Diversity and succession of microbial communities on typical microplastics in Xincun Bay, a long-term mariculture tropical lagoon

In this study, three polymer types of microplastics (MPs), polyethylene (PE), polystyrene (PS) and polypropylene (PP), were exposed for 60 days in Xincun Bay (Hainan, China), a long-term mariculture tropical lagoon. High-throughput sequencing and scanning electron microscopy (SEM) were used to investigate the succession of microbial community structure and function on MPs after 10, 30, and 60 days of exposure, respectively. The results showed that diversity indices for bacteria from MPs were higher than those for bacteria from seawater. Significant differences were observed in community structure and metabolic function between MPs and seawater. The microbial network structure on MPs was more complex and dispersed than that in seawater. No significant differences in bacterial community structure and metabolic function were observed among different types of MPs. The biofilm on PS was the thickest, and the network structure on PP was the most complex one. With increasing exposure time, the biofilm attached to the surface of MPs became thicker and microbial composition showed some differences. The analysis of potential degradation bacteria and pathogens with abundance above 0.01% showed that the abundance of several potential plastic biodegraders on MPs was higher than that in seawater, while no potential pathogen was found enriched on MPs.

References

Amaral-Zettler, L. A., Zettler, E. R., & Mincer, T. J. (2020). Ecology of the plastisphere. Nature Reviews Microbiology, 18(3), 139–151. https://doi.org/10.1038/s41579-019-0308-0 PMID:31937947
Arias-Andres, M., Kettner, M. T., Miki, T., & Grossart, H. P. (2018). Microplastics: New substrates for heterotrophic activity contribute to altering organic matter cycles in aquatic ecosystems. Science of the Total Environment, 635, 1152–1159. https://doi.org/10.1016/j.scitotenv.2018.04.199 PMID:29710570
Bowley, J., Baker-Austin, C., Porter, A., Hartnell, R., & Lewis, C. (2021). Oceanic hitchhikers - Assessing pathogen risks from marine microplastic. Trends in Microbiology, 29(2), 107–116. https://doi.org/10.1016/j.tim.2020.06.011 PMID:32800610
Chen, B., Fan, Y., Huang, W., Rayhan, A. B. M. S., Chen, K., & Cai, M. (2020). Observation of microplastics in mariculture water of Longjiao Bay, southeast China: Influence by human activities. Marine Pollution Bulletin, 160, 111655. https://doi.org/10.1016/j.marpolbul.2020.111655 PMID:33181934
Chen, M., Jin, M., Tao, P., Wang, Z., Xie, W., Yu, X., & Wang, K. (2018). Assessment of microplastics derived from mariculture in Xiangshan Bay, China. Environmental Pollution, 242(Part B), 1146–1156. https://doi.org/10.1016/j.envpol.2018.07.133 PMID:30099319
De Tender, C., Devriese, L. I., Haegeman, A., Maes, S., Vangeyte, J., Cattrijsse, A., Dawyndt, P., & Ruttink, T. (2017). Temporal dynamics of bacterial and fungal colonization on plastic debris in the North Sea. Environmental Science & Technology, 51(13), 7350–7360. https://doi.org/10.1021/acs.est.7b00697 PMID:28562015
Deng, Y., Jiang, Y. H., Yang, Y., He, Z., Luo, F., & Zhou, J. (2012). Molecular ecological network analyses. BMC Bioinformatics, 13, 113. https://doi.org/10.1186/1471-2105-13-113 PMID:22646978
Dudek, K. L., Cruz, B. N., Polidoro, B., & Neuer, S. (2020). Microbial colonization of microplastics in the Caribbean Sea. Limnology and Oceanography Letters, 5(1), 5–17. https://doi.org/10.1002/lol2.10141
Durham, B. P., Grote, J., Whittaker, K. A., Bender, S. J., Luo, H., Grim, S. L., Brown, J. M., Casey, J. R., Dron, A., Florez-Leiva, L., Krupke, A., Luria, C. M., Mine, A. H., Nigro, O. D., Pather, S., Talarmin, A., Wear, E. K., Weber, T. S., Wilson, J. M., . . . Rappé, M. S. (2014). Draft genome sequence of marine alphaproteobacterial strain HIMB11, the first cultivated representative of a unique lineage within the Roseobacter clade possessing an unusually small genome. Standards in Genomic Sciences, 9, 632–645. https://doi.org/10.4056/sigs.4998989 PMID:25197450
Fang, X., Li, X., Xiang, Y., Hao, C., Zhao, Y., & Zhang, Y. (2020). Cumulative impact of anthropogenic nutrient inputs on lagoon ecosystems — A case study of Xincun Lagoon, Hainan, China. Regional Studies in Marine Science, 35, 101213. https://doi.org/10.1016/j.rsma.2020.101213
FAO. (2020). The State of World Fisheries and Aquaculture 2020. Sustainability in action. Rome. https://doi.org/10.4060/ca9229en
Feng, L., He, L., Jiang, S., Chen, J., Zhou, C., Qian, Z. J., Hong, P., Sun, S., & Li, C. (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 PMID:32220722
Frère, L., Maignien, L., Chalopin, M., Huvet, A., Rinnert, E., Morrison, H., Kerninon, S., Cassone, A. L., Lambert, C., Reveillaud, J., & Paul-Pont, I. (2018). Microplastic bacterial communities in the Bay of Brest: Influence of polymer type and size. Environmental Pollution, 242(Part A), 614–625. https://doi.org/10.1016/j.envpol.2018.07.023 PMID:30014939
Graham, E. D., & Tully, B. J. (2021). Marine Dadabacteria exhibit genome streamlining and phototrophy-driven niche partitioning. The ISME Journal, 15(4), 1248–1256. https://doi.org/10.1038/s41396-020-00834-5 PMID:33230264
Harvey, B. P., Kerfahi, D., Jung, Y., Shin, J. H., Adams, J. M., & Hall-Spencer, J. M. (2020). Ocean acidification alters bacterial communities on marine plastic debris. Marine Pollution Bulletin, 161(Part B), 111749. https://doi.org/10.1016/j.marpolbul.2020.111749 PMID:33160120
Hou, D., Hong, M., Wang, K., Yan, H., Wang, Y., Dong, P., Li, D., Liu, K., Zhou, Z., & Zhang, D. (2021). Prokaryotic community succession and assembly on different types of microplastics in a mariculture cage. Environmental Pollution, 268(Part A), 115756. https://doi.org/10.1016/j.envpol.2020.115756 PMID:33162209
Huang, Y., Xiao, X., Xu, C., Perianen, Y. D., Hu, J., & Holmer, M. (2020). Seagrass beds acting as a trap of microplastics - Emerging hotspot in the coastal region? Environmental Pollution, 257, 113450. https://doi.org/10.1016/j.envpol.2019.113450 PMID:31679874
Jiang, P., Zhao, S., Zhu, L., & Li, D. (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.scitotenv.2017.12.105 PMID:29247904
Li, W., Zhang, Y., Wu, N., Zhao, Z., Xu, W., Ma, Y., & Niu, Z. (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 PMID:31441645
Li, X. Y., Yu, R. C., Geng, H. X., & Li, Y. F. (2021). Increasing dominance of dinoflagellate red tides in the coastal waters of Yellow Sea, China. Marine Pollution Bulletin, 168, 112439. https://doi.org/10.1016/j.marpolbul.2021.112439 PMID:33993042
Lusher A., Hollman P. & Mendoza-Hill J. (2017) Microplastics in fisheries and aquaculture. FAO Fisheries and Aquaculture Technical Paper. Rome. DOI:dmd.105.006999 [pii]r10.1124/dmd.105.006999.
Meng, W., & Feagin, R. A. (2019). Mariculture is a double-edged sword in China. Estuarine, Coastal and Shelf Science, 222, 147–150. https://doi.org/10.1016/j.ecss.2019.04.018
Miao, L., Wang, P., Hou, J., Yao, Y., Liu, Z., Liu, S., & Li, T. (2019). Distinct community structure and microbial functions of biofilms colonizing microplastics. Science of the Total Environment, 650(Pt 2), 2395–2402. https://doi.org/10.1016/j.scitotenv.2018.09.378 PMID:30292995
Oberbeckmann, S., & Labrenz, M. (2020). Marine microbial assemblages on microplastics: Diversity, adaptation, and role in degradation. Annual Review of Marine Science, 12, 209–232. https://doi.org/10.1146/annurev-marine-010419-010633 PMID:31226027
Oberbeckmann, S., Löder, M. G. J., & Labrenz, M. (2015). Marine microplastic-associated biofilms – a review. Environmental Chemistry, 12(5), 551–562. https://doi.org/10.1071/EN15069
Oberbeckmann, S., Kreikemeyer, B., & Labrenz, M. (2018). Environmental factors support the formation of specific bacterial assemblages on microplastics. Frontiers in Microbiology, 8, 2709. https://doi.org/10.3389/fmicb.2017.02709 PMID:29403454
Olesen, J. M., Bascompte, J., Dupont, Y. L., & Jordano, P. (2007). The modularity of pollination networks. Proceedings of the National Academy of Sciences of the United States of America, 104(50), 19891–19896. https://doi.org/10.1073/pnas.0706375104 PMID:18056808
Rogers, K. L., Carreres‐Calabuig, J. A., Gorokhova, E., & Posth, N. R. (2020). Micro‐by‐micro interactions: How microorganisms influence the fate of marine microplastics. Limnology and Oceanography Letters, 5(1), 18–36. https://doi.org/10.1002/lol2.10136
Rosato, A., Barone, M., Negroni, A., Brigidi, P., Fava, F., Xu, P., Candela, M., & Zanaroli, G. (2020). Microbial colonization of different microplastic types and biotransformation of sorbed PCBs by a marine anaerobic bacterial community. Science of the Total Environment, 705, 135790. https://doi.org/10.1016/j.scitotenv.2019.135790 PMID:31972939
Shen, M., Zhu, Y., Zhang, Y., Zeng, G., Wen, X., Yi, H., Ye, S., Ren, X., & Song, B. (2019). Micro(nano)plastics: Unignorable vectors for organisms. Marine Pollution Bulletin, 139, 328–331. https://doi.org/10.1016/j.marpolbul.2019.01.004 PMID:30686434
Shi, R., Xu, S., Qi, Z., Zhu, Q., Huang, H., & Weber, F. (2019). Influence of suspended mariculture on vertical distribution profiles of bacteria in sediment from Daya Bay, Southern China. Marine Pollution Bulletin, 146, 816–826. https://doi.org/10.1016/j.marpolbul.2019.07.043 PMID:31426223
Spring, S., & Riedel, T. (2013). Mixotrophic growth of bacteriochlorophyll a-containing members of the OM60/NOR5 clade of marine gammaproteobacteria is carbon-starvation independent and correlates with the type of carbon source and oxygen availability. BMC Microbiology, 13, 117. https://doi.org/10.1186/1471-2180-13-117 PMID:23705861
Sui, Q., Zhang, L., Xia, B., Chen, B., Sun, X., Zhu, L., Wang, R., & Qu, K. (2020). Spatiotemporal distribution, source identification and inventory of microplastics in surface sediments from Sanggou Bay, China. Science of the Total Environment, 723, 138064. https://doi.org/10.1016/j.scitotenv.2020.138064 PMID:32392690
Sun, X., Chen, B., Xia, B., Li, Q., Zhu, L., Zhao, X., Gao, Y., & Qu, K. (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 PMID:32443196
Tu, C., Chen, T., Zhou, Q., Liu, Y., Wei, J., Waniek, J. J., & Luo, Y. (2020). Biofilm formation and its influences on the properties of microplastics as affected by exposure time and depth in the seawater. Science of the Total Environment, 734, 139237. https://doi.org/10.1016/j.scitotenv.2020.139237 PMID:32450399
Tu, C., Liu, Y., Li, L., Li, Y., Vogts, A., et al. (2021). Structural and Functional Characteristics of Microplastic Associated Biofilms in Response to Temporal Dynamics and Polymer Types. Bulletin of Environmental Contamination and Toxicology. https://doi.org/10.1007/s00128-021-03333-1.
Wang, J., Lu, J., Zhang, Y., Wu, J., Zhang, C., Yu, X., Zhang, Z., Liu, H., & Wang, W. (2018). High-throughput sequencing analysis of the microbial community in coastal intensive mariculture systems. Aquacultural Engineering, 83, 93–102. https://doi.org/10.1016/j.aquaeng.2018.10.001
Wang, J., Qin, X., Guo, J., Jia, W., Wang, Q., Zhang, M., & Huang, Y. (2020). Evidence of selective enrichment of bacterial assemblages and antibiotic resistant genes by microplastics in urban rivers. Water Research, 183, 116113. https://doi.org/10.1016/j.watres.2020.116113 PMID:32668354
Wang, L., Tong, J., Li, Y., Zhu, J., Zhang, W., Niu, L., & Zhang, H. (2021). Bacterial and fungal assemblages and functions associated with biofilms differ between diverse types of plastic debris in a freshwater system. Environmental Research, 196, 110371. https://doi.org/10.1016/j.envres.2020.110371 PMID:33130168
Wang, L., Luo, Z., Zhen, Z., Yan, Y., Yan, C., Ma, X., Sun, L., Wang, M., Zhou, X., & Hu, A. (2020). Bacterial community colonization on tire microplastics in typical urban water environments and associated impacting factors. Environmental Pollution, 265, 114922. https://doi.org/10.1016/j.envpol.2020.114922 PMID:32554087
Wen, B., Liu, J.-H., Zhang, Y., Zhang, H.-R., Gao, J.-Z., & Chen, Z. Z. (2020). Community structure and functional diversity of the plastisphere in aquaculture waters: Does plastic color matter? Science of the Total Environment, 740, 140082. https://doi.org/10.1016/j.scitotenv.2020.140082 PMID:32927571
Wright, R. J., Langille, M. G. I., & Walker, T. R. (2021). Food or just a free ride? A meta-analysis reveals the global diversity of the Plastisphere. The ISME Journal, 15(3), 789–806. https://doi.org/10.1038/s41396-020-00814-9 PMID:33139870
Wright, R. J., Erni-Cassola, G., Zadjelovic, V., Latva, M., & Christie-Oleza, J. A. (2020). Marine plastic debris: A new surface for microbial colonization. Environmental Science & Technology, 54(19), 11657–11672. https://doi.org/10.1021/acs.est.0c02305 PMID:32886491
Wu, X., Pan, J., Li, M., Li, Y., Bartlam, M., & Wang, Y. (2019). Selective enrichment of bacterial pathogens by microplastic biofilm. Water Research, 165, 114979. https://doi.org/10.1016/j.watres.2019.114979 PMID:31445309
Xue, N., Wang, L., Li, W., Wang, S., Pan, X., & Zhang, D. (2020). Increased inheritance of structure and function of bacterial communities and pathogen propagation in plastisphere along a river with increasing antibiotics pollution gradient. Environmental Pollution, 265, 114641. https://doi.org/10.1016/j.envpol.2020.114641 PMID:32505934
Yang, Y., Liu, W., Zhang, Z., Grossart, H. P., & Gadd, G. M. (2020). Microplastics provide new microbial niches in aquatic environments. Applied Microbiology and Biotechnology, 104(15), 6501–6511. https://doi.org/10.1007/s00253-020-10704-x PMID:32500269
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(13), 7137–7146. https://doi.org/10.1021/es401288x PMID:23745679
Zhang, Y., Lu, J., Wu, J., Wang, J., & Luo, Y. (2020). Potential risks of microplastics combined with superbugs: Enrichment of antibiotic resistant bacteria on the surface of microplastics in mariculture system. Ecotoxicology and Environmental Safety, 187, 109852. https://doi.org/10.1016/j.ecoenv.2019.109852 PMID:31670243
Zhao, D., Cao, X., Huang, R., Zeng, J., & Wu, Q. L. (2017). Variation of bacterial communities in water and sediments during the decomposition of Microcystis biomass. PLoS One, 12(4), e0176397. https://doi.org/10.1371/journal.pone.0176397 PMID:28437480
Zhou, J., Deng, Y., Luo, F., He, Z., Tu, Q., & Zhi, X. (2010). Functional molecular ecological networks. mBio, 1(4), e00169–e10. https://doi.org/10.1128/mBio.00169-10 PMID:20941329
Zhu, J., Zhang, Q., Li, Y., Tan, S., Kang, Z., Yu, X., Lan, W., Cai, L., Wang, J., & Shi, H. (2019). Microplastic pollution in the Maowei Sea, a typical mariculture bay of China. Science of the Total Environment, 658, 62–68. https://doi.org/10.1016/j.scitotenv.2018.12.192 PMID:30577027