Abstract
Handling of two nitro-aromatic compounds, 4-nitroaniline (4NA) and 4-nitrophenol (4NP), simultaneously by Chlorella pyrenoidosa was investigated. Algae would secrete or degrade nitro-aromatic compounds depending on different environmental conditions, in which the mode of handling was determined by the relative formation and degradation rate of the compound. Repeated intermittent trigger with externally added 4NA would induce the continuous secretion of 4NA by algae. Simultaneous exposure of both 4NA and 4NP to algae at normal condition would induce the algae to secrete both compounds. An increase in 4NA exposure concentration would elevate both 4NA and 4NP secretion, and that would be inhibited by the stress conditions of starving or lack of oxygen. Increased 4NA degradation per production rate induced by starving or lack of oxygen might explain the subsequent decrease in 4NA secretion in the presence of 4NP in algae. For 4NP in the presence of 4NA, secretion at normal condition was completely stopped and turned to degradation mode in stress conditions. The decreased formation and increased degradation of 4NP during starving for replenishing energy would explain the net degradation of 4NP in starving condition. The condition of lack of oxygen would inhibit the 4NP formation from 4NA via oxidative deamination, while the degradation of 4NP might not be significantly affected because alternative pathway of degradation via nitro-reduction was available. It may lead to the degradation rate exceeding the formation and explain the net degradation of 4NP in the condition of lack of oxygen.
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Abbreviations
- TCP:
-
2,4,6-Trichlorophenol
- 4NA:
-
4-Nitroaniline
- 4NP:
-
4-Nitrophenol
- ACN:
-
Acetonitrile
- TAP:
-
Tris-acetate-phosphate
References
Adrian S (1999) High-rate biodegradation of 3- and 4-nitroaniline. Chemosphere 39:2325–2346
Alif A, Boule P (1991) Phototransformation of nitrophenols induced by excitation of nitrite and nitrate ions. J Photochem Photobiol A Chem 59:357–367
Azeem K, Muhammad A, David EC (2009) Biodegradation potential of pure and mixed bacterial cultures for removal of 4-nitroaniline from textile dye wastewater. Water Res 43:1110–1116
Cassidy MB, Lee H, Trevors JT, Zablotowicz RB (1999) Chlorophenol and nitrophenol metabolism by Sphingomonas sp UG30. J Ind Microbiol Biotechnol 23:232–241
De Lara-Isassi G, Álvarez-Hernández S, Lozano-Ramírez C, Hernández-Soto N, Dreckmann KM (2000) Temporal and spatial production of agglutinins in marine macroalgae from the Mexican Caribbean. J Phycol 36:17
Doke N (1983) Involvement of superoxide generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol Plant Pathol 23:345–357
Fong SS, Burgard AP, Herring CD, Knight EM, Blattner FR, Maranas CD, Palsson BO (2005) In silico design and adaptive evolution of Escherichia coli for production of lactic acid. Biotechnol Bioeng 91:643–648
Gao QT, Wong YS, Tam NFY (2011) Removal and biodegradation of nonylphenol by immobilized Chlorella vulgaris. Bioresour Technol 102:10230–10238
Gorman DS, Levine R (1965) Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proc Natl Acad Sci U S A 54:1665–1669
Hirooka T, Ju KS, Parales RE (2010) Nitroaromatic compounds, from synthesis to biodegradation. Microbiol Mol Biol Rev 74:250–272
Jormalainen V, Honkanen T, Koivikk R, Eränen J (2003) Induction of phlorotannin production in a brown alga: defense or resource dynamics? Oikos 103(3):640
Ju K, Parales RE (2010) Nitroaromatic compounds, from synthesis to biodegradation. Microbiol Mol Biol Rev 74:250–272
Khan F, Pandey J, Vikram S, Pal D, Cameotra SS (2013) Aerobic degradation of 4-nitroaniline (4NA) via novel degradation intermediates by Rhodococcus sp. strain FK48. J Hazard Mater 254–255:72–78
Kind T, Meissen JK, Yang D, Nocito F, Vaniya A, Cheng Y, VanderGheynst J, Fiehn O (2012) Qualitative analysis of algal secretions with multiple mass spectrometric platforms. J Chromatogr A 1244:139–147
Kozak AJ, Liu F, Funovics P, Jacoby A, Kubant R, Malinski T (2005) Role of peroxynitrite in the process of vascular tone regulation by nitric oxide and prostanoids—a nanotechnological approach. Prostaglandins Leukot Essent Fat Acids 72:105–113
La Barre S, Potin P, Leblanc C, Delage L (2010) The halogenated metabolism of brown algae (Phaeophyta), its biological importance and its environmental significance. Mar Drugs 8(4):988–1010
LeFlaive J, Loic T (2007) Algal and cyanobacterial secondary metabolites in freshwaters: a comparison of allelopathic compounds and toxins. Freshw Biol 52(2):199–214
Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M (2009) NO signals in the haze: nitric oxide signalling in plant defence. Curr Opin Plant Biol 12:451–458
Luther M (1990) Degradation of different substituted aromatic compounds as nutrient sources by the green alga Scenedesmus obliquus. Dechema Biotechnol Conf 4:613–615
Masojídek J, Prášil O (2010) The development of microalgal biotechnology in the Czech Republic. J Ind Microbiol Biotechnol 37(12):1307–1317
Narayanan KB, Sakthivel N (2011) Heterogeneous catalytic reduction of anthropogenic pollutant, 4-nitrophenol by silver-bionanocomposite using Cylindrocladium floridanum. Bioresour Technol 102:10737–10740
Nevim S, Arzu H, Gülin K, Zekiye Ç (2002) Photocatalytic degradation of 4-nitrophenol in aqueous TiO2 suspensions: theoretical prediction of the intermediates. J Photochem Photobiol A Chem 146:189–197
Newman DJ, Cragg GM (2007) Natural products as sources of new drugs over the last 25 years. J Nat Prod 70:461–477
Padmaja S, Huie RE (1993) The reaction of nitric oxide with organic peroxyloradicals. Biochem Biophys Res Commun 195:539–544
Perez-Garcia O, Escalante FME, de-Bashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: metabolism and potential products. Water Res 45:11–36
Rajamani S, Teplitski M, Kumar A, Krediet C, Sayre R, Bauer W (2011) N-acyl homoserine lactone lactonase, AiiA inactivation of quorum-sensing agonists produced by Chlamydomonas reinhardtii (Chlorophyta) and characterization of AiiA transgenic algae. J Phycol 47(5):1219–1227
Rost TL, Barbour MG, Stocking CR, Murphy TM (2009) Plant biology. Thomson Brooks/Cole
Rowland M, Tozer TN (1989) Clinical pharmacokinetics: concepts and applications. Lea & Febiger, USA
Saito S, Yamamoto-Katou A, Yoshioka H, Doke N, Kawakita K (2006) Peroxynitrite generation and tyrosine nitration in defense responses in tobacco BY-2 cells. Plant Cell Physiol 47:689–697
Semple KT, Cain RB (1996) Biodegradation of phenolics by Ochromonas danica. Appl Environ Microbiol 62:1265–1273
Semple KT, Cain RB, Schmidt S (1999) Biodegradation of aromatic compounds by microalgae. FEMS Microbiol Lett 170:291–300
Shibata T, Hama Y, Miyasaki T, Ito M, Nakamura T (2006) Extracellular secretion of phenol substances from living brown algae. J Appl Phycol 18:787–794
Soojhawon I, Lokhande PD, Kodam KM, Gawai KR (2005) Biotransformation of nitroaromatics and their effects on mixed function oxidase system. Enzym MicrobTechnol 37:527–533
Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96
Stamler JS (1994) Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 78:931–936
Takahashi N, Nakai T, Satoh Y, Katoh Y (1994) Variation of biodegradability of nitrogenous organic compounds by ozonation. Water Res 28:1563–1570
Wilkie AC, Edmundson SJ, Duncan JG (2011) Indigenous algae for local bioresource production: phycoprospecting. Energy Sustain Dev 15(4):365–371
Willey JM, Sherwood LM, Woolverton CJ, Prescott LM (2009) Prescott’s principles of microbiology. McGraw-Hill Higher Education
Yu HY, Wang SJ, Cai ZW, Poon K (2012) Differential handling of toxic chemicals by stress shock algae. Int J Environ Pollut Remed 1:111–118
Zheng Y, Liu D, Xu H, Zhong Y, Yuan Y, Xong L, Li W (2009) Biodegradation of p-nitrophenol by Pseudomonas aeruginosa HS-D38 and analysis of metabolites with HPLC-ESI/MS. Int Biodeterior Biodegrad 63:1125–1129
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The authors would like to thank UIC College Research Grant R201207 for supporting this project.
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Xu, C., Wang, R., Zhang, Y.F. et al. Stress response of Chlorella pyrenoidosa to nitro-aromatic compounds. Environ Sci Pollut Res 22, 3784–3793 (2015). https://doi.org/10.1007/s11356-014-3582-4
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DOI: https://doi.org/10.1007/s11356-014-3582-4