Temporal dynamics of bacterial biofilms and their relationship with heavy metals on expanded polystyrene microplastics

Qun XIE; Yan FENG; Xiangrong XU; Hengxiang LI; Lang LIN; Weiqiong YU; Guanghui ZHU; Nenghao ZHONG; Minhua WU; Kai ZHANG

doi:10.1007/s00343-024-3291-x

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Temporal dynamics of bacterial biofilms and their relationship with heavy metals on expanded polystyrene microplastics

Biofilm on micro- and nano-plastics | Updated：2025-03-21

- Temporal dynamics of bacterial biofilms and their relationship with heavy metals on expanded polystyrene microplastics
- Temporal dynamics of bacterial biofilms and their relationship with heavy metals on expanded polystyrene microplastics
- 海洋湖沼学报(英文) 2025年43卷第2期页码：528-544
- Affiliations：
  
  1.Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
  2.Analytical and Testing Center, Guangdong Ocean University, Zhanjiang 524088, China
  3.Sanya Institute of Ocean Eco-Environmental Engineering, Sanya 572000, China
  4.Marine Environmental Engineering Center, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
  5.College of Chemistry and Environmental Science, Guangdong Ocean University, Zhanjiang 524088, China
  6.School of Basic Medicine, Guangdong Medical University, Zhanjiang 524023, China
  7.National Observation and Research Station of Coastal Ecological Environments in Macao, Macao Environmental Research Institute, Macau University of Science and Technology, Macao SAR 999078, China
- Author bio：
  
  xuxr@scsio.ac.cn
- Funds：
  
  the Hainan Province Science and Technology Special Fund(ZDYF2022SHFZ317);the Guangdong Province Key Laboratory of Applied Marine Biology(2023B1212060047);the Program for Scientific Research Start-up Funds of Guangdong Ocean University(060302332301)
- DOI：10.1007/s00343-024-3291-x
  中图分类号：
- 收稿：2023-05-16，
  
  网络首发：2024-02-16，
  
  纸质出版：2025-03-01
- Accepted：
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Temporal dynamics of bacterial biofilms and their relationship with heavy metals on expanded polystyrene microplastics[J]. 海洋湖沼学报(英文), 2025,43(2):528-544.

XIE Qun,FENG Yan,XU Xiangrong,et al.Temporal dynamics of bacterial biofilms and their relationship with heavy metals on expanded polystyrene microplastics[J].Journal of Oceanology and Limnology,2025,43(02):528-544.
Temporal dynamics of bacterial biofilms and their relationship with heavy metals on expanded polystyrene microplastics[J]. 海洋湖沼学报(英文), 2025,43(2):528-544. DOI： 10.1007/s00343-024-3291-x.

XIE Qun,FENG Yan,XU Xiangrong,et al.Temporal dynamics of bacterial biofilms and their relationship with heavy metals on expanded polystyrene microplastics[J].Journal of Oceanology and Limnology,2025,43(02):528-544. DOI： 10.1007/s00343-024-3291-x.

摘要

Abstract

Expanded polystyrene (EPS) is a common type of microplastics (MPs) often found in coastal areas especially aquaculture areas. It is considered as an important site for microbial colonization and biofilm formation

as well as a carrier of pollutants like heavy metals. However

the dynamic changes of bacterial communities attached to EPS and their interaction with heavy metals are still poorly unknown. In this study

a one-year field exposure experiment was conducted at an aquaculture farm near Donghai Island

in Leizhou Bay

Zhanjiang

Guangdong

in South China Sea. The bacterial communities attached to EPS MPs were examined by 16S rDNA high-throughput sequencing

and the relationships between bacterial biofilms and heavy metals were explored. The results show that there were notable seasonal variations in the bacterial diversity of EPS MPs. Species biodiversity was the highest in summer and the lowest in winter. The greatest number of bacterial species and lowest level of uniformity were observed in the spring. The bacterial community structure changed with exposure time

and the most significant difference in the 12-month group (

0.05) was found. The dominant bacterial species attached to EPS MPs were mainly Proteobackteria and Firmicutes at the phylum level

and

Pseudomonas

and

Exiguobacterium

were dominant at the genus level. Furthermore

EPS MPs acted as transport carriers for potential pathogenic bacteria. High correlations were found between bacterial species and the total concentration of heavy metals on EPS MPs

as well as their speciation fractions. Different chemical speciation of heavy metals migrated and altered over seasons within biofilms

which would further exacerbate the ecological risks.

关键词

Keywords

references

Barnes D K . 2002 . Biodiversity: invasions by marine life on plastic debris . Nature , 416 : 808 - 809 , https://doi.org/10.1038/416808a https://doi.org/10.1038/416808a .

Bergan T . 1981 . Human-and animal-pathogenic members of the genus Pseudomonas . In: Starr M P ed . The Prokaryotes : a Handbook on Habitats, Isolation, and Identification of Bacteria. Springer, Berlin. p . 666 - 700 . https://do 10.1007/978-3-662-13187-9_59 http://dx.doi.org/10.1007/978-3-662-13187-9_59

Bhardwaj H , Gupta R , Tiwari A . 2013 . Communities of microbial enzymes associated with biodegradation of plastics . Journal of Polymers and the Environment , 21 : 575 - 579 , https://doi.org/10.1007/s10924-012-0456-z https://doi.org/10.1007/s10924-012-0456-z .

Chen F J , Lao Q B , Liu M Y et al . 2022 . Impact of intensive mariculture activities on microplastic pollution in a typical semi-enclosed bay: Zhanjiang Bay . Marine Pollution Bulletin , 176 : 113402 , https://doi.‍org/10.1016/j.marpolbul.2022.113402 https://doi.‍org/10.1016/j.marpolbul.2022.113402 . https://do 10.1016/j.marpolbul.2022.113402 http://dx.doi.org/10.1016/j.marpolbul.2022.113402

Chen Y D , Niu S P , Yu J H et al . 2023 . Microplastics and microorganisms in sediments from stormwater drain system . Science of the Total Environment , 889 : 164284 , https://doi.org/10.1016/j.scitotenv.2023.164284 https://doi.org/10.1016/j.scitotenv.2023.164284 .

Cho Y N , Shim W J , Jang M et al . 2019 . Abundance and characteristics of microplastics in market bivalves from South Korea . Environmental Pollution , 245 : 1107 - 1116 , https://doi.org/10.1016/j.envpol.2018.11.091 https://doi.org/10.1016/j.envpol.2018.11.091 .

Debroas D , Mone A , Ter Halle A . 2017 . Plastics in the North Atlantic garbage patch: a boat-microbe for hitchhikers and plastic degraders . Science of the Total Environment , 599 - 600 : 1222 - 1232 , https://doi.org/10.1016/j.citotenv.2017.05.059 https://doi.org/10.1016/j.citotenv.2017.05.059 .

Deng H , Fu Q Q , Li D Z et al . 2021 . Microplastic-associated biofilm in an intensive mariculture pond: temporal dynamics of microbial communities, extracellular polymeric substances and impacts on microplastics properties . Journal of Cleaner Production , 319 : 128774 , https://doi.‍org/10.1016/j.jclepro.2021.128774 https://doi.‍org/10.1016/j.jclepro.2021.128774 . https://do 10.1016/j.jclepro.2021.128774 http://dx.doi.org/10.1016/j.jclepro.2021.128774

Ding S L , Zhang Q J , Dong J et al . 2018 . Microbial community structure and its relationship to heavy metals in Shenzhen and Hong Kong mangrove sediments . Chinese Journal of Ecology , 37 : 3018 - 3030 , https://doi.org/10.13292/j.1000-4890.201810.009. https://doi.org/10.13292/j.1000-4890.201810.009. (in Chinese with English abstract)

Doughari H J , Ndakidemi P A , Human I S et al . 2011 . The ecology, biology and pathogenesis of Acinetobacter spp.: an overview . Microbes and Environments , 26 ( 2 ): 101 - 112 , https://doi.org/10.1264/jsme2.me10179 https://doi.org/10.1264/jsme2.me10179 .

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 .

Frere L , Maignien L , Chalopin M et al . 2018 . Microplastic bacterial communities in the Bay of Brest: influence of polymer type and size . Environmental Pollution , 242 : 614 - 625 , https://doi.‍o‍rg/10.1016/j.envpol.2018.07.023 https://doi.‍o‍rg/10.1016/j.envpol.2018.07.023 . https://do 10.1016/j.envpol.2018.07.023 http://dx.doi.org/10.1016/j.envpol.2018.07.023

Glaser J A . 2020 . The importance of biofilms to the fate and effects of microplastics . In: Dincer S ed. Bacterial Biofilms . Publish with IntechOpen, UK , https://doi.org/10.5772/intechopen.92816 https://doi.org/10.5772/intechopen.92816 .

Gong M , Yang G , Zhuang L et al . 2019 . Microbial biofilm formation and community structure on low-density polyethylene microparticles in lake water microcosms . Environmental Pollution , 252 : 94 - 102 , https://doi.org/10.1016/j.envpol.2019.05.090 https://doi.org/10.1016/j.envpol.2019.05.090 .

He S , Jia M , Xiang Y P et al . 2022 . Biofilm on microplastics in aqueous environment: Physicochemical properties and environmental implications . Journal of Hazardous Materials , 424 : 127286 , https://doi.org/10.1016/j.jhazmat.2021.127286 https://doi.org/10.1016/j.jhazmat.2021.127286 .

Hoellein T J , McCormick A R , Hittie J et al . 2017 . Longitudinal patterns of microplastic concentration and bacterial assemblages in surface and benthic habitats of an urban river . Freshwater Science , 36 ( 3 ): 491 - 507 , https://doi.‍org/10.1086/693012 https://doi.‍org/10.1086/693012 . https://do 10.1086/693012 http://dx.doi.org/10.1086/693012

Jiang P L , Zhao S Y , Zhu L X et al . 2018 . Microplastic-associated bacterial assemblages in the intertidal zone of the Yangtze Estuary . Science of the Total Environment , 624 : 48 - 54 , https://doi.org/10.1016/j.citotenv.2017.12.105 https://doi.org/10.1016/j.citotenv.2017.12.105 .

Johansen M P , Prentice E , Cresswell T et al . 2018 . Initial data on adsorption of Cs and Sr to the surfaces of microplastics with biofilm . Journal of Environmental Radioactivity , 190 - 191 : 130 - 133 , https://doi.org/10.1016/j.jenvrad.2018.05.001 https://doi.org/10.1016/j.jenvrad.2018.05.001 .

Keswani A , Oliver D M , Gutierrez T et al . 2016 . Microbial hitchhikers on marine plastic debris: human exposure risks at bathing waters and beach environments . Marine Environmental Research , 118 : 10 - 19 , https://doi.org/10.1016/j.marenvres.2016.04.006 https://doi.org/10.1016/j.marenvres.2016.04.006 .

Kirstein I V , Kirmizi S , Wichels A et al . 2016 . Dangerous hitchhikers? Evidence for potentially pathogenic Vibrio spp. on microplastic particles . Marine Environmental Research , 120 : 1 - 8 , https://doi.org/10.1016/j.marenvres.2016.07.004 https://doi.org/10.1016/j.marenvres.2016.07.004 .

Kurniawan A , Yamamoto T , Tsuchiya Y et al . 2012 . Analysis of the ion adsorption-desorption characteristics of biofilm matrices . Microbes and Environments , 27 ( 4 ): 399 - 406 , https://doi.org/10.1264/jsme2.ME11339 https://doi.org/10.1264/jsme2.ME11339 .

Lacerda A L , Taylor J D , d S Rodrigues L et al . 2022 . Floating plastics and their associated biota in the Western South Atlantic . Science of the Total Environment , 805 : 150186 , https://doi.org/10.1016/j.scitotenv.2021.150186 https://doi.org/10.1016/j.scitotenv.2021.150186 .

Li W J , Zhang Y , Wu N et al . 2019 . Colonization characteristics of bacterial communities on plastic debris influenced by environmental factors and polymer types in the Haihe Estuary of Bohai Bay, China . Environmental Science & Technology , 53 ( 18 ): 10763 - 10773 , https://doi.org/10.1021/acs.est.9b03659 https://doi.org/10.1021/acs.est.9b03659 .

Lobelle D , Cunliffe M . 2011 . Early microbial biofilm formation on marine plastic debris . Marine Pollution Bulletin , 62 ( 1 ): 197 - 200 , https://doi.org/10.1016/j.marpolbul.2010.10.013 https://doi.org/10.1016/j.marpolbul.2010.10.013 .

Long M , Moriceau B , Gallinari M et al . 2015 . Interactions between microplastics and phytoplankton aggregates: Impact on their respective fates . Marine Chemistry , 175 : 39 - 46 , https://doi.org/10.1016/j.marchem.2015.04.003 https://doi.org/10.1016/j.marchem.2015.04.003 .

Ma Y , Song W J , Zhao C X . 2018 . The complexation of extracellular polymeric substances from alga-bacteria biofilm with heavy metal contained in lead-zinc mine tailings . Chinese Research of Environmental Sciences , 31 ( 7 ): 1296 - 1302 , https://doi.org/10.13198/j.issn.1001-6929.2018.03.27. https://doi.org/10.13198/j.issn.1001-6929.2018.03.27. (in Chinese with English abstract)

Maaghloud H , Houssa R , Ouansafi S et al . 2020 . Ingestion of microplastics by pelagic fish from the Moroccan Central Atlantic coast . Environmental Pollution , 261 : 114194 , https://doi.org/10.1016/j.envpol.2020.114194 https://doi.org/10.1016/j.envpol.2020.114194 .

Mammo F K , Amoah I D , Gani K M et al . 2020 . Microplastics in the environment: Interactions with microbes and chemical contaminants . Science of the Total Environment , 743 ( 7 ): 140518 , https://doi.org/10.1016/j.scitotenv.2020.140518 https://doi.org/10.1016/j.scitotenv.2020.140518 .

McCormick A R , Hoellein T J , London M G et al . 2016 . Microplastic in surface waters of urban rivers: concentration, sources, and associated bacterial assemblages . Ecosphere , 7 : e01556 , https://doi.org/10.1002/cs2.1556 https://doi.org/10.1002/cs2.1556 .

Miao L , Wang P , Hou J et al . 2019 . Distinct community structure and microbial functions of biofilms colonizing microplastics . Science of the Total Environment , 650 : 2395 - 2402 , https://doi.org/10.1016/j.citotenv.2018.09.378 https://doi.org/10.1016/j.citotenv.2018.09.378 .

Oberbeckmann S , Labrenz M . 2020 . Marine microbial assemblages on microplastics : Diversity, adaptation, and role in degradation . In: Carlson C A, Giovannoni S J eds. Annual Review of Marine Science. p. 209 - 232 . https://do 10.1146/annurev-marine-010419-010633 http://dx.doi.org/10.1146/annurev-marine-010419-010633

Oberbeckmann S , Löder M , Labrenz M . 2015 . Marine microplastic-associated biofilms—a review . Environmental Chemistry , 12 ( 5 ): 551 - 562 , https://doi.org/10.1071/EN15069 https://doi.org/10.1071/EN15069 .

Oberbeckmann S , Wichels A , Wiltshire K H et al . 2011 . Occurrence of Vibrio parahaemolyticus and Vibrio alginolyticus in the German Bight over a seasonal cycle . Antonie Van Leeuwenhoek , 100 ( 2 ): 291 - 307 , https://doi.org/10.1007/s10482-011-9586-x https://doi.org/10.1007/s10482-011-9586-x .

Ogonowski M , Motiei A , Ininbergs K et al . 2018 . Evidence for selective bacterial community structuring on microplastics . Environmental Microbiology , 20 ( 8 ): 2796 - 2808 , https://doi.org/10.1111/1462-2920.14120 https://doi.org/10.1111/1462-2920.14120 .

Onrubia J , Djaoudi K , Borgogno F et al . 2021 . Quantification of microplastics in North-Western Mediterranean harbors: seasonality and biofilm-related metallic contaminants . Journal of Marine Science and Engineering , 9 ( 3 ): 337 , https://doi.org/10.3390/jmse9030337 https://doi.org/10.3390/jmse9030337 .

Peng D M , Zhang J B , Fan C P et al . 2024 . Effects of terrestrial input on heavy metals in Zhanjiang Bay, a typical subtropical bay in the South China Sea . Marine Pollution Bulletin , 199 : 116015 , https://doi.‍org/10.1016/j.marpolbul.2023.116015 https://doi.‍org/10.1016/j.marpolbul.2023.116015 . https://do 10.1016/j.marpolbul.2023.116015 http://dx.doi.org/10.1016/j.marpolbul.2023.116015

Qi K , Lu N , Zhang S et al . 2021 . Uptake of Pb(II) onto microplastic-associated biofilms in freshwater: adsorption and combined toxicity in comparison to natural solid substrates . Journal of Hazardous Materials , 411 ( 6 ): 125115 , https://doi.‍org/10.1016/j.jhazmat.2021.125115 https://doi.‍org/10.1016/j.jhazmat.2021.125115 . https://do 10.1016/j.jhazmat.2021.125115 http://dx.doi.org/10.1016/j.jhazmat.2021.125115

Richard H , Carpenter E J , Komada T et al . 2019 . Biofilm facilitates metal accumulation onto microplastics in estuarine waters . Science of the Total Environment , 683 : 600 - 608 , https://doi.‍org/10.1016/j.scitotenv.2019.04.331 https://doi.‍org/10.1016/j.scitotenv.2019.04.331 . https://do 10.1016/j.scitotenv.2019.04.331 http://dx.doi.org/10.1016/j.scitotenv.2019.04.331

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 & Technology Letters , 4 ( 7 ): 258 - 267 , https://doi.org/10.1021/acs.estlett.7b00164 https://doi.org/10.1021/acs.estlett.7b00164 .

Schneider A R , Gommeaux M , Duclercq J et al . 2017 . Response of bacterial communities to Pb smelter pollution in contrasting soils . Science of the Total Environment , 605 - 606 : 436 - 444 .

Shao Z Y , Wang Y , Zhang J et al . 2017 . The bacterial community structure associated with a copper-tolerant plant, Artemisia capillaries Thunb, and its influencing factors . Acta Ecologica Sinica , 37 : 7679 - 7688 , https://doi.org/10.5846/stxb201608261743. https://doi.org/10.5846/stxb201608261743. (in Chinese with English abstract)

Stabnikova O , Stabnikov V , Marinin A et al . 2022 . The role of microplastics biofilm in accumulation of trace metals in aquatic environments . World Journal of Microbiology & Biotechnology , 38 ( 7 ): ARTN 117 , https://doi.org/10.1007/s11274-022-03293-6 https://doi.org/10.1007/s11274-022-03293-6 .

Sun X M , Chen B J , Xia B et al . 2020 . Impact of mariculture-derived microplastics on bacterial biofilm formation and their potential threat to mariculture: a case in situ study on the Sungo Bay, China . Environmental Pollution , 262 : 114336 , https://doi.org/10.1016/j.envpol.2020.114336 https://doi.org/10.1016/j.envpol.2020.114336 .

Thompson R C , Olsen Y , Mitchell R P et al . 2004 . Lost at sea: where is all the plastic? Science , 304 : 838 , https://doi.org/10.1126/science.1094559 https://doi.org/10.1126/science.1094559 .

Vezzulli L , Previati M , Pruzzo C et al . 2010 . Vibrio infections triggering mass mortality events in a warming Mediterranean Sea . Environmental Microbiology , 12 ( 7 ): 2007 - 2019 , https://doi.org/10.1111/j.1462-2920.2010.02209.x https://doi.org/10.1111/j.1462-2920.2010.02209.x .

Wang Q J , Zhang Y , Zhang Y Y et al . 2022 . Effects of biofilm on metal adsorption behavior and microbial community of microplastics . Journal of Hazardous Materials , 424 : 127340 , https://doi.org/10.1016/j.jhazmat.2021.127340 https://doi.org/10.1016/j.jhazmat.2021.127340 .

Wu N , Zhang Y , Li W et al . 2020 . Co-effects of biofouling and inorganic matters increased the density of environmental microplastics in the sediments of Bohai Bay coast . Science of the Total Environment , 717 : 134431 . https://doi.org/10.1016/j.scitotenv.2019.134431 https://doi.org/10.1016/j.scitotenv.2019.134431 .

Xie Q , Li H X , Li Z L et al . 2022 . Accumulation, chemical speciation and ecological risks of heavy metals on expanded polystyrene microplastics in seawater . Gondwana Research , 108 : 181 - 192 , https://doi.org/10.1016/j.gr.2022.01.017 https://doi.org/10.1016/j.gr.2022.01.017 .

Xu N N , Wang W L , Xu K et al . 2022 . Cultivation of different seaweed species and seasonal changes cause divergence of the microbial community in coastal seawaters . Front Microbiol. , 13 : 988743 , https://doi.‍org/10.3389/fmicb.2022.988743 https://doi.‍org/10.3389/fmicb.2022.988743 . https://do 10.3389/fmicb.2022.988743 http://dx.doi.org/10.3389/fmicb.2022.988743

Xu X Y , Wang S , Gao F L et al . 2019 . Marine microplastic-associated bacterial community succession in response to geography, exposure time, and plastic type in China's coastal seawaters . Marine Pollution Bulletin , 145 : 278 - 286 , https://doi.org/10.1016/j.marpolbul.2019.05.036 https://doi.org/10.1016/j.marpolbul.2019.05.036 .

Yan M T , Chen X F , Chu W et al . 2023 . Microplastic pollution and enrichment of distinct microbiota in sediment of mangrove in Zhujiang River estuary, China . Journal of Oceanology and Limnology , 41 ( 1 ): 215 - 228 , https://doi.org/10.1007/s00343-021-1300-x https://doi.org/10.1007/s00343-021-1300-x .

Yang G , Gong M , Mai L et al . 2021 . Diversity and structure of microbial biofilms on microplastics in riverine waters of the Pearl River Delta, China . Chemosphere , 272 : 129870 , https://doi.org/10.1016/j.chemosphere.2021.129870 https://doi.org/10.1016/j.chemosphere.2021.129870 .

Zettler E R , Mincer T J , Amaral-Zettler L A . 2013 . Life in the 'Plastisphere': Microbial communities on plastic marine debris . Environmental Science & Technology , 47 : 7137 - 7146 , https://doi.org/10.1021/es401288x https://doi.org/10.1021/es401288x .

Zhang B , Yang X , Liu L et al . 2021 . Spatial and seasonal variations in biofilm formation on microplastics in coastal waters . Science of the Total Environment , 770 ( 1 ): 145303 , https://doi.org/10.1016/j.scitotenv.2021.145303 https://doi.org/10.1016/j.scitotenv.2021.145303 .

Zhang X H , He X X , Austin B . 2020 . Vibrio harveyi : a serious pathogen of fish and invertebrates in mariculture . Marine Life Science & Technology , 2 : 231 - 245 , https://doi.org/10.1007/s42995-020-00037-z https://doi.org/10.1007/s42995-020-00037-z .

Zhu C Y , Li D N , Sun Y X et al . 2019 . Plastic debris in marine birds from an island located in the South China Sea . Marine Pollution Bulletin , 149 : 110566 , https://doi.org/10.1016/j.marpolbul.2019.110566 https://doi.org/10.1016/j.marpolbul.2019.110566 .

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