

FOLLOWUS
1.School of Environment, Nanjing Normal University, Nanjing 210023, China
2.Department of Geological Sciences, University of Alabama, Tuscaloosa, AL 35487, USA
3.Key Laboratory of Integrated Regulation and Resource Development on Shallow Lakes of Ministry of Education; School of Environment, Hohai University, Nanjing 210098, China
4.Jiangsu Center for Collaborative Innovation in Geographical Information Resource Development and Application, Nanjing 210023, China
nilixiao@hhu.edu.cn
lishiyin@njnu.edu.cn
Received:13 September 2022,
Accepted:13 October 2022,
Online First:29 November 2022,
Published:01 November 2023
Scan QR Code
YIN Li,XU Ying,KONG Desheng,et al.Role of extracellular polymeric substances in resistance to allelochemical stress on Microcystis aeruginsosa and its mechanism[J].Journal of Oceanology and Limnology,2023,41(06):2219-2231.
Using allelochemicals to suppress cyanobacteria growth is a prospective method for its high efficiency and ecological safety. However
the suppression efficiency is affected inevit
ably by the extracellular polymeric substances (EPS) produced by cyanobacteria
and the knowledge about the roles of EPS in resistance to allelochemical stress is scarce. For the study
two typical anti-cyanobacterial allelochemicals were adopted to investigate the role of EPS in resistance to allelochemical stress on
Microcystis
aeruginosa
. Results show that EPS was crucial in alleviating the toxicity of allelochemicals to algae
especially in stabilizing the metabolism and photosynthetic activity of algal cells. The aggregation rate of algal cells increased with the increase of EPS secretion
which alleviated the stress of allelopathy. Tryptophan proteins and humic acids in EPS provided a binding site for allelochemicals
and the EPS-allelochemicals complex were formed by chemical bonding. This study improved our comprehension of the role of EPS in algal inhibition by allelochemicals.
Andreadakis A D . 1993 . Physical and chemical properties of activated sludge floc . Water Research , 27 ( 12 ): 1707 - 1714 , https://doi.org/10.1016/0043-1354(93)90107-S https://doi.org/10.1016/0043-1354(93)90107-S .
Badawy A M E , Luxton T P , Silva R G et al . 2010 . Impact of environmental conditions (pH, ionic strength, and electrolyte type) on the surface charge and aggregation of silver nanoparticles suspensions . Environmental Science and Technology , 44 ( 4 ): 1260 - 1266 , https://doi.org/10.1021/es902240k https://doi.org/10.1021/es902240k .
Baker A . 2001 . Fluorescence excitation-emission matrix characterization of some sewage-impacted rivers . Environmental Science & Technology , 35 ( 5 ): 948 - 953 , https://doi.org/10.1021/es000177t https://doi.org/10.1021/es000177t .
Chen B , Li F , Liu N et al . 2015 . Role of extracellular polymeric substances from Chlorella vulgaris in the removal of ammonium and orthophosphate under the stress of cadmium . Bioresource Technology , 190 : 299 - 306 , https://doi.org/10.1016/j.biortech.2015.04.080 https://doi.org/10.1016/j.biortech.2015.04.080 .
Chen H . 2012 . Determination of polysaccharide in extracellular polymeric substances by phenol-sulfuric acid method . Sichuan Environment , 31 ( 5 ): 1 - 3 , https://doi.org/10.14034/j.cnki.schj.2012.05.012. https://doi.org/10.14034/j.cnki.schj.2012.05.012. (in Chinese with English abstract)
Chen W , Westerhoff P , Leenheer J A et al . 2003 . Fluorescence excitation-emission matrix regional integration to quantify spectra for dissolved organic matter . Environmental Science & Technology , 37 ( 24 ): 5701 - 5710 , https://doi.org/10.1021/es034354c https://doi.org/10.1021/es034354c .
Eftink M R , Ghiron C A . 1981 . Fluorescence quenching studies with proteins . Analytical Biochemistry , 114 ( 2 ): 199 - 227 , https://doi.org/10.1016/0003-2697(81)90474-7 https://doi.org/10.1016/0003-2697(81)90474-7 .
Fan G D , Lin J H , Xia M Q et al . 2021 . Impact of extracellular polymeric substance in the inactivation of harmful algae by Ag 2 O/g-C 3 N 4 under visible light. Particle and Particle Systems Characterization , 38 ( 2 ): 2000272 , https://doi.org/10.1002/ppsc.202000272 https://doi.org/10.1002/ppsc.202000272 .
Frølund B , Griebe T , Nielsen P H . 1995 . Enzymatic-activity in the activated-sludge floc matrix . Applied Microbiology and Biotechnology , 43 ( 4 ): 755 - 761 , https://doi.org/10.1007/bf00164784 https://doi.org/10.1007/bf00164784 .
Frølund B , Palmgren R , Keiding K et al . 1996 . Extraction of extracellular polymers from activated sludge using a cation exchange resin . Water Research , 30 ( 8 ): 1749 - 1758 , https://doi.org/10.1016/0043-1354(95)00323-1 https://doi.org/10.1016/0043-1354(95)00323-1 .
Fu Q L , Zhang D Y , Mu S Y et al . 2012 . Interaction between chloramphenicol and the extracellular polymeric substances from cyanobacterium Synechocystis sp . Research of Environmental Sciences , 25 ( 1 ): 58 - 62 , https://doi.org/10.13198/j.res.2012.01.61.fuql.011 https://doi.org/10.13198/j.res.2012.01.61.fuql.011 .
Gao L , Pan X L , Zhang D Y et al . 2015 . Extracellular polymeric substances buffer against the biocidal effect of H 2 O 2 on the bloom-forming cyanobacterium Microcystis aeruginosa . Water Research , 69 : 51 - 58 , https://doi.org/10.1016/j.watres.2014.10.060 https://doi.org/10.1016/j.watres.2014.10.060 .
Gao Y N , Ge F J , Liu Z Y et al . 2015 . Comparative study on antialgal effects of allelochemicals from aquatic plants under different exposure protocols . Ecology and Environmental Sciences , 24 ( 4 ): 554 - 560 , https://doi.org/10.16258/j.cnki.1674-5906.2015.04.002 https://doi.org/10.16258/j.cnki.1674-5906.2015.04.002 .
Guo X N , Zhu A N , Chen R S . 2021 . China's algal bloom suffocates marine life . Science , 373 ( 6556 ): 751 - 751 , https://doi.org/10.1126/science.abl5774 https://doi.org/10.1126/science.abl5774 .
Hu Y J , Liu Y , Wang J B et al . 2004 . Study of the interaction between monoammonium glycyrrhizinate and bovine serum albumin . Journal of Pharmaceutical and Biomedical Analysis , 36 ( 4 ): 915 - 919 , https://doi.org/10.1016/j.jpba.2004.08.021 https://doi.org/10.1016/j.jpba.2004.08.021 .
Huang S Y , Yu H G , Dai C J et al . 2022a . Dynamic analysis of a modified algae and fish model with aggregation and Allee effect . Mathematical Biosciences and Engineering , 19 ( 4 ): 3673 - 3700 , https://doi.org/10.3934/mbe.2022169 https://doi.org/10.3934/mbe.2022169 .
Huang X H , Gu P , Wu H Q et al . 2022b . Shift of calcium-induced Microcystis aeruginosa colony formation mechanism: from cell adhesion to cell division . Environmental Pollution , 313 : 119997 , https://doi.org/10.1016/j.envpol.2022.119997 https://doi.org/10.1016/j.envpol.2022.119997 .
Kragh-Hansen U , Hellec F , De Foresta B et al . 2001 . Detergents as probes of hydrophobic binding cavities in serum albumin and other water-soluble proteins . Biophysical Journal , 80 ( 6 ): 2898 - 2911 , https://doi.org/10.1016/S0006-3495(01)76255-8 https://doi.org/10.1016/S0006-3495(01)76255-8 . https://do 10.1016/s0006-3495(01)76255-8 http://dx.doi.org/10.1016/s0006-3495(01)76255-8
Lakowicz J R , Weber G . 1973 . Quenching of fluorescence by oxygen. Probe for structural fluctuations in macromolecules . Biochemistry , 12 ( 21 ): 4161 - 4170 , https://doi.org/10.1021/bi00745a020 https://doi.org/10.1021/bi00745a020 . https://do 10.1021/bi00745a020 http://dx.doi.org/10.1021/bi00745a020
Li B H , Yin Y J , Kang L F et al . 2021a . A review: application of allelochemicals in water ecological restoration——algal inhibition . Chemosphere , 267 : 128869 , https://doi.org/10.1016/j.chemosphere.2020.128869 https://doi.org/10.1016/j.chemosphere.2020.128869 .
Li S , Tao Y , Zhan X M et al . 2020 . UV-C irradiation for harmful algal blooms control: A literature review on effectiveness, mechanisms, influencing factors and facilities . Science of the Total Environment , 723 : 137986 , https://doi.org/10.1016/j.scitotenv.2020.137986 https://doi.org/10.1016/j.scitotenv.2020.137986 .
Li X X , Yu H G , Dai C J et al . 2021b . Bifurcation analysis of a new aquatic ecological model with aggregation effect . Mathematics and Computers in Simulation , 190 : 75 - 96 , https://doi.org/10.1016/j.matcom.2021.05.015 https://doi.org/10.1016/j.matcom.2021.05.015 .
Liu S , Lin C , Diao X X et al . 2019 . Interactions between tetracycline and extracellular polymeric substances in anammox granular sludge . Bioresource Technology , 293 : 122069 , https://doi.org/10.1016/j.biortech.2019.122069 https://doi.org/10.1016/j.biortech.2019.122069 .
Liu X M , Sheng G P , Luo H Wet al . 2010 . Contribution of extracellular polymeric substances (EPS) to the sludge aggregation . Environmental Science & Technology , 44 ( 11 ): 4355 - 4360 , https://doi.org/10.1021/es9016766 https://doi.org/10.1021/es9016766 .
Liu Y , Fang H H P . 2003 . Influences of extracellular polymeric substances (EPS) on flocculation, settling, and dewatering of activated sludge . Critical Reviews in Environmental Science and Technology , 33 ( 3 ): 237 - 273 , https://doi.org/10.1080/10643380390814479 https://doi.org/10.1080/10643380390814479 .
Liu Y , Guo P Y , Lu B B et al . 2014 . Effects of new algaecide chitosan-gallate on growth of Microcystis flos - aquae and Chlorella pyrenoidosa . Journal of Central South University (Science and Technology) , 45 ( 7 ): 2538 - 2546 . (in Chinese with English abstract)
Lu Z Y , Sha J , Tian Y et al . 2017 . Polyphenolic allelochemical pyrogallic acid induces caspase-3(like)-dependent programmed cell death in the cyanobacterium Microcystis aeruginosa . Algal Research , 21 : 148 - 155 , https://doi.org/10.1016/j.algal.2016.11.007 https://doi.org/10.1016/j.algal.2016.11.007 .
Ni L X , Li D Y , Rong S Y et al . 2017 . Characterization of extracellular polymeric substance (EPS) fractions produced by Microcystis aeruginosa under the stress of linoleic acid sustained-release microspheres . Environmental Science and Pollution Research , 24 ( 26 ): 21091 - 21102 , https://doi.org/10.1007/s11356-017-9540-1 https://doi.org/10.1007/s11356-017-9540-1 .
Ni L X , Rong S Y , Gu G X et al . 2018 . Inhibitory effect and mechanism of linoleic acid sustained-release microspheres on Microcystis aeruginosa at different growth phases . Chemosphere , 212 : 654 - 661 , https://doi.org/10.1016/j.chemosphere.2018.08.045 https://doi.org/10.1016/j.chemosphere.2018.08.045 .
Paerl H W , Otten T G . 2013 . Blooms bite the hand that feeds them . Science , 342 ( 6157 ): 433 - 434 , https://doi.org/10.1126/science.1245276 https://doi.org/10.1126/science.1245276 .
Pal M , Yesankar P J , Dwivedi A et al . 2020 . Biotic control of harmful algal blooms (HABs): A brief review . Journal of Environmental Management , 268 : 110687 , https://doi.org/10.1016/j.jenvman.2020.110687 https://doi.org/10.1016/j.jenvman.2020.110687 .
Pan X L , Liu J , Zhang D Y . 2010 . Binding of phenanthrene to extracellular polymeric substances (EPS) from aerobic activated sludge: A fluorescence study . Colloids and Surfaces B : Biointerfaces , 80 ( 1 ): 103 - 106 , https://doi.org/10.1016/j.colsurfb.2010.05.002 https://doi.org/10.1016/j.colsurfb.2010.05.002 .
Sheng G P , Yu H Q , Li X Y . 2010 . Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: a review . Biotechnology Advances , 28 ( 6 ): 882 - 894 , https://doi.org/10.1016/j.biotechadv.2010.08.001 https://doi.org/10.1016/j.biotechadv.2010.08.001 . https://do 10.1016/j.biotechadv.2010.08.001 http://dx.doi.org/10.1016/j.biotechadv.2010.08.001
Stedmon C A , Bro R . 2008 . Characterizing dissolved organic matter fluorescence with parallel factor analysis: a tutorial . Limnology and Oceanography : Methods , 6 ( 11 ): 572 - 579 , https://doi.org/10.4319/lom.2008.6.572b https://doi.org/10.4319/lom.2008.6.572b .
Tan L R , Xia P F , Zeng R J et al . 2018 . Low-level concentrations of aminoglycoside antibiotics induce the aggregation of cyanobacteria . Environmental Science and Pollution Research , 25 ( 17 ): 17128 - 17136 , https://doi.org/10.1007/s11356-018-1894-5 https://doi.org/10.1007/s11356-018-1894-5 .
Ueshima M , Ginn B R , Haack E A et al . 2008 . Cd adsorption onto Pseudomonas putida in the presence and absence of extracellular polymeric substances . Geochimica et Cosmochimica Acta , 72 ( 24 ): 5885 - 5895 , https://doi.org/10.1016/j.gca.2008.09.014 https://doi.org/10.1016/j.gca.2008.09.014 . https://do 10.1016/j.gca.2008.09.014 http://dx.doi.org/10.1016/j.gca.2008.09.014
Wang S , Li Q , Huang S Z et al . 2021 . Single and combined effects of microplastics and lead on the freshwater algae Microcystis aeruginosa . Ecotoxicology and Environmental Safety , 208 : 111664 , https://doi.org/10.1016/j.ecoenv.2020.111664 https://doi.org/10.1016/j.ecoenv.2020.111664 .
Wang X Z , Han X Y , Ge H M . 2022 . Effect of light intensity on bound EPS characteristics of two Microcystis morphospecies: the role of bEPS in the proliferation of Microcystis . Journal of Oceanology and Limnology , 40 ( 5 ): 1706 - 1719 , https://doi.org/10.1007/s00343-022-1362-4 https://doi.org/10.1007/s00343-022-1362-4 .
Ware W R . 1962 . Oxygen quenching of fluorescence in solution: an experimental study of the diffusion process . The Journal of Physical Chemistry , 66 ( 3 ): 455 - 458 , https://doi.org/10.1021/j100809a020 https://doi.org/10.1021/j100809a020 .
Weber S J , Mishra D R , Wilde S B et al . 2020 . Risks for cyanobacterial harmful algal blooms due to land management and climate interactions . Science of the Total Environment , 703 : 134608 , https://doi.org/10.1016/j.scitotenv.2019.134608 https://doi.org/10.1016/j.scitotenv.2019.134608 .
Xia P F , Li Q , Tan L R et al . 2016 . Extracellular polymeric substances protect Escherichia coli from organic solvents . RSC Advances , 6 ( 64 ): 59438 - 59444 , https://doi.org/10.1039/c6ra11707d https://doi.org/10.1039/c6ra11707d .
Xie Q T , Liu N , Liu D H et al . 2020 The complexation with proteins in extracellular polymeric substances alleviates the toxicity of Cd (II) to Chlorella vulgaris . Environmental Pollution , 263 : 114102 , https://doi.org/10.1016/j.envpol.2020.114102 https://doi.org/10.1016/j.envpol.2020.114102 .
Xu H C , Cai H Y , Yu G H et al . 2013a . Insights into extracellular polymeric substances of cyanobacterium Microcystis aeruginosa using fractionation procedure and parallel factor analysis . Water Research , 47 ( 6 ): 2005 - 2014 , https://doi.org/10.1016/j.watres.2013.01.019 https://doi.org/10.1016/j.watres.2013.01.019 .
Xu H C , Jiang H L , Yu G H et al . 2014 . Towards understanding the role of extracellular polymeric substances in cyanobacterial Microcystis , aggregation and mucilaginous bloom formation . Chemosphere , 117 : 815 - 822 , https://doi.org/10.1016/j.chemosphere.2014.10.061 https://doi.org/10.1016/j.chemosphere.2014.10.061 .
Xu J , Sheng G P , Ma Y et al . 2013b . Roles of extracellular polymeric substances (EPS) in the migration and removal of sulfamethazine in activated sludge system . Water Research , 47 ( 14 ): 5298 - 5306 , https://doi.org/10.1016/j.watres.2013.06.009 https://doi.org/10.1016/j.watres.2013.06.009 .
Yan P , Xia J S , Chen Y P et al . 2017 . Thermodynamics of binding interactions between extracellular polymeric substances and heavy metals by isothermal titration microcalorimetry . Bioresource Technology , 232 : 354 - 363 , https://doi.org/10.1016/j.biortech.2017.02.067 https://doi.org/10.1016/j.biortech.2017.02.067 .
Yan Z R , Meng H S , Yang X Y et al . 2019a . Insights into the interactions between triclosan (TCS) and extracellular polymeric substance (EPS) of activated sludge . Journal of Environmental Management , 232 : 219 - 225 , https://doi.org/10.1016/j.jenvman.2018.11.059 https://doi.org/10.1016/j.jenvman.2018.11.059 .
Yan Z R , Zhu Y Y , Meng H S et al . 2019b . Insights into thermodynamic mechanisms driving bisphenol A (BPA) binding to extracellular polymeric substances (EPS) of activated sludge . Science of the Total Environment , 677 : 502 - 510 , https://doi.org/10.1016/j.scitotenv.2019.04.413 https://doi.org/10.1016/j.scitotenv.2019.04.413 .
Yang Y Y , Huang B Z , Tang Y Z et al . 2021 . Allelopathic effects of mixotrophic dinoflagellate Akashiwo sanguinea on co-occurring phytoplankton: the significance of nutritional ecology . Journal of Oceanology and Limnology , 39 ( 3 ): 903 - 917 , https://doi.org/10.1007/s00343-020-0132-4 https://doi.org/10.1007/s00343-020-0132-4 .
Yin L , Wang J , Shi K P et al . 2022 . Interactions between tannins allelochemicals and extracellular polymeric substance (EPS) of Microcystis aeruginosa . Environmental Science and Pollution Research , 29 ( 55 ): 83211 - 83219 , https://doi.org/10.1007/s11356-022-21661-5 https://doi.org/10.1007/s11356-022-21661-5 .
You G X , Hou J , Xu Y et al . 2015 . Effec ts of CeO 2 nanoparticles on production and physicochemical characteristics of extracellular polymeric substances in biofilms in sequencing batch biofilm reactor . Bioresource Technology , 194 : 91 - 98 , https://doi.org/10.1016/j.biortech.2015.07.006 https://doi.org/10.1016/j.biortech.2015.07.006 .
Zhang Y Z , Dai J , Zhang X P et al . 2008 . Studies of the interaction between Sudan I and bovine serum albumin by spectroscopic methods . Journal of Molecular Structure , 888 ( 1-3 ): 152 - 159 , https://doi.org/10.1016/j.molstruc.2007.11.043 https://doi.org/10.1016/j.molstruc.2007.11.043 .
Zhao J F , Liu S X , Liu N et al . 2019a . Accelerated productions and physicochemical characterizations of different extracellular polymeric substances from Chlorella vulgaris with nano-ZnO . Science of the Total Environment , 658 : 582 - 589 , https://doi.org/10.1016/j.scitotenv.2018.12.019 https://doi.org/10.1016/j.scitotenv.2018.12.019 .
Zhao M M , Chen X Y , Ma N et al . 2018 . Overvalued allelopathy and overlooked effects of humic acid-like substances on Microcystis aeruginosa and Scenedesmus obliquus competition . Harmful Algae , 78 : 18 - 26 , https://doi.org/10.1016/j.hal.2018.07.003 https://doi.org/10.1016/j.hal.2018.07.003 .
Zhao M M , Qu D , Shen W D et al . 2019b . Effects of dissolved organic matter from different sources on Microcystis aeruginosa growth and physiological characteristics . Ecotoxicology and Environmental Safety , 176 : 125 - 131 , https://doi.org/10.1016/j.ecoenv.2019.03.085 https://doi.org/10.1016/j.ecoenv.2019.03.085 .
Zhao R R , Chen G W . 2018 . Simulation of the effect of EPS on aggregation behavior of single-celled microalgae . Journal of Hefei University of Technology , 41 ( 11 ): 1531 - 1536 , https://doi.org/10.3969/j.issn.1003-5060.2018.11.018. https://doi.org/10.3969/j.issn.1003-5060.2018.11.018. (in Chinese with English abstract)
Zhu X Q , Dao G H , Tao Y et al . 2021a . A review on control of harmful algal blooms by plant-derived allelochemicals . Journal of Hazardous Materials , 401 : 123403 , https://doi.org/10.1016/j.jhazmat.2020.123403 https://doi.org/10.1016/j.jhazmat.2020.123403 .
Zhu Y X , Cheng J , Zhang Z et al . 2021b . Promoting extracellular polymeric substances to alleviate phenol toxicity in Arthrospira platensis at high carbon dioxide concentrations . Journal of Cleaner Production , 290 : 125167 , https://doi.org/10.1016/j.jclepro.2020.125167 https://doi.org/10.1016/j.jclepro.2020.125167 .
0
Views
0
Downloads
0
CSCD
Publicity Resources
Related Articles
Related Author
Related Institution
京公网安备11010802024621