquatic ecosystem. Mar Pollut Bull 56:1400–1405. https://doi.org/10.1016/j.marpolbul.2008.05.003
Hussar E, Richards S, Lin ZQ, Dixon RP, Johnson KA (2012) Human health risk assessment of 16 priority polycyclic aromatic hydrocarbons in soils of Chattanooga, Tennessee, USA. Water Air Soil Pollut 223:5535–5548. https://doi.org/10.1007/s11270-012-1265-7
Kanaly RA, Hharayama S (2000) Biodegradation of high-molecular-weight polycyclic aromatic Hydrocarbons by Bacteria. J Bacteriol 182:2059–2067. https://doi.org/10.1128/JB.182.8.2059-2067.2000
Karigar CS, Rao SS (2011) Role of Microbial Enzymes in the Bioremediation of Pollutants: a Review. Enzyme Res 7:805187. https://doi.org/10.4061/2011/805187
Kreslavski VD, Brestic M, Zharmukhamedov SK, Yu Lyubimov V, Lankin AV, Jajoo A, SI Allakhverdiev SI (2017) Mechanisms of inhibitory effects of polycyclic aromatic hydrocarbons in photosynthetic primary processes in pea leaves and thylakoid preparations. Plant Biol 19:683–688. https://doi.org/10.1111/plb.12598
Kumar RR, Rao PH, Subramanian VV, Sivasubramanian V (2014) Enzymatic and non-enzymatic antioxidant potentials of Chlorella vulgaris grown in effluent of a confectionery industry. J Food Sci Technol 51:322–328. https://doi.org/10.1007/s13197-011-0501-2
Laurens LML, Dempster TA, Jones HDT, Wolfrum EJ, Wychen SV, McAllister JSP, Rencenberger M, Parchert KJ, Gloe LM (2012) Algal biomass constituent analysis: method uncertainties and investigation of the underlying measuring chemistries. Anal Chem 84:1879–1887. https://doi.org/10.1021/ac202668c
Lei A, Hu Z, Wong Y, Tam N (2006) Antioxidant responses of microalgal species to pyrene. J Appl Phycol 18:67–78. https://doi.org/10.1007/s10811-005-9016-4
Lei AP, Wong YS, Tam NFY (2002) Removal of pyrene by different microalgal species. Water Sci Technol 46:195–201
Lei A-P, Hu Z-L, Wong Y-S, Tam NF-Y (2007) Removal of Fluoranthene and pyrene by different microalgal species. Bioresour Technol 98:273–280. https://doi.org/10.1016/j.biortech.2006.01.012
Li M, Hu C, Zhu Q (2006) Copper and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in the microalga Pavlova viridis (Prymnesiophyceae). Chemosphere 62:565–572. https://doi.org/10.1016/j.chemosphere.2005.06.029
Lim SL, Chu WL, Phang SM (2010) Use of Chlorella vulgaris for bioremediation of textile waste water. Bioresour Technol 101:7314–7322. https://doi.org/10.1016/j.biortech.2010.04.092
Ma Y, McGree J, Liu A, Deilami K, Egodawatta P, Goonetilleke A (2017) Catchment scale assessment of risk posed by traffic generated heavy metals and polycyclic aromatic hydrocarbons. Ecotoxicol Environ Saf 144:593–600. https://doi.org/10.1016/j.ecoenv.2017.06.073
Meulenberg R, Rijnaarts HHM, Doddema HJ, Field JA (1997) Partially oxidized polycyclic aromatic hydrocarbons show an increased bioavailability and biodegradability. FEMS Microbiol Lett 154:45–49. https://doi.org/10.1016/S0378-1097(97)00176-6
Mishra SK, Suh WI, Farooq W, Moon M, Shrivastav A, Park MS, Yang J-W (2014) Rapid quantification of microalgal lipids in aqueous medium by a simple colorimetric method. Bioresour Technol 155:330–333. https://doi.org/10.1016/j.biortech.2013.12.077
Olmos-Espejel JJ, Garcia de Llasera MP, Velasco-Cruz M (2012) Extraction and analysis of polycyclic aromatic hydrocarbons and benzo[a]pyrene metabolites in microalgae cultures by off-line/on-line methodology based on matrix solid-phase dispersion, solid-phase extraction and high-performance liquid chromatography. J Chromatogr A 1262:138–147. https://doi.org/10.1016/j.chroma.2012.09.015
Pancha I, Chokshi K, George B, Ghosh T, Paliwal C, Maurya R, Mishra S (2014) Nitrogen stress triggered biochemical and morphological changes in the microalgae Scenedesmus sp. CCNM 1077. Bioresour Technol 156:146–154. https://doi.org/10.1016/j.biortech.2014.01.025
Phale PS, Sharma A, Gautam K (2019) Microbial degradation of xenobiotics like aromatic pollutants from the terrestrial environments. In: Prasad MNV, Vithanage M, Kapley A (eds.) Pharmaceuticals and personal care products: waste management and treatment technology, Butterworth-Heinemann, p 259–278. https://doi.org/10.1016/B978-0-12-816189-0.00011-1
Ruiz J, Alvarez P, Arbib Z, Garrido C, Barragan J, Perales JA (2011) Effect of nitrogen and phosphorus concentration on their removal kinetic in treated urban wastewater by Chlorella vulgaris. Int J Phytorem 13:884–896. https://doi.org/10.1080/15226514.2011.573823
Schoeny R, Cody T, Warshawsky D, Radike M (1988) Metabolism of mutagenic polycyclic aromatic hydrocarbons by photosynthetic algal species. Mutat Res 197:289–302. https://doi.org/10.1016/0027-5107(88)90099-1
Semple KT, Cain RB (1996) Biodegradation of phenols by the alga Ochromonas danica. App. Environ Microbiol 62:1265–1273
Siaut M, Cuine S, Cagnon C, Fessler B, Nguyen M, Carrier P, Beyly A, Beisson F, Triantaphylides C, Li-Beisson Y, Peltier G (2011) Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability be-tween common laboratory strains and relationship with starch reserves. BMC Biotechnol 11:7. https://doi.org/10.1186/1472-6750-11-7
Slocombe SP, Ross M, Thomas N, McNeill S, Stanley MS (2013) A rapid and general method for measurement of protein in micro-algal biomass. Bioresour Technol 129:51–57. https://doi.org/10.1016/j.biortech.2012.10.163
Song J, Sung J, Kim YM, Zylstra GJ, Kim E (2000) Roles of the meta and ortho-cleavage pathways for the efficient utilization of aromatic hydrocarbons by Sphingomonas yanoikuyae B1. J Microbiol 38:245–249
Subashchandrabose SR, Logeshwaran P, Venkateswarlu K, Naidu R, Megharaj M (2017) Pyrene degradation by Chlorella sp. MM3 in liquid medium and soil slurry: Possible role of dihydrolipoamide acetyltransferase in pyrene biodegradation. Algal Res 23:223–232. https://doi.org/10.1016/j.algal.2017.02.010
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. https://doi.org/10.1016/j.envint.2012.10.007
Tam NFY, Chong AMY, Wong YS (2002) Removal of tributyltin (TBT) by live and dead microalgal cells. Mar Pollut Bull 45:362–371. https://doi.org/10.1016/S0025-326X(02)00184-4
Tomar RS, Jajoo A (2015) Photomodified fluoranthene exerts more harmful effects as compared to intact fluoranthene by inhibiting growth and photosynthetic processes. Ecotoxicol Environ Saf 122:31–36. https://doi.org/10.1016/j.ecoenv.2015.07.002
Warshawsky D, Cody T, Radike M, Reilman R, Schumann B, LaDow K, Schneider J (1995) Biotransformation of benzo[a]pyrene and other polycyclic aromatic hydrocarbons and heterocyclic analogs by several green algae and other algal species under gold and white light. Chem Biol Interact 97:131–148. https://doi.org/10.1016/0009-2797(95)03610-X
Xie J, Hu W, Pei H, Dun M, Qi F (2008) Detection of amount and activity of living algae in fresh water by dehydrogenase activity (DHA). Environ Monit Assess 146:473–478. https://doi.org/10.1007/s10661-008-0250-5
Zhang FQ, Wang YS, Lou ZP, Dong JD (2007) Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67:44–50. https://doi.org/10.1016/j.chemosphere.2006.10.007
Funding
RST thanks Council of Scientific and Industrial Research for the CSIR-RA fellowship (09/301/(0134)/2018-EMR-I).
Author information
Authors and Affiliations
Contributions
RST, AJ conceptualized the problem and planned the experiments, RST carried out work and RST, AJ wrote and edited the paper.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
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
Tomar, R.S., Jajoo, A. Enzymatic pathway involved in the degradation of fluoranthene by microalgae Chlorella vulgaris. Ecotoxicology 30, 268–276 (2021). https://doi.org/10.1007/s10646-020-02334-w
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-020-02334-w