Abstract
Bisphenol A (BPA) and 4-nonylphenol (NP) are ubiquitous pollutants with estrogenic activity in aquatic environment and have attracted global concern due to their disruption of endocrine systems. This study investigated the spatial distribution characteristics of the bacterial groups involved in the degradation of BPA and NP within biofilms in an urban river using terminal restriction fragment length polymorphism based on 16S rRNA gene sequences. The effects of the pollution level and water parameters on these groups were also assessed. Hierarchical cluster analysis grouped the sampling sites into three clusters reflecting their varying nutrient pollution levels of relatively slight pollution (SP), moderate pollution (MP), and high pollution (HP) based on water quality data and Environmental Quality Standard for Surface Water of China (GB3838-2002). The BPA and NP concentration in river water ranged from 0.8 to 77.5 and 10.2 to 162.9 ng L−1, respectively. Comamonadaceae, Pseudomonadaceae, Alcaligenaceae, Bacillaceae, Sphingomonadacea, Burkholderiaceae, and Rhizobiaceae were the dominant bacterial taxa involved in BPA and NP degradation, comprising an average of 9.8, 8.1, 7.6, 6.7, 6.2, 4.1, and 2.8 % of total sequences, respectively. The total abundance of these groups showed a slight upward trend and subsequently rapidly decreased with increasing pollution levels. The average proportion of Comamonadaceae in MP river sections was almost 1.5–2 times than that in SP or HP one. The distribution of functional groups was found related to environmental variables, especially pH, conductivity, ammonium nitrogen (NH3-N), and BPA. The abundance of Comamonadaceae and Rhizobiaceae was both closely related to higher values of pH and conductivity as well as lower concentrations of NP and BPA. Alcaligenaceae and Pseudomonadaceae were associated with higher concentrations of TP and CODMn and inversely correlated with DO concentration. This study might provide effective data on bacterial group changes in polluted urban rivers.
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References
Allan JD (1995) Stream ecology. Structure and function of running waters. Chapman & Hall, London, p 388
Anderson-Glenna MJ, Bakkestuen V, Clipson NJ (2008) Spatial and temporal variability in epilithic biofilm bacterial communities along an upland river gradient. FEMS Microbiol Ecol 64:407–418
Araya R, Tani K, Takagi T, Yamaguchi N, Nasu M (2003) Bacterial activity and community composition in stream water and biofilm from an urban river determined by fluorescent in situ hybridization and DGGE analysis. FEMS Microbiol Ecol 43:111–119
Brümmer IHM, Fehr W, Wagner-Döbler I (2000) Biofilm community structure in polluted rivers: abundance of dominant phylogenetic groups over a complete annual cycle. Appl Environ Microbiol 66:3078–3082
Brümmer IHM, Felske A, Wagner-Döbler I (2003) Diversity and seasonal variability of Betaproteobacteria in biofilms of polluted rivers: analysis by temperature gradient gel electrophoresis and cloning. Appl Environ Microbiol 69:4463–4473
Carlyle GC, Hill AR (2001) Groundwater phosphate dynamics in a river riparian zone: effects of hydrologic flowpaths, lithology and redox chemistry. J Hydrol 247:151–168
Carson JK, Rooney D, Gleeson DB, Clipson N (2007) Altering the mineral composition of soil causes a shift in microbial community structure. FEMS Microbiol Ecol 61:414–423
Chang B, Yu C, Yuan S (2004) Degradation of nonylphenol by anaerobic microorganisms from river sediment. Chemosphere 55:493–500
De Weert J, Vinas M, Grotenhuis T, Rijnaarts H, Langenhoff A (2010) Aerobic nonylphenol degradation and nitro-nonylphenol formation by microbial cultures from sediments. Appl Microbiol Biotechnol 86:761–771
Engel A, Piontek J, Grossart HP, Riebesell U, Kai GS, Sperling M (2014) Impact of CO2 enrichment on organic matter dynamics during nutrient induced coastal phytoplankton blooms. J Plankton Res 36:641–657
Franke C, Kissel C, Robin E, Bonté P, Lagroix F (2009) Characterization of magnetic particles in the seine river system: implications for the determination of natural versus anthropogenic input. Geochem Geophy Geosy 10:4918–4918
Fujii K, Urano N, Kimura S, Nomura Y, Karube I (2000) Microbial degradation of nonylphenol in some aquatic environments. Fisheries Sci 66(1):44–48
Fujii K, Urano N, Ushio H, Satomi M, Kimura S (2001) Sphingomonas cloacae sp. nov., a nonylphenol-degrading bacterium isolated from wastewater of a sewage-treatment plant in Tokyo. Int J Syst Evol Micr 51:603–610
Gasol JM, Comerma M, García JC, Armengol J, Casamayor EO, Kojecká P, Šimek K (2002) A transplant experiment to identify the factors controlling bacterial abundance, activity, production, and community composition in a eutrophic canyon-shaped reservoir. Limnol Oceanogr 47:62–77
Gu D, Xu H, He Y, Zhao F, Huang M (2015) Remediation of urban river water by Pontederia cordata combined with artificial aeration: organic matter and nutrients removal and root-adhered bacterial communities. Int J Phytoremediat (just-accepted): 00–00.
Hou S, Sun H (2007) Pollution of npeos in four municipal sewage treatment plants in the north of china. Front Env Sci Eng 1:196–201
Huang X, Chen W, Cai Q (1999) Survey, observation and analysis of lake ecology. Standard methods for observation and analysis in Chinese Ecosystem Research Network, Series V. Standards Press of China, Beijing (in Chinese)
Klecka GM, Gonsior SJ, West RJ, Goodwin PA, Markham DA (2011) Biodegradation of bisphenol A in aquatic environments: river die-away. Environ Toxicol Chem 20:2725–2735
Kowalkowski T, Zbytniewski R, Szpejna J, Buszewski B (2006) Application of chemometrics in river water classification. Water Res 40:744–752
Liu Z, Huang S, Sun G, Xu Z, Xu M (2012) Phylogenetic diversity, composition and distribution of bacterioplankton community in the Dongjiang River, China. FEMS Microbiol Ecol 80:30–44
Li S, Li J, Zhang Q (2011) Water quality assessment in the rivers along the water conveyance system of the Middle Route of the South to North Water Transfer Project (China) using multivariate statistical techniques and receptor modeling. J Hazard Mater 195:306–317
Matsumura Y, Hosokawa C, Sasaki-Mori M, Akahira A, Fukunaga K, Ikeuchi T, Oshiman K, Tsuchido T (2009) Isolation and characterization of novel bisphenol-A-degrading bacteria from soils. Biocontrol Sci 14:161–169
Mao Z, Zheng X, Zhang Y, Tao X, Li Y, Wang W (2012) Occurrence and biodegradation of nonylphenol in the environment. Int J Mol Sci 13:491–505
Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 75:14–49
Nie L, Wang L, Wang Q, Wang S, Zhou Q, Huang X (2015) Effects of bisphenol A on mineral nutrition in soybean seedling roots. Environ Toxicol Chem 34:133–140
Ortmann AC, Ortell N (2014) Changes in free-living bacterial community diversity reflect the magnitude of environmental variability. FEMS Microbiol Ecol 87:291–301
Oshiman K, Tsutsumi Y, Nishida T, Matsumura Y (2007) Isolation and characterization of a novel bacterium, Sphingomonas bisphenolicum strain AO1, that degrades bisphenol A. Biodegradation 18:247–255
Patel V, Munot H, Shouche YS, Madamwar D (2014) Response of bacterial community structure to seasonal fluctuation and anthropogenic pollution on coastal water of Alang–Sosiya ship breaking yard, Bhavnagar, India. Bioresource Technol 161:362–370
Qiu J (2011) China to spend billions cleaning up groundwater. Science 334
Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a Ph gradient in an arable soil. Isme J 4:1340–1351
Rubin MA, Leff LG (2007) Nutrients and other abiotic factors affecting bacterial communities in an Ohio River (USA). Microbial Ecol 54:374–383
Ruiz-González C, Proia L, Ferrera I, Gasol JM, Sabater S (2013) Effects of large river dam regulation on bacterioplankton community structure. FEMS Microbiol Ecol 84:316–331
Sabater S, Guasch H, Romaní A, Muñoz I (2002) The effect of biological factors on the efficiency of river biofilms in improving water quality. Hydrobiologia 469:149–156
Saiyood S, Vangnai AS, Thiravetyan P, Inthorn D (2010) Bisphenol A removal by the Dracaena plant and the role of plant-associating bacteria. J Hazard Mater 178:777–785
Wang X, Hu M, Xia Y, Wen X, Ding K (2012) Pyrosequencing analysis of bacterial diversity in 14 wastewater treatment systems in china. Appl Environ Microbiol 78:7042–7047
Wang Z, Yang Y, Sun W, Dai Y, Xie S (2015) Variation of nonylphenol-degrading gene abundance and bacterial community structure in bioaugmented sediment microcosm. Environ Sci Pollut R 22:2342–2349
Winkler M, Lawrence JR, Neu TR (2001) Selective degradation of ibuprofen and clofibric acid in two model river biofilm systems. Water Res 35:3197–3205
Yang S, Hai F, Nghiem LD, Price WE, Roddick F, Moreira MT, Magram SF (2013) Understanding the factors controlling the removal of trace organic contaminants by white-rot fungi and their lignin modifying enzymes: a critical review. Bioresour Technol 141:97–108
Yang Y, Wang Z, Xie S (2014a) Aerobic biodegradation of bisphenol a in river sediment and associated bacterial community change. Sci Total Environ 470–471:1184–1188
Yang J, Li H, Ran Y, Chan K (2014b) Distribution and bioconcentration of endocrine disrupting chemicals in surface water and fish bile of the Pearl River Delta, South China. Chemosphere 107:439–446
Ylla I, Romaní AM, Sabater S (2012) Labile and recalcitrant organic matter utilization by river biofilm under increasing water temperature. Microbiol Ecol 64:593–604
Yuan H, Ge T, Wu X, Liu S, Tong C, Qin H, Wu M, Wei W, Wu J (2012) Long-term field fertilization alters the diversity of autotrophic bacteria based on the ribulose-1,5-biphosphate carboxylase/oxygenase (RubisCO) large-subunit genes in paddy soil. Appl Microbiol Biot 95:1061–1071
Zhang C, Li Y, Wang C, Niu LH, Cai W (2015) Occurrence of endocrine disrupting compounds in aquatic environment and their bacterial degradation: a review. Crit Rev Env Sci Tec. doi:10.1080/10643389.2015.1061881
Zhang C, Zeng G, Yu L, Yu J, Li J, Huang G, Xi B, Liu H (2007) Aerobic degradation of bisphenol A by Achromobacter xylosoxidans strain B-16 isolated from compost leachate of municipal solid waste. Chemosphere 68:181–190
Zhang M, Xu J (2011) Nonpoint source pollution, environmental quality, and ecosystem health in China: introduction to the special section. J Environ Qual 40:1685–1694
Zhang Z, Ren N, Kannan K, Nan J, Liu L, Ma W, Qi H, Li Y (2014) Occurrence of endocrine-disrupting phenols and estrogens in water and sediment of the Songhua River, Northeastern China. Arch Environ Con Tox 66:361–369
Acknowledgments
The study was financially supported by the National Natural Science Foundation of China (No. 51322901 and 51479066), Foundation for Innovative Research Groups of the National Natural Science Foundation of China (51421006), the Fundamental Research Funds for the Central Universities, top-notch Academic Programs Project of Jiangsu Higher Education Institutions, and a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions.
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Responsible editor: Gerald Thouand
An erratum to this article is available at http://dx.doi.org/10.1007/s11356-017-8422-x.
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Cai, W., Li, Y., Wang, P. et al. Effect of the pollution level on the functional bacterial groups aiming at degrading bisphenol A and nonylphenol in natural biofilms of an urban river. Environ Sci Pollut Res 23, 15727–15738 (2016). https://doi.org/10.1007/s11356-016-6757-3
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DOI: https://doi.org/10.1007/s11356-016-6757-3