Skip to main content
Log in

Exploration of phenol tolerance mechanism through antioxidative responses of an evolved strain, Chlorella sp. L5

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Phenol is a typical pollutant which can be degraded by microalgae. Phenol induces formation of reactive oxygen species (ROS). Tolerance to oxidative damage produced by ROS is critical for phenol degradation by microalgae. An evolved strain, Chlorella sp. L5 was obtained from Chlorella sp. L3 in a previous study. The current study investigated the phenol tolerance mechanism by the dynamic responses of antioxidative enzyme activities of Chlorella sp. L3 and Chlorella sp. L5 in TAP medium with and without 500 mg L−1 phenol. It was shown that the activities of superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD) were increased in Chlorella sp. L5 when phenol was added in the medium. They were also significantly higher than those of Chlorella sp. L3 under 500 mg L−1 phenol conditions. There were slight increases of the malondialdehyde (MDA) contents of Chlorella sp. L5 in TAP medium with and without 500 mg L−1 phenol while they were significantly lower than the MDA content of Chlorella sp. L3 under 500 mg L−1 phenol conditions. The results indicated that Chlorella sp. L5 had higher tolerance to 500 mg L−1 phenol than Chlorella sp. L3. The antioxidative responses of Chlorella sp. L3 and Chlorella sp. L5 in control and TAP medium + phenol were consisted with the results of the comparative transcriptomic analysis in another published result. The phenol tolerance mechanism was also confirmed by the photosynthetic efficiency under oxidative conditions and control.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Belghith T, Athmouni K, Bellassoued K, El Feki A, Ayadi H (2016) Physiological and biochemical response of Dunaliella salina to cadmium pollution. J Appl Phycol 28:991–999

    Article  CAS  Google Scholar 

  • Chia MA, Chimdirim PK, Japhet WS (2015) Lead induced antioxidant response and phenotypic plasticity of Scenedesmus quadricauda (Turp.) de Brebisson under different nitrogen concentrations. J Appl Phycol 27:293–302

    Article  CAS  Google Scholar 

  • Cho K, Lee CH, Ko K, Lee YJ, Kim KN, Kim MK, Chung YH, Kim D, Yeo IK, Oda T (2016) Use of phenol-induced oxidative stress acclimation to stimulate cell growth and biodiesel production by the oceanic microalga Dunaliella salina. Algal Res 17:61–66

    Article  Google Scholar 

  • Chokshi K, Pancha I, Ghosh A, Mishra S (2017) Nitrogen starvation-induced cellular crosstalk of ROS - scavenging antioxidants and phytohormone enhanced the biofuel potential of green microalga Acutodesmus dimorphus. Biotechnol Biofuels 10:60

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gao QT, Tam NF (2011) Growth, photosynthesis and antioxidant responses of two microalgal species, Chlorella vulgaris and Selenastrum capricornutum, to nonylphenol stress. Chemosphere 82:346–354

    Article  PubMed  CAS  Google Scholar 

  • Gao QT, Wong YS, Tam NFY (2017) Antioxidant responses of different microalgal species to nonylphenol-induced oxidative stress. J Appl Phycol 29:1317–1329

    Article  CAS  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron - transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  PubMed  CAS  Google Scholar 

  • Grudzinski W, Krzeminska I, Luchowski R, Nosalewicz A, Gruszecki WI (2016) Strong light induced yellowing of green microalgae Chlorella: a study on molecular mechanisms of the acclimation response. Algal Res 16:245–254

    Article  Google Scholar 

  • Ibanez SG, Alderete LGS, Medina MI, Agostini E (2012) Phytoremediation of phenol using Vicia sativa L. plants and its antioxidative response. Environ Sci Pollut Res 19:1555–1562

    Article  CAS  Google Scholar 

  • Ibaniez SG, Medina MI, Agostini E (2011) Phenol tolerance, changes of antioxidative enzymes and cellular damage in transgenic tobacco hairy roots colonized by arbuscular mycorrhizal fungi. Chemosphere 83:700–705

    Article  CAS  Google Scholar 

  • Klekner V, Kosaric N (1992) Degradation of phenols by algae. Environ Technol 13:493–501

    Article  CAS  Google Scholar 

  • Li DJ, Wang L, Zhao QY, Wei W, Sun YH (2015) Improving high carbon dioxide tolerance and carbon dioxide fixation capability of Chlorella sp by adaptive laboratory evolution. Bioresour Technol 185:269–275

    Article  PubMed  CAS  Google Scholar 

  • Liu F, Pang SJ (2010) Stress tolerance and antioxidant enzymatic activities in the metabolisms of the reactive oxygen species in two intertidal red algae Grateloupia turuturu and Palmaria palmata. J Exp Mar Biol Ecol 382:82–87

    Article  CAS  Google Scholar 

  • Lv H, Cui X, Tan Z, Jia S (2017) Analysis of metabolic responses of Dunaliella salina to phosphorus deprivation. J Appl Phycol 29:1251–1260

    Article  CAS  Google Scholar 

  • Martins PL, Marques LG, Colepicolo P (2015) Antioxidant enzymes are induced by phenol in the marine microalga Lingulodinium polyedrum. Ecotoxicol Environ Saf 116:84–89

    Article  PubMed  CAS  Google Scholar 

  • Menon KR, Balan R, Suraishkumar GK (2013) Stress induced lipid production in Chlorella vulgaris: relationship with specific intracellular reactive species levels. Biotechnol Bioeng 110:1627–1636

    Article  PubMed  CAS  Google Scholar 

  • Mittal S, Kumari N, Sharma V (2012) Differential response of salt stress on Brassica juncea: photosynthetic performance, pigment, proline, D1 and antioxidant enzymes. Plant Physiol Biochem 54:17–26

    Article  PubMed  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  PubMed  CAS  Google Scholar 

  • Palsson BO (2011) Adaptive laboratory evolution. Microbe 6:69–74

    Google Scholar 

  • Pang SJ, Jin ZH, Sun JZ, Gao SQ (2007) Temperature tolerance of young sporophytes from two populations of Laminaria japonica revealed by chlorophyll fluorescence measurements and short-term growth and survival performances in tank culture. Aquaculture 262:493–503

  • Portnoy VA, Bezdan D, Zengler K (2011) Adaptive laboratory evolution—harnessing the power of biology for metabolic engineering. Curr Opin Biotechnol 22:590–594

    Article  PubMed  CAS  Google Scholar 

  • Priyadharshini SD, Bakthavatsalam AK (2016) Optimization of phenol degradation by the microalga Chlorella pyrenoidosa using Plackett-Burman design and response surface methodology. Bioresour Technol 207:150–156

    Article  CAS  Google Scholar 

  • Scragg AH (2006) The effect of phenol on the growth of Chlorella vulgaris and Chlorella VT-1. Enzyme Microb Tech 39:796–799

    Article  CAS  Google Scholar 

  • Semple KT, Cain RB (1997) Degradation of phenol and its methylated homologues by Ochromonas danica. FEMS Microbiol Lett 152:133–139

    Article  CAS  Google Scholar 

  • Stephen DP, Ayalur BK (2017) Effect of nutrients on Chlorella pyrenoidosa for treatment of phenolic effluent of coal gasification plant. Environ Sci Pollut Res 24:13594–13603

    Article  CAS  Google Scholar 

  • Sueoka N (1960) Mitotic replication of deoxyribonucleic acid in Chlamydomonas reinhardi. Proc Natl Acad Sci U S A 46:83–91

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Swapnil P, Yadav AK, Srivastav S, Sharma NK, Srikrishna S, Rai AK (2017) Biphasic ROS accumulation and programmed cell death in a cyanobacterium exposed to salinity (NaCl and Na2SO4). Algal Res 23:88–95

    Article  Google Scholar 

  • Wang LB, Xue CZ, Wang L, Zhao QY, Wei W, Sun YH (2016a) Strain improvement of Chlorella sp for phenol biodegradation by adaptive laboratory evolution. Bioresour Technol 205:264–268

    Article  PubMed  CAS  Google Scholar 

  • Wang T, Ge H, Liu T, Tian X, Wang Z, Guo M, Chu J, Zhuang Y (2016b) Salt stress induced lipid accumulation in heterotrophic culture cells of Chlorella protothecoides: mechanisms based on the multi-level analysis of oxidative response, key enzyme activity and biochemical alteration. J Biotechnol 228:18–27

    Article  PubMed  CAS  Google Scholar 

  • Wu S, Meng YY, Cao XP, Xue S (2016) Regulatory mechanisms of oxidative species and phytohormones in marine microalgae Isochrysis zhangjiangensis under nitrogen deficiency. Algal Res 17:321–329

    Article  Google Scholar 

  • Zampieri M, Enke T, Chubukov V, Ricci V, Piddock L, Sauer U (2017) Metabolic constraints on the evolution of antibiotic resistance. Mol Syst Biol 13:917

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang YM, Chen H, He CL, Wang Q (2013) Nitrogen starvation induced oxidative stress in an oil-producing green alga Chlorella sorokiniana C3. PLoS One 8(7):e69225

  • Zhong Y, Chen T, Zheng W, Yang Y (2015) Selenium enhances antioxidant activity and photosynthesis in Ulva fasciata. J Appl Phycol 27:555–562

    Article  CAS  Google Scholar 

  • Zhou L, Cheng D, Wang L, Gao J, Zhao Q, Wei W, Sun Y (2017) Comparative transcriptomic analysis reveals phenol tolerance mechanism of evolved Chlorella strain. Bioresour Technol 227:266–272

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This study is supported by National Natural Science Foundation of China (21576278).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Quanyu Zhao.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, L., Yuan, Y., Li, X. et al. Exploration of phenol tolerance mechanism through antioxidative responses of an evolved strain, Chlorella sp. L5. J Appl Phycol 30, 2379–2385 (2018). https://doi.org/10.1007/s10811-018-1428-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-018-1428-z

Keywords

Navigation