Abstract
Cyanobacteria are photosynthetic autotrophic aquatic prokaryotes. One of the methods for controlling cyanobacterial blooms is to destroy the phycobiliproteins required for photosynthesis. In this study, to improve the biodegradation of the fluoroquinolones through inhibit cyanobacteria, the molecular docking scores of 32 fluoroquinolones (FQs) with four categories of phycobiliproteins from cyanobacteria were calculated after sine normalization to characterize the binding ability between them. A two-dimensional quantitative structure-activity relationship (2D-QSAR) model was constructed based on the comprehensive scores. Danofloxacin (DAN) with the highest comprehensive score was chosen for molecular modification. When docking with four categories of phycobiliproteins from cyanobacteria, the docking values of DAN-11 and DAN-16 were increased up to 35.75%. Moreover, their functional characteristics and environmentally friendly predictive values were improved. When the DAN-11 and DAN-16 molecules docked with the other cyanobacterial phycobiliproteins, indicating that the designed DAN derivatives had general applicability to poison cyanobacteria, the weak interaction forces might increase the binding ability between the DAN derivatives and the receptor phycobiliprotein compared with the target molecule.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Albini A, Monti S (2003) Photophysics and photochemistry of fluoroquinolones. Chem Soc Rev 32:238–250. https://doi.org/10.1039/b209220b
Bryant DA (2006) The molecular biology of cyanobacteria. Springer Sci Bus Media. https://doi.org/10.1007/978-94-011-0227-8
Brain RA, Hanson ML, Solomon KR, Brooks BW (2008) Aquatic plants exposed to pharmaceuticals: effects and risks. Rev Environ Contam T 192:67–115. https://doi.org/10.1007/978-0-387-71724-1_3
Boulanger B, Vargo JD, Schnoor JL, Schnoor JL, Hornbuckle KC (2005) Evaluation of perfluorooctane surfactants in a wastewater treatment system and in a commercial surface protection product. Environ Sci Technol 39:5524–5530. https://doi.org/10.1021/es050213u
Bharate SB, Yadav RR, Vishwakarma RA (2013) QSAR and pharmacophore study of Dyrk1A inhibitory meridianin analogs as potential agents for treatment of neurodegenerative diseases. Med Chem 9:152–161. https://doi.org/10.2174/157340613804488459
Castiglioni S, Fanelli R, Calamari D, Bagnati R, Zuccato E (2004) Methodological approaches for studying pharmaceuticals in the environment by comparing predicted and measured concentrations in River Po, Italy. Regul Toxicol Pharmacol 39:25–32. https://doi.org/10.1016/j.yrtph.2003.10.002
Contreras MC, Martinez-Oyanedel J, Bunster M, Legrand P, Piras C, Vernede X, Fontecilla-Camps JC (2001) Crystallization and 2.2 A resolution structure of R-phycoerythrin from Gracilaria chilensis: a case of perfect hemihedral twinning. Acta Crystallogr D Biol Crystallogr 57:52–60. https://doi.org/10.1107/S0907444900015274
Cuquerella MC, Bosca F, Miranda MA (2004) Photonucleophilic aromatic substitution of 6-fluoroquinolones in basic media: triplet quenching by hydroxide anion. J Organomet Chem 69:7256–7261. https://doi.org/10.1021/jo049293v
Diller DJ, Merz KM (2001) High throughput docking for library design and library prioritization. Proteins 43:113–124. https://doi.org/10.1002/1097-0134(20010501)43:2<113::aid-prot1023>3.0.co;2-t
Dittmann E, Wiegand C (2006) Cyanobacterial toxins-occurrence, biosynthesis and impact on human affairs. Mol Nutr Food Res 50:7–17. https://doi.org/10.1002/mnfr.200500162
Du MJ, Zhang D, Yl H, Zhao XH, Li Y (2019) Combined 2D-QSAR, principal component analysis and sensitivity analysis studies on fluoroquinolones’ genotoxicity. Int J Env Res Public Health 16:4156–4169. https://doi.org/10.3390/ijerph16214156
Emmerson AM, Jones AM (2003) The quinolones: decades of development and use. J Antimicrob Chemother 51:13–20. https://doi.org/10.1093/jac/dkg208
Evans S, Saleh M (2015) Cyanobacteria diversity in blooms from the Greater Sudbury area. J Water Res Protect 7:871–882. https://doi.org/10.4236/jwarp.2015.711071
Gérard G, Cohen-Bazire G, Bryant DA (1981) The structure of Gloeobacter violaceus and its phycobilisomes. Arch Microbiol 129:181–189. https://doi.org/10.1007/BF00425248
Ginebreda A, Muñoz I, Alda MLD, Brix R, López-Doval J, Barceló D (2010) Environmental risk assessment of pharmaceuticals in rivers: relationships between hazard indexes and aquatic macroinvertebrate diversity indexes in the Llobregat River (NE Spain). Environ Int 36:153–162. https://doi.org/10.1016/j.envint.2009.10.003
Granato D, Santos JS, Escher GB, Ferreira BL, Maggio RM (2018) Use of principal component analysis (PCA) and hierarchical cluster analysis (HCA) for multivariate association between bioactive compounds and functional properties in foods: a critical perspective. Trends Food Sci Technol 72:83–90. https://doi.org/10.1016/j.tifs.2017.12.006
Gu WW, Zhao YY, Li Q, Li Y (2018) Environmentally friendly polychlorinated naphthalenes (PCNs) derivatives designed using 3D-QSAR and screened using molecular docking, density functional theory and health-based risk assessment. J Hazard Mater 363:316–327. https://doi.org/10.1016/j.jhazmat.2018.09.060
Hussain J, Adams D, Allgar V, Campbell C (2014) Triggers in advanced neurological conditions: prediction and management of the terminal phase. BMJ Support Palliat Care 4:30–37. https://doi.org/10.1136/bmjspcare-2012-000389
Isobe T, Okuhata H, Miyasaka H, Jeon BS, Park HD (2013) Detoxification of microcystin-LR in water by Portulaca oleracea CV. J Biosci Bioeng 117:330–332. https://doi.org/10.1016/j.jbiosc.2013.08.003
Jochimsen EM, Carmichael WW, An JS, Cardo DM, Cookson ST, Holmes CE, Antunes MB, de Melo FDA, Lyra TM, Barreto VS, Azevedo SM, Jarvis WR (1998) Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. New Engl J Med 338:873–878. https://doi.org/10.1056/NEJM199803263381304
Johnson ER, Keinan S, Morisánchez P, Contreras-García J, Cohen AJ, Yang W (2010) Revealing noncovalent interactions. J Am Chem Soc 132:6498–6506. https://doi.org/10.1021/ja100936w
Julien O, Macabiau C, Cannon M, Lachapelle G (2007) ASPeCT: unambiguous sine-BOC(n,n) acquisition/tracking technique for navigation applications. IEEE Trans Aerosp Electron Syst 43:150–162. https://doi.org/10.1109/TAES.2007.357123
Jiang MN, Zhou XP, Sun DR, Gao H, Zheng QC, Zhang HX, Liang D (2017) 2D-QSAR study, molecular docking and molecular dynamics simulation studies of interaction mechanism between inhibitors and transforming growth factor-beta receptorI (ALK5). J Biomol Struct Dyn 36:3705–3717. https://doi.org/10.1080/07391102.2017.1396256
Kivaisi AK (2001) The potential for constructed wetlands for wastewater treatment and reuse in developing countries: a review. Ecol Eng 16:545–560. https://doi.org/10.1016/S0925-8574(00)00113-0
Kemper N (2008) Veterinary antibiotics in the aquatic and terrestrial environment. Ecol Indic 8:1–13. https://doi.org/10.1016/j.ecolind.2007.06.002
Kumar SN, Hasan SS, Kumar J, Hasan SS, Kumar J, Raj I, Pathan AA, Parmar A, Shakil S, Gourinath S, Madamwar D (2014) Crystal structure and interaction of phycocyanin with β-secretase: a putative therapy for Alzheimer’s disease. CNS Neurol Disord-Dr 13:691–698. https://doi.org/10.2174/1871527313666140228114456
Lu T, Chen FW (2012a) Multiwfn: a multifunctional wavefunction analyzer. J Comput Chem 33:580–592. https://doi.org/10.1002/jcc.22885
Lu T, Chen FW (2012b) Quantitative analysis of molecular surface based on improved Marching Tetrahedra algorithm. J Mol Graph Model 38:314–323. https://doi.org/10.1016/j.jmgm.2012.07.004
Lürling M, Eshetu F, Faassen EJ, Kosten S, Huszar VL (2013) Comparison of cyanobacterial and green algal growth rates at different temperatures. Freshw Biol 58:552–559. https://doi.org/10.1111/j.1365-2427.2012.02866.x
Lee ML, Kuei JC, Adams NW, Tarbet BJ, Nishioka M, Jones BA, Bradshaw JS (1984) Polarizable polysiloxane stationary phases for capillary column gas chromatography. J Chromatogr A 302:303–318. https://doi.org/10.1016/S0021-9673(01)89019-1
Liu BY, Liu WQ, Nie XP, Guan C, Yang YF, Wang ZH, Liao W (2011) Growth response and toxic effects of three antibiotics on Selenastrum capricornutum evaluated by photosynthetic rate and chlorophyll biosynthesis. J Environ Sci 23:1558–1563 CNKI:SUN:HJKB.0.2011-09-022
Liu CL, Marukawa K (2004) Global shape normalization for handwritten Chinese character recognition: a new method In Ninth International Workshop on Frontiers in Handwriting Recognition. IEEE 2004:300–305. https://doi.org/10.1109/IWFHR.2004.47
Liu SC, Sun SJ, Cui P, Ding YF (2019) Molecular modification of fluoroquinolone-biodegrading enzymes based on molecular docking and homology modelling. Int J Env Res Pub Health 16:3407–3439. https://doi.org/10.3390/ijerph16183407
Li Y, Lin Y, Garvey CJ, Birch D, Corkery RW, Loughlin PC, Scheer H, Willows RD, Chen M (2015) Characterization of red-shifted phycobilisomes isolated from the chlorophyll f-containing cyanobacterium Halomicronema hongdechloris. Biochim Biophys Acta 1857:107–114. https://doi.org/10.1016/j.bbabio.2015.10.009
Marx A, Adir N (2013) Allophycocyanin and phycocyanin crystal structures reveal facets of phycobilisome assembly. Biochim Biophys Acta 1827:311–318. https://doi.org/10.1016/j.bbabio.2012.11.006
Mullineaux CW (1992) Excitation energy transfer from phycobilisomes to photosystem I in a cyanobacterium. BBA-Protein Struct M 1100:285–292. https://doi.org/10.1016/0167-4838(92)90483-T
Ma J, Chen H, Qin S, Lin H (2015) Applications of natural and artificial phycobiliproteins in solar cells. Curr Biotec 4:275–281. https://doi.org/10.2174/2211550104666151016203528
Mazur-Marzec H, Toruńska A, Błońska MJ, Moskot M, Pliński M, Jakóbkiewicz-Banecka J, Wegrzyn G (2009) Biodegradation of nodularin and effects of the toxin on bacterial isolates from the Gulf of Gdańsk. Water Res 43:2801–2810. https://doi.org/10.1016/j.watres.2009.03.042
Martin NH, Jefford CW (2004) Self-sensitized photo oxygenation of 1-benzyl-3,4-dihydroisoquinolines. Helvetica Chimica Acta 64:2189–2192. https://doi.org/10.1002/hlca.19810640725
Perrow MR, Meijer ML, Dawidowicz P, Coops H (1997) Biomanipulation in shallow lakes: state of the art. Hydrobiologia 342:355–365 https://xs.scihub.ltd/10.1023/A:1017092802529
Poelman E, Pauw ND, Jeurissen B (1997) Potential of electrolytic flocculation for recovery of micro-algae. Resour Conserv Recycl 19:1–10. https://doi.org/10.1016/S0921-3449(96)01156-1
Pawlik-Skowrońska B, Toporowska M, Mazur-Marzec H (2019) Effects of secondary metabolites produced by different cyanobacterial populations on the freshwater zooplankters Brachionus calyciflorus and Daphnia pulex. Environ Sci Pollut Res 26:11793–11804. https://doi.org/10.1007/s11356-019-04543-1
Pavagadhi S, Tang AL, Sathishkumar M, Loh KP, Balasubramanian R (2013) Removal of microcystin-LR and microcystin-RR by graphene oxide: adsorption and kinetic experiments. Water Res 47:4621–4629. https://doi.org/10.1016/j.watres.2013.04.033
Pouria S, Andrade A, Barbosa J, Cavalcanti RL, Barreto VTS, Ward CJ, Preiser W, Poon GK, Neild GH, Codd GA (1998) Fatal microcystin intoxication in haemodialysis unit in Caruaru, Brazil. Lancet 253:21–26. https://doi.org/10.1016/s0140-6736(97)12285-1
Qu RJ, Li CG, Liu JQ, Xiao RY, Pan XX, Zeng XL, Wang ZY, Wu JC (2018) Hydroxyl radical based photocatalytic degradation of halogenated organic contaminants and paraffin on silica gel. Environ Sci Technol 52:7220–7229. https://doi.org/10.1021/acs.est.8b00499
Qu RJ, Li CG, Pan XX, Zeng XL, Liu JQ, Huang QG, Feng JF, Wang ZY (2017) Solid surface-mediated photochemical transformation of decabromodiphenyl ether (BDE-209) in aqueous solution. Water Res 125:114–122. https://doi.org/10.1016/j.watres.2017.08.033
Qu RJ, Liu JQ, Li CG, Wang LS, Wang ZY, Wu JC (2016) Experimental and theoretical insights into the photochemical decomposition of environmentally persistent perfluorocarboxylic acids. Water Res 104:34–43. https://doi.org/10.1016/j.watres.2016.07.071
Qiu YL, Li Y (2018) A theoretical method for the high-sensitivity fluorescence detection of PAEs through double-substitution modification. Environ Sci Pollut Res 25:34684–34692. https://doi.org/10.1007/s11356-018-3432-x
Quesada SP, Paschoal JAR, Reyes FGR (2013) Considerations on the aquaculture development and on the use of veterinary drugs: special issue for fluoroquinolones-a review. J Food Sci 78:R1321–R1333. https://doi.org/10.1111/1750-3841.12222
Robinson AA, Belden JB, Lydy MJ (2005) Toxicity of fluoroquinolone antibiotics to aquatic organisms. Environ Toxicol Chem 24:423–430. https://doi.org/10.1897/04-210r.1
Ritter S, Hiller RG, Wrench PM, Welte W, Diederichs K (1999) Crystal structure of a phycourobilin-containing phycoerythrin at 1.90-Å resolution. J Struct Biol 126:86–97. https://doi.org/10.1006/jsbi.1999.4106
Roth CM, Neal BL, Lenhoff AM (1996) Van der Waals interactions involving proteins. Biophys J 70:977–987. https://doi.org/10.1016/S0006-3495(96)79641-8
Rodier M, Borgne RL (2008) Population dynamics and environmental conditions affecting Trichodesmium spp. (filamentous cyanobacteria) blooms in the south-west lagoon of New Caledonia. J Exp Mar Biol Ecol 358:20–32. https://doi.org/10.1016/j.jembe.2008.01.016
Reuter W, Wiegand N, Huber R, Than ME (1999) Structural analysis at 2.2 Å of orthorhombic crystals presents the asymmetry of the allophycocyanin-linker complex, APLC7.8, from phycobilisomes of Mastigocladus laminosus. Proc Natl Acad Sci 96:1363–1368. https://doi.org/10.1073/pnas.96.4.1363
Ren ZX, Wang YW, Xu HH, Li YF, Han S (2019) Fuzzy comprehensive evaluation assistant 3D-QSAR of environmentally friendly FQs to reduce ADRs. Int J Env Res Public Health 16:3161–3180. https://doi.org/10.3390/ijerph16173161
Sandmann G, Boger P (1981) Inhibition of photosynthetic electron transport by amphotericin B. Physiol Plant 51:326–328. https://doi.org/10.1111/j.1399-3054.1981.tb04486.x
Schmidt GCM, Federspiel NA (1993) In vivo and in vitro footprinting of a light-regulated promoter in the cyanobacterium Fremyella diplosiphon. J Bacteriol 175:1806–1813. https://doi.org/10.1128/jb.175.6.1806-1813.1993
Soe KM, Yokoyama A, Yokoyama J, Hara Y (2011) Morphological and genetic diversity of the thermophilic cyanobacterium, Mastigocladus laminosus (Stigonematales, Cyanobacteria) from Japan and Myanmar. Phycol Res 59:135–142. https://doi.org/10.1111/j.1440-1835.2011.00611.x
Staahlberg J, Joensson B, Horvath C (1992) Combined effect of coulombic and van der Waals interactions in the chromatography of proteins. Anal Chem 64:3118–3124. https://doi.org/10.1021/ac00048a009
Shi JQ, Qu RJ, Feng MB, Wang XH, Wang LS, Yang SG, Wang ZY (2015) Oxidative degradation of decabromodiphenyl ether (BDE 209) by potassium permanganate: reaction pathways, kinetics, and mechanisms assisted by DFT calculations. Environ Sci Technol 49:4209–4217. https://doi.org/10.1021/es505111r
Schmidt M, Krasselt A, Reuter W (2006) Local protein flexibility as a prerequisite for reversible chromophore isomerization in α-phycoerythrocyanin. BBA-Proteo 1764:55–62. https://doi.org/10.1016/j.bbapap.2005.10.022
Schmidt M, Patel A, Zhao Y, Reuter W (2007) Structural basis for the photochemistry of alfa-phycoerythrocyanin. Biochemistry 46:416–423. https://doi.org/10.1021/bi061844j
Topliss JG, Edwards RP (1979) Chance factors in studies of quantitative structure-activity relationships. J Med Chem 22:1238–1244. https://doi.org/10.1021/jm00196a017
Valverde JR (2001) Molecular modelling: principles and applications. Brief Bioinform 2:199–200. https://doi.org/10.1093/bib/2.2.199
Ueno Y, Nagata S, Tsutsumi T, Hasegawa A, Watanabe MF, Park HD, Chen GC, Chen G, Yi SZ (1996) Detection of microcystins, a blue-green algal hepatotoxin in drinking water sampled in Haimen and Fusui, endemic areas of primary liver cancer in China, by highly sensitive immunoassay. Carcinogenesis 17:1317–1321. https://doi.org/10.1093/carcin/17.6.1317
Wang L, Li QY, Ben W (2017) An insight into the removal of fluoroquinolones in activated sludge process: sorption and biodegradation characteristics. J Environ Sci 56:263–271. https://doi.org/10.1016/j.jes.2016.10.006
Wang XQ, Li LN, Chang WR, Zhang JP, Gui LL, Guo BJ, Liang DC (2001) Structure of C-phycocyanin from Spirulina platensis at 2.2 A resolution: a novel monoclinic crystal form for phycobiliproteins in phycobilisomes. Acta Crystallogr D Biol Crystallogr 57:784–792. https://doi.org/10.1107/s0907444901004528
Wise R (2002) Antimicrobial resistance: priorities for action. J Antimicrob Chemother 49:585–586. https://doi.org/10.1093/jac/49.4.585
Wu ZX, Gan NQ, Huang Q, Song LR (2007) Response of Microcystis to copper stress: do phenotypes of Microcystis make a difference in stress tolerance? Environ Pollut 147:324–330. https://doi.org/10.1016/j.envpol.2006.05.022
Wetzstein HG, Schmeer N, Karl W (1997) Degradation of the fluoroquinolone enrofloxacin by the brown rot fungus Gloeophyllum striatum: identification of metabolites. Appl Environ Microbiol 63:4272–4281. https://doi.org/10.1002/pad.467
Wang D, Zhao CF, Chen S, Sun XP (2010) A composite fitting algorithm based on Sine function and a polynomial. 2010 3rd International Congress on Image and Signal Processing. IEEE 7:3116–3119. https://doi.org/10.1109/CISP.2010.5648122
Xiao R, Noerpel M, Luk LH, Wei ZS, Spinney R (2014) Thermodynamic and kinetic study of ibuprofen with hydroxyl radical: a density functional theory approach. Int J Quantum Chem 114:74–83. https://doi.org/10.1002/qua.24518
Xie Y, Zhang J, Yin S, Loo JA (2006) Top-down ESI-ECD-FT-ICR mass spectrometry localizes noncovalent protein-ligand binding sites. J Am Chem Soc 128:14432–14433. https://doi.org/10.1021/ja063197p
Yang LZ, Liu M (2019) 3D-QSAR model of polybrominated biphenyls tri-activity modified by standard deviation standardization method and its application in environmental friendly molecular modification. Chem J Chin Univ 40:2471–2479. (In Chinese). https://doi.org/10.7503/cjcu20190402
Zhao XH, Chu ZH, Li Y (2018) Molecular design of lower photodegradation fluoroquinolone antibiotics and their photolysis paths inference. Chem J Chineses Universities-Chinese 39:2707–2718. (In Chinese). https://doi.org/10.7503/cjcu20180475
Zhong F, Gao YN, Yu T, Xu D, Xiao E, He F, Zhou Q, Wu Z (2011) The management of undesirable cyanobacteria blooms in channel catfish ponds using a constructed wetland: contribution to the control of off-flavor occurrences. Water Res 45:6479–6488. https://doi.org/10.1016/j.watres.2011.09.044
Zong Z, Ma L, Yu L, Zhang D, Yang Z, Chen S (2015) Characterization of the interactions between polyethylene glycol and cellulase during the hydrolysis of lignocellulose. Bioenerg Res 8:270–278. https://doi.org/10.1007/s12155-014-9516-7
Zou S, Xu W, Zhang R, Tang J, Chen Y, Zhang G (2011) Occurrence and distribution of antibiotics in coastal water of the Bohai Bay, China: impacts of river discharge and aquaculture activities. Environ Pollut 159:2913–2920. https://doi.org/10.1016/j.envpol.2011.04.037
Zhao XH, Wang XL, Li Y (2019a) Combined HQSAR method and molecular docking study on genotoxicity mechanism of quinolones with higher genotoxicity. Environ Sci Pollut Res 26:34830–34853. https://doi.org/10.1007/s11356-019-06482-3
Zhang XN, Wang YJ, Sun S, Hou L, Wu P, Wu ZL, Zheng Q (2018) A tough and stiff hydrogel with tunable water content and mechanical properties based on the synergistic effect of hydrogen bonding and hydrophobic interaction. Macromolecules 51:8136–8146. https://doi.org/10.1021/acs.macromol.8b01496
Zhao XH, Zhao YY, Ren ZX, Yu L (2019b) Combined QSAR/QSPR and molecular docking study on fluoroquinolones to reduce biological enrichment. Comput Biol Chem 79:177–184. https://doi.org/10.1016/j.compbiolchem.2019.02.008
Acknowledgments
We thank Wordvice company (https://wordvice.cn/) for English language editing.
Author information
Authors and Affiliations
Contributions
Minghao Li: Conceptualization, data curation, software, and writing (original draft). Meijin Du: Investigation, methodology. Ruihao Sun: writing (review and editing) and investigation. Wenhui Zhang: Investigation. Yilin Hou: Investigation. Yu Li: Methodology and writing (review and editing).
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Responsible Editor: Vitor Manuel Oliveira Vasconcelos
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 33 kb)
Rights and permissions
About this article
Cite this article
Li, M., Du, M., Sun, R. et al. Application of a 2D-QSAR with a sine normalization method for the biodegradation of fluoroquinolones to poison cyanobacteria. Environ Sci Pollut Res 28, 11302–11316 (2021). https://doi.org/10.1007/s11356-020-11366-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-11366-y