

FOLLOWUS
1.College of Geography and Environment, Shandong Normal University, Jinan 250014, China
2.College of Chemistry and Chemical Engineering, Ocean University of China, Qingdao 266100, China
chensdcn@163.com
zy76031961@163.com
Received:28 October 2023,
Online First:05 February 2024,
Published:01 March 2025
Scan QR Code
ZHANG Ling,ZHOU Yuxin,ZHU Zixian,et al.Microbial community and dynamic changes of extracellular polymeric substances in relation to plastisphere of disposable surgical masks in natural aquatic environment[J].Journal of Oceanology and Limnology,2025,43(02):502-514.
ZHANG Ling,ZHOU Yuxin,ZHU Zixian,et al.Microbial community and dynamic changes of extracellular polymeric substances in relation to plastisphere of disposable surgical masks in natural aquatic environment[J].Journal of Oceanology and Limnology,2025,43(02):502-514. DOI: 10.1007/s00343-024-3229-3.
In the context of global COVID-19 epidemic preparedness
the extensive use of disposable surgical masks (DSM) may lead to its emergence as a main new source of microplastics in the environment. Nowadays
DSMs have become a non-negligible source of plastic waste in aquatic environment
however
less research has been done on DSM after biofilm colonization in freshwater environment. The study investigated the microbial community of DSM-associated biofilms by 16S rRNA gene sequencing. Analysis of the microbial community in the middle and inner/outer layers of the DSM showed that the middle layer was different from the remaining two layers and that potential pathogens were enriched only in the middle layer of the DSM. Herein
we focused on the middle layer and explored the characterization properties and extracellular polymeric substances (EPS) components changes during biofilm formation. The results showed that the EPS components varied with the biofilm incubation time. As the formation of biofilm
the protein (PN) and polysaccharide (PS) in EPS showed an overall increasing trend
and the growth of PS was well synchronized with PN. Three fluorescent components of EPS were determined by the three-dimensional excitation emission matrix (3D-EEM)
including humic acid-like
fulvic acid-like
and aromatic protein-like components. The percentage of fluorescent components varied with increasing biofilm development time and then stabilized. Fourier transform infrared spectroscopy (FTIR) characterization results elucidated the emergence of oxygen-containing functional groups during biofilm formation. Moreover
the hydrophilicity increased with biofilm development. In conclusion
the environmental behavior and ecological risks of DSM in aquatic environment deserve urgent attention in future studies.
Abdel-Hamid H M . 2005 . Effect of electron beam irradiation on polypropylene films-dielectric and FT-IR studies . Solid-State Electronics , 49 ( 7 ): 1163 - 1167 , https://doi.org/10.1016/j.sse.2005.03.025 https://doi.org/10.1016/j.sse.2005.03.025 .
Achar J C , Na J , Im H et al . 2021 . Role of extracellular polymeric substances in leaching and bioconcentration of benzophenone-3 from microplastic fragments . Journal of Hazardous Materials , 416 : 125832 , https://doi.org/10.1016/j.jhazmat.2021.125832 https://doi.org/10.1016/j.jhazmat.2021.125832 . https://do 10.1016/j.jhazmat.2021.125832 http://dx.doi.org/10.1016/j.jhazmat.2021.125832
Adeleye A S , Keller A A . 2016 . Interactions between algal extracellular polymeric substances and commercial TiO 2 nanoparticles in aqueous media . Environmental Science and Technology , 50 ( 22 ): 12258 - 12265 , https://doi.org/10.1021/acs.est.6b03684 https://doi.org/10.1021/acs.est.6b03684 .
Akarsu C , Madenli Ö , Deveci E Ü . 2021 . Characterization of littered face masks in the southeastern part of Turkey . Environmental Science and Pollution Research , 28 ( 34 ): 47517 - 47527 , https://doi.org/10.1007/s11356-021-14099-8 https://doi.org/10.1007/s11356-021-14099-8 .
Anastopoulos I , Pashalidis I . 2021 . Single-use surgical face masks, as a potential source of microplastics: do they act as pollutant carriers? Journal of Molecular Liquids , 326 : 115247 , https://doi.org/10.1016/j.molliq.2020.115247 https://doi.org/10.1016/j.molliq.2020.115247 .
Bradford M M . 1976 . A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding . Analytical Biochemistry , 72 ( 1-2 ): 248 - 254 , https://doi.org/10.1016/0003-2697(76)90527-3 https://doi.org/10.1016/0003-2697(76)90527-3 .
Brandon J , Goldstein M , Ohman M D . 2016 . Long-term aging and degradation of microplastic particles: comparing in situ oceanic and experimental weathering patterns . Marine Pollution Bulletin , 110 ( 1 ): 299 - 308 , https://doi.org/10.1016/j.marpolbul.2016.06.048 https://doi.org/10.1016/j.marpolbul.2016.06.048 .
Cao B , Shi L , Brown R N et al . 2011 . Extracellular polymeric substances from Shewanella sp. HRCR-1 biofilms: characterization by infrared spectroscopy and proteomics . Environmental Microbiology , 13 ( 4 ): 1018 - 1031 , https://doi.org/10.1111/j.1462-2920.2010.02407.x https://doi.org/10.1111/j.1462-2920.2010.02407.x .
Celik M , Nakano H , Uchida K et al . 2023 . Comparative evaluation of the carbonyl index of microplastics around the Japan coast . Marine Pollution Bulletin , 190 : 114818 , https://doi.org/10.1016/j.marpolbul.2023.114818 https://doi.org/10.1016/j.marpolbul.2023.114818 .
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 and Technology , 37 ( 24 ): 5701 - 5710 , https://doi.org/10.1021/es034354c https://doi.org/10.1021/es034354c .
Cheng J G , Wang P , Ghiglione J F et al . 2024 . Bacterial pathogens associated with the plastisphere of surgical face masks and their dispersion potential in the coastal marine environment . Journal of Hazardous Materials , 462 : 132741 , https://doi.org/10.1016/j.jhazmat.2023.132741 https://doi.org/10.1016/j.jhazmat.2023.132741 .
Dogsa I , Kriechbaum M , Stopar D et al . 2005 . Structure of bacterial extracellular polymeric substances at different pH values as determined by SAXS . Biophysical Journal , 89 ( 4 ): 2711 - 2720 , https://doi.org/10.1529/biophysj.105.061648 https://doi.org/10.1529/biophysj.105.061648 .
Dubois M , Gilles K A , Hamilton J K et al . 1956 . Colorimetric method for determination of sugars and related substances . Analytical Chemistry , 28 ( 3 ): 350 - 356 , https://doi.org/10.1021/ac60111a017 https://doi.org/10.1021/ac60111a017 .
Fang J , Zhang L , Sutton D et al . 2012 . Needleless melt-electrospinning of polypropylene nanofibres . Journal of Nanomaterials , 2012 : 382639 , https://doi.org/10.1155/2012/382639 https://doi.org/10.1155/2012/382639 . https://do 10.1155/2012/382639 http://dx.doi.org/10.1155/2012/382639
Feng L M , He L , Jiang S Q et al . 2020 . Investigating the composition and distribution of microplastics surface biofilms in coral areas . Chemosphere , 252 : 126565 , https://doi.org/10.1016/j.chemosphere.2020.126565 https://doi.org/10.1016/j.chemosphere.2020.126565 .
Flemming H C , Wingender J , Szewzyk U et al . 2016 . Biofilms: an emergent form of bacterial life . Nature Reviews Microbiology , 14 ( 9 ): 563 - 575 , https://doi.org/10.1038/nrmicro.2016.94 https://doi.org/10.1038/nrmicro.2016.94 .
Flemming H C , Wuertz S . 2019 . Bacteria and archaea on Earth and their abundance in biofilms . Nature Reviews Microbiology , 17 ( 4 ): 247 - 260 , https://doi.org/10.1038/s41579-019-0158-9 https://doi.org/10.1038/s41579-019-0158-9 .
Gereffi G . 2020 . What does the COVID-19 pandemic teach us about global value chains? The case of medical supplies . Journal of International Business Policy , 3 ( 3 ): 287 - 301 , https://doi.org/10.1057/s42214-020-00062-w https://doi.org/10.1057/s42214-020-00062-w . https://do 10.1057/s42214-020-00062-w http://dx.doi.org/10.1057/s42214-020-00062-w
Haque M S , Uddin S , Sayem S M et al . 2021 . Coronavirus disease 2019 (COVID-19) induced waste scenario: a short overview . Journal of Environmental Chemical Engineering , 9 ( 1 ): 104660 , https://doi.org/10.1016/j.jece.2020.104660 https://doi.org/10.1016/j.jece.2020.104660 .
Hong P N , Honda R , Noguchi M et al . 2017 . Optimum selection of extraction methods of extracellular polymeric substances in activated sludge for effective extraction of the target components . Biochemical Engineering Journal , 127 : 136 - 146 , https://doi.org/10.1016/j.bej.2017.08.002 https://doi.org/10.1016/j.bej.2017.08.002 .
Huguet A , Vacher L , Relexans S et al . 2009 . Properties of fluorescent dissolved organic matter in the Gironde Estuary . Organic Geochemistry , 40 ( 6 ): 706 - 719 , https://doi.org/10.1016/j.orggeochem.2009.03.002 https://doi.org/10.1016/j.orggeochem.2009.03.002 .
Jain R , Jordan N , Weiss S et al . 2015 . Extracellular polymeric substances govern the surface charge of biogenic elemental selenium nanoparticles . Environmental Science and Technology , 49 ( 3 ): 1713 - 1720 , https://doi.org/10.1021/es5043063 https://doi.org/10.1021/es5043063 .
Jang A , Kim S M , Kim S Y et al . 2001 . Effect of heavy metals (Cu, Pb, and Ni) on the compositions of EPS in biofilms . Water Science and Technology , 43 ( 6 ): 41 - 48 , https://doi.org/10.2166/wst.2001.0336 https://doi.org/10.2166/wst.2001.0336 .
Jiao Y Q , Cody G D , Harding A K et al . 2010 . Characterization of extracellular polymeric substances from acidophilic microbial biofilms . Applied and Environmental Microbiology , 76 ( 9 ): 2916 - 2922 , https://doi.org/10.1128/aem.02289-09 https://doi.org/10.1128/aem.02289-09 .
Karygianni L , Ren Z , Koo H et al . 2020 . Biofilm matrixome: extracellular components in structured microbial communities . Trends in Microbiology , 28 ( 8 ): 668 - 681 , https://doi.org/10.1016/j.tim.2020.03.016 https://doi.org/10.1016/j.tim.2020.03.016 .
Kim J , Kim T H , Park S R et al . 2020 . Factors controlling the distributions of dissolved organic matter in the East China Sea during summer . Scientific Reports , 10 ( 1 ): 11854 , https://doi.org/10.1038/s41598-020-68863-w https://doi.org/10.1038/s41598-020-68863-w .
Kvale K , Prowe A E F , Chien C T et al . 2020 . The global biological microplastic particle sink . Scientific Reports , 10 ( 1 ): 16670 , https://doi.org/10.1038/s41598-020-72898-4 https://doi.org/10.1038/s41598-020-72898-4 .
LaFrentz B R , Králová S , Burbick C R et al . 2022 . The fish pathogen Flavobacterium columnare represents four distinct species: Flavobacterium columnare , Flavobacterium covae sp. nov., Flavobacterium davisii sp. nov. and Flavobacterium oreochromis sp. nov., and emended description of Flavobacterium columnare . Systematic and Applied Microbiology , 45 ( 2 ): 126293 , https://doi.org/10.1016/j.syapm.2021.126293 https://doi.org/10.1016/j.syapm.2021.126293 .
Laspidou C S , Rittmann B E . 2002 . A unified theory for extracellular polymeric substances, soluble microbial products, and active and inert biomass . Water Research , 36 ( 11 ): 2711 - 2720 , https://doi.org/10.1016/s0043-1354(01)00413-4 https://doi.org/10.1016/s0043-1354(01)00413-4 . https://do 10.1016/s0043-1354(01)00413-4 http://dx.doi.org/10.1016/s0043-1354(01)00413-4
Li G F , Ma W J , Ren Z Q et al . 2021 . Molecular insight into the binding property and mechanism of sulfamethoxazole to extracellular proteins of anammox sludge . Environmental Science and Technology , 55 ( 24 ): 16627 - 16635 , https://doi.org/10.1021/acs.est.1c05203 https://doi.org/10.1021/acs.est.1c05203 .
Li J L , Zhang T L , Shan X L et al . 2023 . Abandoned disposable masks become hot substrates for plastisphere, whether in soil, atmosphere or water . Journal of Hazardous Materials , 452 : 131321 , https://doi.org/10.1016/j.jhazmat.2023.131321 https://doi.org/10.1016/j.jhazmat.2023.131321 .
Liang H , Ji Y , Ge W et al . 2022 . Release kinetics of microplastics from disposable face masks into the aqueous environment . Science of the Total Environment , 816 : 151650 , https://doi.org/10.1016/j.scitotenv.2021.151650 https://doi.org/10.1016/j.scitotenv.2021.151650 .
Lin L J , Yuan B , Hong H L et al . 2022 . Post COVID-19 pandemic: disposable face masks as a potential vector of antibiotics in freshwater and seawater . Science of the Total Environment , 820 : 153049 , https://doi.org/10.1016/j.scitotenv.2022.153049 https://doi.org/10.1016/j.scitotenv.2022.153049 .
Lindh E L , Bergenstråhle-Wohlert M , Terenzi C et al . 2016 . Non-exchanging hydroxyl groups on the surface of cellulose fibrils: the role of interaction with water . Carbohydrate Research , 434 : 136 - 142 , https://doi.org/10.1016/j.carres.2016.09.006 https://doi.org/10.1016/j.carres.2016.09.006 .
Liu Y J , Li Z H , He Y T et al . 2023 . Antibiotic resistomes in face-mask biofilm along an urban river: multiple drivers and co-occurrence with human opportunistic pathogens . Journal of Hazardous Materials , 455 : 131587 , https://doi.org/10.1016/j.jhazmat.2023.131587 https://doi.org/10.1016/j.jhazmat.2023.131587 .
Ma J , Chen F Y , Xu H et al . 2021 . Face masks as a source of nanoplastics and microplastics in the environment: quantification, characterization, and potential for bioaccumulation . Environmental Pollution , 288 : 117748 , https://doi.org/10.1016/j.envpol.2021.117748 https://doi.org/10.1016/j.envpol.2021.117748 .
Maqbool T , Cho J , Hur J . 2017 . Spectroscopic descriptors for dynamic changes of soluble microbial products from activated sludge at different biomass growth phases under prolonged starvation . Water Research , 123 : 751 - 760 , https://doi.org/10.1016/j.watres.2017.07.033 https://doi.org/10.1016/j.watres.2017.07.033 .
Maqbool T , Ly Q V , Asif M B et al . 2020 . Fate and role of fluorescence moieties in extracellular polymeric substances during biological wastewater treatment: a review . Science of the Total Environment , 718 : 137291 , https://doi.org/10.1016/j.scitotenv.2020.137291 https://doi.org/10.1016/j.scitotenv.2020.137291 .
Metcalf R , Oliver D M , Moresco V et al . 2022 . Quantifying the importance of plastic pollution for the dissemination of human pathogens: the challenges of choosing an appropriate 'control' material . Science of the Total Environment , 810 : 152292 , https://doi.org/10.1016/j.scitotenv.2021.152292 https://doi.org/10.1016/j.scitotenv.2021.152292 .
Metzger U , Lankes U , Fischpera K et al . 2009 . The concentration of polysaccharides and proteins in EPS of Pseudomonas putida and Aureobasidum pullulans as revealed by C-13 CPMAS NMR spectroscopy . Applied Microbiology and Biotechnology , 85 ( 1 ): 197 - 206 , https://doi.org/10.1007/s00253-009-2218-y https://doi.org/10.1007/s00253-009-2218-y .
Noda I . 2012 . Close-up view on the inner workings of two-dimensional correlation spectroscopy . Vibrational Spectroscopy , 60 : 146 - 153 , https://doi.org/10.1016/j.vibspec.2012.01.006 https://doi.org/10.1016/j.vibspec.2012.01.006 .
Pi J , Zhu G , Gong T et al . 2022 . Dissolved organic matter derived from aquatic plants in constructed wetlands: characteristics and disinfection byproducts formation . Journal of Environmental Chemical Engineering , 10 ( 3 ): 107991 , https://doi.org/10.1016/j.jece.2022.107991 https://doi.org/10.1016/j.jece.2022.107991 .
Pu Y , Zheng J , Chen F et al . 2018 . Preparation of polypropylene micro and nanofibers by electrostatic-assisted melt blown and their application . Polymers , 10 ( 9 ): 959 , https://doi.org/10.3390/polym10090959 https://doi.org/10.3390/polym10090959 .
Rummel C D , Jahnke A , Gorokhova E et al . 2017 . Impacts of biofilm formation on the fate and potential effects of microplastic in the aquatic environment . Environmental Science and Technology Letters , 4 ( 7 ): 258 - 267 , https://doi.org/10.1021/acs.estlett.7b00164 https://doi.org/10.1021/acs.estlett.7b00164 .
Schofield E J , Veeramani H , Sharp J O et al . 2008 . Structure of biogenic uraninite produced by Shewanella oneidensis strain MR-1 . Environmental Science and Technology , 42 ( 21 ): 7898 - 7904 , https://doi.org/10.1021/es800579g https://doi.org/10.1021/es800579g .
Shi L , Rosso K , Clarke T et al . 2012 . Molecular underpinnings of Fe(Ⅲ) oxide reduction by Shewanella oneidensis MR-1 . Frontiers in Microbiology , 3 : 50 , https://doi.org/10.3389/fmicb.2012.00050 https://doi.org/10.3389/fmicb.2012.00050 .
Stout L M , Dodova E N , Tyson J F et al . 2010 . Phytoprotective influence of bacteria on growth and cadmium accumulation in the aquatic plant Lemna minor . Water Research , 44 ( 17 ): 4970 - 4979 , https://doi.org/10.1016/j.watres.2010.07.073 https://doi.org/10.1016/j.watres.2010.07.073 .
Sutherland I W . 2001 . Biofilm exopolysaccharides: a strong and sticky framework . Microbiology , 147 : 3 - 9 , https://doi.org/10.1099/00221287-147-1-3 https://doi.org/10.1099/00221287-147-1-3 .
Wang S , Zhi L , Shan W et al . 2020a . Correlation of extracellular polymeric substances and microbial community structure in denitrification biofilm exposed to adverse conditions . Microbial Biotechnology , 13 ( 6 ): 1889 - 1903 , https://doi.org/10.1111/1751-7915.13633 https://doi.org/10.1111/1751-7915.13633 .
Wang Y , Wang X , Li Y et al . 2020b . Biofilm alters tetracycline and copper adsorption behaviors onto polyethylene microplastics . Chemical Engineering Journal , 392 : 123808 , https://doi.org/10.1016/j.cej.2019.123808 https://doi.org/10.1016/j.cej.2019.123808 .
Wang Z , Li K , Shen X et al . 2023 . Soil nitrogen substances and denitrifying communities regulate the anaerobic oxidation of methane in wetlands of Yellow River Delta, China . Science of the Total Environment , 857 : 159439 , https://doi.org/10.1016/j.scitotenv.2022.159439 https://doi.org/10.1016/j.scitotenv.2022.159439 .
Wu N , Zhang Y , Zhao Z et al . 2020 . Colonization characteristics of bacterial communities on microplastics compared with ambient environments (water and sediment) in Haihe Estuary . Science of The Total Environment , 708 : 134876 , https://doi.org/10.1016/j.scitotenv.2019.134876 https://doi.org/10.1016/j.scitotenv.2019.134876 .
Xu E G , Ren Z J . 2021 . Preventing masks from becoming the next plastic problem . Frontiers of Environmental Science and Engineering , 15 ( 6 ): 125 , https://doi.org/10.1007/s11783-021-1413-7 https://doi.org/10.1007/s11783-021-1413-7 .
Xu F , Sun R , Wang H et al . 2021 . Improving the outcomes from electroactive constructed wetlands by mixing wastewaters from different beverage-processing industries . Chemosphere , 283 : 131203 , https://doi.org/10.1016/j.chemosphere.2021.131203 https://doi.org/10.1016/j.chemosphere.2021.131203 .
Ye T , Yang A , Wang Y et al . 2022 . Changes of the physicochemical properties of extracellular polymeric substances (EPS) from Microcystis aeruginosa in response to microplastics . Environmental Pollution , 315 : 120354 , https://doi.org/10.1016/j.envpol.2022.120354 https://doi.org/10.1016/j.envpol.2022.120354 .
Yin Y , Sun J , Liu F et al . 2019 . Effect of nitrogen deficiency on the stability of aerobic granular sludge . Bioresource Technology , 275 : 307 - 313 , https://doi.org/10.1016/j.biortech.2018.12.069 https://doi.org/10.1016/j.biortech.2018.12.069 .
Zhang H , Jia Y , Khanal S K et al . 2018 . Understanding the role of extracellular polymeric substances on ciprofloxacin adsorption in aerobic sludge, anaerobic sludge, and sulfate-reducing bacteria sludge systems . Environmental Science and Technology , 52 ( 11 ): 6476 - 6486 , https://doi.org/10.1021/acs.est.8b00568 https://doi.org/10.1021/acs.est.8b00568 .
Zou J , Liu X , Zhang D et al . 2020 . Adsorption of three bivalent metals by four chemical distinct microplastics . Chemosphere , 248 : 126064 , https://doi.org/10.1016/j.chemosphere.2020.126064 https://doi.org/10.1016/j.chemosphere.2020.126064 .
0
Views
12
Downloads
0
CSCD
Publicity Resources
Related Articles
Related Author
Related Institution
京公网安备11010802024621