Abstract
Bacterial communities in the activated sludge (AS) determine the wastewater treatment performance in the municipal wastewater treatment plants (WWTPs). Aiming at identifying the affecting factors and the variation patterns of the bacterial assemblages in AS, a 2-year time-series AS samples were collected from two separated WWTPs and metagenomic sequencing was conducted. Obvious seasonal shift and succession of the bacterial community were observed in both WWTPs on the genus and species levels, especially for the persistent taxa, implying that temperature was a decisive factor for maintaining bacterial assemblage patterns in long-term period. Taxa abundance distribution (TAD) concerning occurrence frequency and average abundance were found fitting for exponential formulations, and the approximately equal total abundance of persistent taxa suggested that stable and high abundance (~ 90%) of core functional bacterial groups would help to maintain wastewater treatment performance. Drastic changes of environmental factors were found causing temporally significant bacterial structure variation, while the innate correlations between bacterial species could recover the community gradually and maintain relative stability of the AS system. Delayed correlations between environmental factors and abundant (persistent or intermittent) bacterial species were observed widely, while synchronous biotic interactions were identified more frequently. Besides, bacterial species with similar functions were prone to cluster together and shared the same seasonal variation pattern, implicating that the cooperation of functional correlated taxa played the most dominant role in shaping the bacterial assemblages. Furthermore, rare bacterial groups were to be explored for removing emerging pollutants with lower concentrations. The results of this study would assist dealing with operational defect and optimize the treatment system in WWTPs.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bond PL, Hugenholtz P, Keller J, Blackall LL (1995) Bacterial community structures of phosphate-removing and non-phosphate-removing activated sludge from sequencing batch reactors. Appl Environ Microbiol 61:1910–1916. https://doi.org/10.1002/bit.260460313
Curtis TP, Sloan WT (2006) Towards the design of diversity: stochastic models for community assembly in wastewater treatment plants. Water Sci Technol 54(1):227–236. https://doi.org/10.2166/wst.2006.391
Cytryn E, Minz D, Gelfand I, Neori A, Gieseke A, de Beer D, van Rijn J (2005) Sulfide-oxidizing activity and bacterial community structure in a fluidized bed reactor from a zero-discharge mariculture system. Environ Sci Technol 39:1802–1810. https://doi.org/10.1021/es0491533
Daims H, Taylor MW, Wagner M (2006) Wastewater treatment: a model system for microbial ecology. Trends Biotechnol 24:483–489. https://doi.org/10.1016/j.tibtech.2006.09.002
Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14(6):927–930. https://doi.org/10.1111/j.1654-1103.2003.tb02228.x
Fernández A, Huang S, Seston S, Xing J, Hickey R, Criddle C, Tiedje J (1999) How stable is stable? Function versus community composition. Appl Environ Microbiol 65:3697–3704. https://doi.org/10.1089/oli.1.1999.9.359
Gentile M, Yan T, Tiquia SM, Fields MW, Nyman J, Zhou J, Criddle CS (2006) Stability in a denitrifying fluidized bed reactor. Microb Ecol 52:311–321. https://doi.org/10.1007/s00248-006-9024-1
Gentile ME, Nyman JL, Criddle CS (2007) Correlation of patterns of denitrification instability in replicated bioreactor communities with shifts in the relative abundance and the denitrification patterns of specific populations. ISME J 1:714–728. https://doi.org/10.1038/ismej.2007.87
Guo F, Zhang T (2012) Profiling bulking and foaming bacteria in activated sludge by high throughput sequencing. Water Res 46:2772–2782. https://doi.org/10.1016/j.watres.2012.02.039
Hamasaki K, Taniguchi A, Tada Y, Kaneko R, Miki T (2015) Active populations of rare microbes in oceanic environments as revealed by bromide oxy-uridine incorporation and 454 tag sequencing. Gene 576(2):650–656. https://doi.org/10.1016/j.gene.2015.10.016
Hammer MO, Dat H, Ryan P (2001) Past: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):4–9
Hu M, Wang X, Wen X, Xia Y (2012) Microbial community structures in different wastewater treatment plants as revealed by 454-pyrosequencing analysis. Bioresour Technol 117:72–79. https://doi.org/10.1016/j.biortech.2012.04.061
Jiang XT, Li B, Ma LP (2018a) Temporal dynamics of activated sludge bacterial communities in two diversity variant full-scale sewage treatment plants. Appl Microbiol Biotechnol 102(21):9379–9388. https://doi.org/10.1007/s00253-018-9287-8
Jiang XT, Ye L, Ju F, Wang YL, Zhang T (2018b) Toward an intensive longitudinal understanding of activated sludge bacterial assembly and dynamics. Environ Sci Technol 52:8224–8232. https://doi.org/10.1021/acs.est.7b05579
Ju F, Zhang T (2014) Bacterial assembly and temporal dynamics in activated sludge of a full-scale municipal wastewater treatment plant. ISME J 9(3):683–695. https://doi.org/10.1038/ismej.2014.162
Ju F, Zhang T (2015) Experimental design and bioinformatics analysis for the application of metagenomics in environmental sciences and biotechnology. Environ Sci Technol 49:12628–12640. https://doi.org/10.1021/acs.est.5b03719
Ju F, Guo F, Ye L, Xia Y, Zhang T (2014) Metagenomic analysis on seasonal microbial variations of activated sludge from a full-scale wastewater treatment plant over 4 years. Environ Microbiol Rep 6(1):80–89. https://doi.org/10.1111/1758-2229.12110
Juretschko S, Timmermann G, Schmid M, Schleifer KH, Wagner M (1998) Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl Environ Microbiol 64:3042–3051
Karkman A, Mattila K, Tamminen M, Virta M (2011) Cold temperature decreases bacterial species richness in nitrogen-removing bioreactors treating inorganic mine waters. Biotechnol Bioeng 108:2876–2883. https://doi.org/10.1002/bit.23267
Kim YM, Cho HU, Lee DS, Park D, Park JM (2011) Influence of operational parameters on nitrogen removal efficiency and microbial communities in a full-scale activated sludge process. Water Res 45:5785–5795. https://doi.org/10.1016/j.watres.2011.08.063
Kim BC,Kim S, Shin T, Kim H, Sang BI (2013) Comparison of the bacterial communities in anaerobic, anoxic, and oxic chambers of a pilot A2O process using pyrosequencing analysis. Curr Microbiol 66(5):555-565. https://doi.org/10.1007/s00284-013-0311-z
Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinforma 9(1):559–571. https://doi.org/10.1186/1471-2105-9-559
Liu H, Yang F, Shi S, Liu X (2010) Effect of substrate COD/N ratio on performance and microbial community structure of a membrane aerated biofilm reactor. J Environ Sci (China) 22:540–546. https://doi.org/10.1016/S1001-0742(09)60143-1
Liu F, Hu X, Zhao X, Guo H, Zhao Y (2018) Microbial community structures' response to seasonal variation in a full-scale municipal wastewater treatment plant. Environ Eng Sci 0:1–8. https://doi.org/10.1089/ees.2018.0280
Ma Z, Wen XH, Zhao F, Xia F, Huang X, Waite D, Guan J (2013) Effect of temperature variation on membrane fouling and microbial munity structure in membrane bioreactor. Bioresour Technol 133:462–468. https://doi.org/10.1016/j.biortech.2013.01.023
McGill BJ, Etienne RS, Gray JS, David A, Anderson MJ, Habtamu Kassa B, Maria D, Enquist BJ, Green JL, Han FL (2010) Species abundance distributions: moving beyond single prediction theories to integration within an ecological framework. Ecol Lett 10(10):995–1015. https://doi.org/10.1111/j.1461-0248.2007.01094.x
Miura Y, Hiraiwa MN, Ito T, Itonaga T, Watanabe Y, Okabe S (2007) Bacterial community structures in MBRs treating municipal wastewater: relationship between community stability and reactor performance. Water Res 41:627–637. https://doi.org/10.1016/j.watres.2006.11.005
Nemergut DR, Schmidt SK, Fukami T, O'Neill SP, Bilinski TM, Stanish LF, Knelman JE, Darcy JL, Lynch RC, Wickey P (2013) Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev 77:342–356. https://doi.org/10.1128/MMBR.00051-12
Pholchan MK, Baptista JC, Davenport RJ, Curtis TP (2010) Systematic study of the effect of operating variables on reactor performance and microbial diversity in laboratory-scale activated sludge reactors. Water Res 44(5):1341–1352. https://doi.org/10.1016/j.watres.2009.11.005
Pholchan MK, Baptista JC, Davenport RJ, Sloan WT, Curtis TP (2013) Microbial community assembly, theory and rare functions. Front Microbiol 4(68):1–9. https://doi.org/10.3389/fmicb.2013.00068
Ruan Q, Dutta D, Schwalbach M, Steele J, Fuhrman J, Sun F (2006) Local similarity analysis reveals unique associations among marine bacterio plankton species and environmental factors. Bioinformatics 22:2532–2538. https://doi.org/10.1093/bioinformatics/btl417
Saunders AM, Albertsen M, Vollertsen J, Nielsen PH (2016) The activated sludge ecosystem contains a core community of abundant organisms. ISME J 10:11–20. https://doi.org/10.1038/ismej.2015.117
Schmid M, Thil A, Purkhold U, Walcher M, Bottero JY, Ginestet P, Nielsen PH, Wuertz S, Wagner M (2003) Characterization of activated sludge flocs by confocal laser scanning microscopy and image analysis. Water Res 37:2043–2052. https://doi.org/10.1016/S0043-1354(02)00616-4
Seviour R, (2010) Microbial Ecology of Activated Sludge. Water Intelligence Online 9
Shanks OC, Newton RJ, Kelty CA, Huse SM, Sogin ML, Mclellan SL (2013) Comparison of the microbial community structures of untreated wastewaters from different geographic locales. Appl Environ Microbiol 79:2906–2913. https://doi.org/10.1128/AEM.03448-12
Shannon P (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303
Sheng X, Liu R, Song X, Chen L, Tomoki K (2017) Comparative study on microbial community in intermittently aerated sequencing batch reactors (SBR) and a traditional SBR treating digested piggery wastewater. Front Environ Sci Eng 11(3):8. https://doi.org/10.1007/s11783-017-0929-3
Slater FR, Johnson CR, Blackall LL, Beiko RG, Bond PL (2010) Monitoring associations between clade-level variation, overall community structure and ecosystem function in enhanced biological phosphorus removal (EBPR) systems using terminal-restriction fragment length polymorphism (T-RFLP). Water Res 44:4908–4923. https://doi.org/10.1016/j.watres.2010.07.028
Truong DT, Franzosa E, Tickle TL, Scholz M, Weingart G, Pasolli E, Tett A, Huttenhower C, Segata N (2015) MetaPhlAn2 for enhanced metagenomic taxonomic profiling. Nat Methods 12,902–903. https://doi.org/10.1038/nmeth.3589
USGS (2004) Estimated use of water in the United States in 2000. U.S. Geological Survey, Washington, DC
van der Gast CJ, Walker AW, Stressmann FS, Rogers GB, Scott P, Daniels TW, Caroll MP, Parkhill J, Bruce KD (2011) Partitioning core and satellite taxa from within cystic fibrosis lung bacterial communities. ISME J 5:780–791. https://doi.org/10.1038/ismej.2010.175
Wagner M, Loy A (2002) Bacterial community composition and function in sewage treatment systems. Curr Opin Biotechnol 13:218–227. https://doi.org/10.1016/S0958-1669(02)00315-4
Wang XH, Hu M, Xia Y, Wen XH, Ding K (2012) Pyrosequencing analysis of bacterial diversity in 14 wastewater treatment systems in China. Appl Environ Microb 78(19):7042–7047. https://doi.org/10.1128/AEM.01617-1
Wells GF, Park HD, Yeung CH, Eggleston B, Francis CA, Criddle CS (2009) Ammonia-oxidizing communities in a highly aerated full-scale activated sludge bioreactor: Betaproteo bacterial dynamics and low relative abundance of Crenarchaea. Environ Microbiol 11(9):2310–2328. https://doi.org/10.1111/j.1462-2920.2009.01958.x
Xia LC, Ai D, Cram J, Fuhrman JA, Sun F, (2013) Efficient statistical significance approximation for local similarity analysis of high-throughput time series data. Bioinformatics 29(2):230–237
Xia SQ, Duan L, Song YH, Li JX, Piceno YM, Andersen GL, Alvarezcohen L, Morenoandrade I, Huang CL, Hermanowicz SW (2010) Bacterial community structure in. geographically distributed biological wastewater treatment reactors. Environ Sci Technol 44:7391–7396. https://doi.org/10.1021/es101554m
Xia Y, Wang X, Wen X, Ding K, Zhou J, Yang Y, Zhang Y (2014) Overall functional gene diversity of microbial communities in three full-scale activated sludge bioreactors. Appl Microbiol Biot 98(16):7233–7242. https://doi.org/10.1007/s00253-014-5791-7
Xia Y, Wen X, Zhang B, Yang Y (2018) Diversity and assembly patterns of activated sludge microbial communities: a review. Biotechnol Adv 36(4):1038–1047. https://doi.org/10.1016/j.biotechadv.2018.03.005
Yang C, Zhang W, Liu RH, Li Q, Li BB, Wang SF, Song CJ, Qiao CL, Mulchandani A (2011) Phylogenetic diversity and metabolic potential of activated sludge microbial communities in full-scale waste-water treatment plants. Environ Sci Technol 45(17):7408–7415. https://doi.org/10.1021/es2010545
Zhang T, Shao MF, Ye L, (2012) 454 Pyrosequencing reveals bacterial diversity of activated sludge from 14 sewage treatment plants. The ISME Journal 6(6):1137–1147
Zhou J, Liu W, Ye D, Jiang YH, Wang A (2013) Stochastic assembly leads to alternative communities with distinct functions in a bioreactor microbial community. MBio 4:e00584–e00512. https://doi.org/10.1128/mBio.00584-12
Funding
This study was funded by National Natural Science Foundation of China (51608329, 41907214), the Natural Science Foundation of Guangdong Province (2017A030313315), Shenzhen Science and Technology Projects (JCYJ20170412171918012), Postdoctoral Research Foundation of China (2019M653053), National Major Science and Technology Program for Water Pollution Control and Treatment (2017ZX07202).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
All abbreviations appearing in the text are interpreted in supplementary Table S1.
Rights and permissions
About this article
Cite this article
Cai, X., Mao, Y., Xu, J. et al. Characterizing community dynamics and exploring bacterial assemblages in two activated sludge systems. Appl Microbiol Biotechnol 104, 1795–1808 (2020). https://doi.org/10.1007/s00253-019-10279-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-019-10279-2