Abstract
Microplastics are frequently detected in wastewater treatment plants, but the knowledge of their effects on microalgal-bacterial granular sludge (MBGS) is still unknown. This study investigated the performance and adaptive response of MBGS exposed in municipal wastewater in the presence of polystyrene (PS) microplastic particles with different sizes (i.e., 100 nm, 5 μm, and 10 μm). Results indicated that the average removal efficiency of influent organics, ammonia, and phosphorus by MBGS process was stable at above 85%, showing insignificant difference between three sizes of microplastic particles. The community richness of MBGS was reduced by nano-sized (i.e., 100 nm) and micro-sized (i.e., 5 μm) PS microplastic particles, while the community diversity decreased in all types. Although filamentous cyanobacteria were broken by PS microplastic particles, the performance of MBGS process was insignificantly affected due to the stimulated extracellular polymeric substances, which could act as adaptive responses and protect MBGS from stress damage. This study proves that MBGS process can be operated in the presence of prevalent PS microplastic particles.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable.
References
APHA (2005) Standard methods for the examination of water and wastewater. APHA, Washington, DC
Buchan A, LeCleir GR, Gulvik CA, Gonzalez JM (2014) Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol 12:686–698. https://doi.org/10.1038/nrmicro3326
Bergami E, Pugnalini S, Vannuccini ML, Manfra L, Faleri C, Savorelli F, Dawson KA, Corsi I (2017) Long-term toxicity of surface-charged polystyrene nanoplastics to marine planktonic species Dunaliella tertiolecta and Artemia franciscana. Aquat Toxicol 189:159–169. https://doi.org/10.1016/j.aquatox.2017.06.008
Besseling E, Wang B, Lürling M, Koelmans A (2014) Nanoplastic Affects Growth of S. obliquus and reproduction of D. magna. Environ Sci Technol 48:12336–12343. https://doi.org/10.1021/es503001d
Cardeña R, Moreno G, Bakonyi P, Buitrón G (2017) Enhancement of methane production from various microalgae cultures via novel ozonation pretreatment. Chem Eng J 307:948–954. https://doi.org/10.1016/j.cej.2016.09.016
Carr SA, Liu J, Tesoro AG (2016) Transport and fate of microplastic particles in wastewater treatment plants. Water Res 91:174–182. https://doi.org/10.1016/j.watres.2016.01.002
Cunha C, Faria M, Nogueira N, Ferreira A, Cordeiro N (2019) Marine vs freshwater microalgae exopolymers as biosolutions to microplastics pollution. Environ Pollut 249:372–380. https://doi.org/10.1016/j.envpol.2019.03.046
Ding S, Zhang M, Song Y (2019) Exploring China’s carbon emissions peak for different carbon tax scenarios. Energy Policy 129:1245–1252. https://doi.org/10.1016/j.enpol.2019.03.037
Estahbanati S, Fahrenfeld NL (2016) Influence of wastewater treatment plant discharges on microplastic concentrations in surface water. Chemosphere 162:277–284. https://doi.org/10.1016/j.chemosphere.2016.07.083
Eckert EM, Cesare AD, Kettner MT, Arias-Andres M, Fontaneto D, Grossart H, Corno G (2018) Microplastics increase impact of treated wastewater on freshwater microbial community. Environ Pollut 234:495–502. https://doi.org/10.1016/j.envpol.2017.11.070
Fu S, Ding J, Zhang Y, Li Y, Zhu R, Yuan X, Zou H (2018) Exposure to polystyrene nanoplastic leads to inhibition of anaerobic digestion system. Sci Total Environ 625:64–70. https://doi.org/10.1016/j.scitotenv.2017.12.158
Gong M, Bassi A (2016) Carotenoids from microalgae: a review of recent developments. Biotechnol Adv 34:1396–1412. https://doi.org/10.1016/j.biotechadv.2016.10
Geyer R, Jambeck JR, Law KL (2017) Production, use, and fate of all plastics ever made. Sci Adv 3:e1700782. https://doi.org/10.1126/sciadv.1700782
González-Pleiter M, Pedrouzo-Rodríguez A, Verdú I, Leganés F, Marco E, Rosal R, Fernández-Piñas F (2021) Microplastics as vectors of the antibiotics azithromycin and clarithromycin: effects towards freshwater microalgae. Chemosphere 268:e128824. https://doi.org/10.1016/j.chemosphere.2020.128824
Hamidian AH, Ozumchelouei EJ, Feizi F, Wu C, Zhang Y, Yang M (2021) A review on the characteristics of microplastics in wastewater treatment plants: a source for toxic chemicals. J Clean Prod 295:126480. https://doi.org/10.1016/j.jclepro.2021.126480
Hu Y, Hao X, Loosdrecht M, Chen H (2017) Enrichment of highly settleable microalgal consortia in mixed cultures for effluent polishing and low-cost biomass production. Water Res 125:11–22. https://doi.org/10.1016/j.watres.2017.08.034
Herbert D, Phipps PJ, Strange RE (1971) Chapter III chemical analysis of microbial cells. Methods Microbiol 5:209–344. https://doi.org/10.1016/S0580-9517(08)70641-X
Huang W, Li B, Zhang C, Zhang Z, Lei Z, Lu B, Zhou B (2015) Effect of algae growth on aerobic granulation and nutrients removal from synthetic wastewater by using sequencing batch reactors. Bioresour Technol 179:187–192. https://doi.org/10.1016/j.biortech.2014.12.024
Hu Z, Qi Y, Zhao L, Chen G (2019) Interactions between microalgae and microorganisms for wastewater remediation and biofuel production. Waste Biomass Valoriz 10:3907–3919. https://doi.org/10.1007/s12649-018-0325-7
Ji B, Liu C (2022) CO2 improves the microalgal-bacterial granular sludge towards carbon-negative wastewater treatment. Water Res 208:e117865. https://doi.org/10.1016/j.watres.2021.117865
Ji B, Liang J, Ma Y, Zhu L (2019) Bacterial community and eutrophic index analysis of the East Lake. Environ Pollut 252:682–688. https://doi.org/10.1016/j.envpol.2019.05.138
Ji B, Zhang M, Wang L, Wang S, Liu Y (2020) Removal mechanisms of phosphorus in non-aerated microalgal-bacterial granular sludge process. Bioresour Technol 312:e123531. https://doi.org/10.1016/j.biortech.2020.123531
Ji B, Zhu L, Wang S, Liu Y (2021) Temperature-effect on the performance of non-aerated microalgal-bacterial granular sludge process in municipal wastewater treatment. J Environ Manag 282:e111955. https://doi.org/10.1016/j.jenvman.2021.111955
Li X, Liu Q, Yang Q, Guo L, Zeng G, Hu J, Zheng W (2009) Enhanced aerobic sludge granulation in sequencing batch reactor by Mg2+ augmentation. Bioresour Technol 100:64–67. https://doi.org/10.1016/j.biortech.2008.06.015
Liu L, Gao D, Zhang M, Fu Y (2010) Comparison of Ca2+ and Mg2+ enhancing aerobic granulation in SBR. J Hazard Mater 181:382–387. https://doi.org/10.1016/j.jhazmat.2010.05.021
Liu W, Zhang J, Liu H, Guo X, Zhang X, Yao X, Cao Z, Zhang T (2021) A review of the removal of microplastics in global wastewater treatment plants: characteristics and mechanisms. Environ Int 146:e106277. https://doi.org/10.1016/j.envint.2020.106277
Murphy F, Ewins C, Carbonnier F, Quinn B (2016) Wastewater treatment works (WwTW) as a source of microplastics in the aquatic environment. Environ Sci Technol 50:5800–5808. https://doi.org/10.1021/acs.est.5b05416
Mao Y, Ai H, Chen Y, Zhang Z, Zeng P, Kang L, Li W, Gu W, He Q, Li H (2018) Phytoplankton response to polystyrene microplastics: perspective from an entire growth period. Chemosphere 208:59–68. https://doi.org/10.1016/j.chemosphere.2018.05.170
Mandal SK, Singh RP, Patel V (2011) Isolation and characterization of exopolysaccharide secreted by a toxic dinoflagellate, Amphidinium carterae Hulburt 1957 and its probable role in harmful algal blooms (HABs). Environ Microbiol 62:518–527. https://doi.org/10.1007/s00248-011-9852-5
Pham DN, Clark L, Li M (2021) Microplastics as hubs enriching antibiotic-resistant bacteria and pathogens in municipal activated sludge. J Hazard Mater 2:e100014. https://doi.org/10.1016/j.hazl.2021.100014
Quijano G, Arcila JS, Buitron G (2017) Microalgal-bacterial aggregates: applications and perspectives for wastewater treatment. Biotechnol Adv 35:772–781. https://doi.org/10.1016/j.biotechadv.2017.07.003
Ramanan R, Kim B, Cho D, Oh H, Kim H (2016) Algae-bacteria interactions: evolution, ecology and emerging applications. Biotechnol Adv 34:14–29. https://doi.org/10.1016/j.biotechadv.2015.12.003
Raunkjær K, Hvitved-Jacobsen T, Nielsen PH (1994) Measurement of pools of protein, carbohydrate and lipid in domestic wastewater. Water Res 28:251–262. https://doi.org/10.1016/0043-1354(94)90261-5
Rani-Borges B, Moschini-Carlos V, Pompêo M (2021) Microplastics and freshwater microalgae: what do we know so far? Aquat Ecol 55:363–377. https://doi.org/10.1007/s10452-021-09834-9
Rochman CM (2018) Microplastics research–from sink to source. Science 360:28–29. https://doi.org/10.1126/science.aar7734
Sun J, Dai X, Wang Q, Loosdrecht M, Ni B (2019) Microplastics in wastewater treatment plants: detection, occurrence and removal. Water Res 152:21–37. https://doi.org/10.1016/j.watres.2018.12.050
Sjollema SB, Redondo- Hasselerharm P, Leslie HA, Kraak MHS, Vethaak AD (2016) Do plastic particles affect microalgal photosynthesis and growth? Aquatic Toxicol 170:259–261. https://doi.org/10.1016/j.aquatox.2015.12.002
Sun X, Chen B, Li Q, Liu N, Xia B, Zhu L, Qu K (2018) Toxicities of polystyrene nano-and microplastics toward marine bacterium Halomonas alkaliphila. Sci Total Environ 642:1378–1385. https://doi.org/10.1016/j.scitotenv.2018.06.141
Stauch-White K, Srinivasan VN, Kuo-Dahab WC, Park C, Butler CS (2017) The role of inorganic nitrogen in successful formation of granular biofilms for wastewater treatment that support cyanobacteria and bacteria. AMB Express 7:1–10. https://doi.org/10.1186/s13568-017-0444-8
Tunali M, Uzoefuna EN, Tunali MM, Yenigun O (2020) Effect of microplastics and microplastic-metal combinations on growth and chlorophyll a concentration of Chlorella vulgaris. Sci Total Environ 743:e140479. https://doi.org/10.1016/j.scitotenv.2020.140479
Tang J, Wu Y, Esquivel-Elizondo S, Sorensen SJ, Rittmann BE (2018) How microbial aggregates protect against nanoparticle toxicity. Trends Biotechnol 36:1171–1182. https://doi.org/10.1016/j.tibtech.2018.06.009
Wang S, Ji B, Zhang M, Ma Y, Gu J, Liu Y (2020) Defensive responses of microalgal-bacterial granules to tetracycline in municipal wastewater treatment. Bioresour Technol 312:e123605. https://doi.org/10.1016/j.biortech.2020.123605
Wang J, Lei Z, Tian C, Liu S, Wang Q, Shimizu K, Zhang Z, Adachi Y, Lee D (2021a) Ionic response of algal-bacterial granular sludge system during biological phosphorus removal from wastewater. Chemosphere 264:e128534. https://doi.org/10.1016/j.chemosphere.2020.128534
Wang S, Ji B, Cui B, Ma Y, Guo D, Liu Y (2021b) Cadmium-effect on performance and symbiotic relationship of microalgal-bacterial granules. J Clean Prod 282:e125383. https://doi.org/10.1016/j.jclepro.2020.125383
Wang S, Ji B, Zhang M, Gu J, Ma Y, Liu Y (2021c) Tetracycline-induced decoupling of symbiosis in microalgal-bacterial granular sludge. Environ Res 197:e111095. https://doi.org/10.1016/j.envres.2021.111095
Zhang W, Cao B, Wang D, Ma T, Xia H, Yu D (2016) Influence of wastewater sludge treatment using combined peroxyacetic acid oxidation and inorganic coagulants re-flocculation on characteristics of extracellular polymeric substances (EPS). Water Res 88:728–739. https://doi.org/10.1016/j.watres.2015.10.049
Zhang C, Chen X, Wang J, Tan L (2017) Toxic effects of microplastic on marine microalgae Skeletonema costatum: interactions between microplastic and algae. Environ Pollut 220:1282–1288. https://doi.org/10.1016/j.envpol.2016.11.005
Zhang B, Lens PNL, Shi W, Zhang R, Zhang Z, Guo Y, Bao X, Cui F (2018) Enhancement of aerobic granulation and nutrient removal by an algal–bacterial consortium in a lab-scale photobioreactor. Chem Eng J 334:2373–2382. https://doi.org/10.1016/j.cej.2017.11.151
Zhang Y, Dong X, Nuramkhaan M, Lei Z, Shimizu K, Zhang Z, Adachi Y, Lee D, Tay JH (2020) Rapid granulation of aerobic granular sludge: a mini review on operation strategies and comparative analysis. Bioresour Technol Rep 7:e100206. https://doi.org/10.1016/j.biteb.2019.100206
Zhang M, Ji B, Liu Y (2021) Microalgal-bacterial granular sludge process: a game changer of future municipal wastewater treatment? Sci Total Environ 752:e141957. https://doi.org/10.1016/j.scitotenv.2020.141957
Zhao D, Huang R, Zeng J, Yu Z, Liu P, Cheng S, Wu Q (2014) Pyrosequencing analysis of bacterial community and assembly in activated sludge samples from different geographic regions in China. Appl Microbiol Biotechnol 98:9119–9128. https://doi.org/10.1007/s00253-014-5920-3
Funding
This work was funded by the National Natural Science Foundation of China (51909082).
Author information
Authors and Affiliations
Contributions
Huan Hou: investigation, writing — original draft. Shulian Wang: supervision, writing — review and editing, funding acquisition. Bin Ji: methodology. Yu Zhang: data curation. Yafei Shi: formal analysis. Kewu Pi: validation.
Corresponding author
Ethics declarations
Ethical approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Robert Duran
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hou, H., Wang, S., Ji, B. et al. Adaptation responses of microalgal-bacterial granular sludge to polystyrene microplastic particles in municipal wastewater. Environ Sci Pollut Res 29, 59965–59973 (2022). https://doi.org/10.1007/s11356-022-20107-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-20107-2