Identifying human-induced influence on microbial community: A comparative study in the effluent-receiving areas in Hangzhou Bay

doi:10.1007/s11783-019-1174-8

Front. Environ. Sci. Eng.

2019, Vol. 13

Issue (6) : 90 https://doi.org/10.1007/s11783-019-1174-8

RESEARCH ARTICLE

Identifying human-induced influence on microbial community: A comparative study in the effluent-receiving areas in Hangzhou Bay

Yuhan Zheng¹, Zhiguo Su², Tianjiao Dai², Feifei Li¹, Bei Huang³, Qinglin Mu³, Chuanping Feng¹(

), Donghui Wen²(

)

¹. School of Water Resource and Environmental Science, China University of Geosciences (Beijing), Beijing 100083, China
². College of Environmental Sciences and Engineering, Peking University, Beijing 100871, China
³. Zhejiang Provincial Zhoushan Marine Ecological Environmental Monitoring Station, Zhoushan 316021, China

Download: PDF(1230 KB) HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

Abstract

Microbial compositions showed high differences in two study areas.

COD was the key anthropogenic indicator in the coastal wastewater disposal area.

Distinctive microbes capable of degrading toxic pollutants were screened.

Microbial communities in effluent-receiving areas followed “niche theory”.

Microbial community structure is affected by both natural processes and human activities. In coastal area, anthropegenetic activity can usually lead to the discharge of the effluent from wastewater treatment plant (WWTP) to sea, and thus the water quality chronically turns worse and marine ecosystem becomes unhealthy. Microorganisms play key roles in pollutants degradation and ecological restoration; however, there are few studies about how the WWTP effluent disposal influences coastal microbial communities. In this study, sediment samples were collected from two WWTP effluent-receiving areas (abbreviated as JX and SY) in Hangzhou Bay. First, based on the high-throughput sequencing of 16S rRNA gene, microbial community structure was analyzed. Secondly, several statistical analyses were conducted to reveal the microbial community characteristics in response to the effluent disposal. Using PCoA, the significant difference of in microbial community structure was determined between JX and SY; using RDA, water COD and temperature, and sediment available phosphate and ammonia nitrogen were identified as the key environmental factors for the community difference; using LDA effect size analysis, the most distinctive microbes were found and their correlations with environmental factors were investigated; and according to detrended beta-nearest-taxon-index, the sediment microbial communities were found to follow “niche theory”. An interesting and important finding was that in SY that received more and toxic COD, many distinctive microbes were related to the groups that were capable of degrading toxic organic pollutants. This study provides a clear illustration of eco-environmental deterioration under the long-term human pressure from the view of microbial ecology.

Keywords Microbial community structure Effluent-receiving area High-throughput sequencing Costal sediments Wastewater treatment plant (WWTP)

Corresponding Author(s): Chuanping Feng,Donghui Wen

Issue Date: 29 November 2019

Cite this article:

Yuhan Zheng,Zhiguo Su,Tianjiao Dai, et al. Identifying human-induced influence on microbial community: A comparative study in the effluent-receiving areas in Hangzhou Bay[J]. Front. Environ. Sci. Eng., 2019, 13(6): 90.

URL:

https://academic.hep.com.cn/fese/EN/10.1007/s11783-019-1174-8
https://academic.hep.com.cn/fese/EN/Y2019/V13/I6/90

Tab.1 The locations of the sampling sites

Fig.1 Boxplot of environmental factors in JX (red) and SY (green): (a) Seawater and (b) sediments.

Fig.2 The microbial community structures and taxonomic compositions at (a) phylum level and (b) class level.

Fig.3 Principal coordinate analysis (PCoA) of the microbial community compositions based on Bray-Curtis distance.

Fig.4 Redundancy analysis (RDA) between the microbial compositions and the environmental factors. Red arrows indicate environment factors. Gray points represent sampling sites.

Fig.5 Indicators of microbial classes or genera in JX and SY with LDA values higher than 2.0, and their Pearson correlations with the environmental factors: red is negatively correlated, blue is positively correlated, and circle size indicates the size of the correlation.

Fig.6 Boxplot of beta nearest taxon Index (bNTI) in JX and SY.

Tab.2 Characteristics about the differential microbes reported in literatures

1	J C Aciego Pietri, P C Brookes (2009). Substrate inputs and pH as factors controlling microbial biomass, activity and community structure in an arable soil. Soil Biology & Biochemistry, 41(7): 1396–1405 https://doi.org/10.1016/j.soilbio.2009.03.017
2	D Ager, S Evans, H Li, A K Lilley, C J van der Gast (2010). Anthropogenic disturbance affects the structure of bacterial communities. Environmental Microbiology, 12(3): 670–678 https://doi.org/10.1111/j.1462-2920.2009.02107.x pmid: 20002134
3	K K Arkema, G M Verutes, S A Wood, C Clarke-Samuels, S Rosado, M Canto, A Rosenthal, M Ruckelshaus, G Guannel, J Toft (2015). Embedding ecosystem services in coastal planning leads to better outcomes for people and nature. Proceedings of the National Academy of Sciences, 122(24): 7390–7395
4	A Basset, E Barbone, M Elliott, B L Li, S E Jorgensen, P Lucena-Moya, I Pardo, D Mouillot (2013). A unifying approach to understanding transitional waters: Fundamental properties emerging from ecotone ecosystems. Estuarine Coastal and Shelf Science, 132(SI): 5–16
5	L Cai, K Yu, Y Yang, B W Chen, X D Li, T Zhang (2013). Metagenomic exploration reveals high levels of microbial arsenic metabolism genes in activated sludge and coastal sediments. Applied Microbiology and Biotechnology, 97(21): 9579–9588 https://doi.org/10.1007/s00253-012-4678-8 pmid: 23340578
6	X Cao, M Diao, B Zhang, H Liu, S Wang, M Yang (2017). Spatial distribution of vanadium and microbial community responses in surface soil of Panzhihua mining and smelting area, China. Chemosphere, 183: 9–17 https://doi.org/10.1016/j.chemosphere.2017.05.092 pmid: 28527917
7	G R Craig, P L Orr, J L Robertson, W M Vrooman (1990). Toxicity and bioaccumulation of AOX and EOX. Pulp & Paper Canada, 91(9): 39–45
8	C Cravo-Laureau, R Duran (2014). Marine coastal sediments microbial hydrocarbon degradation processes: Contribution of experimental ecology in the omics’ era. Frontiers in Microbiology, 5(39): 1–8
9	T Dai, Y Zhang, D Ning, Z Su, Y Tang, B Huang, Q Mu, D Wen (2018). Dynamics of sediment microbial functional capacity and community interaction networks in an urbanized coastal estuary. Frontiers in Microbiology, 9(2731): 1–14 https://doi.org/10.3389/fmicb.2018.02731 pmid: 30487783
10	T Dai, Y Zhang, Y Tang, Y Bai, Y Tao, B Huang, D Wen (2016). Identifying the key taxonomic categories that characterize microbial community diversity using full-scale classification: a case study of microbial communities in the sediments of Hangzhou Bay. FEMS Microbiology Ecology, 92(10): fiw150 https://doi.org/10.1093/femsec/fiw150 pmid: 27402713
11	J Du, K Xiao, Y Huang, H Li, H Tan, L Cao, Y Lu, S Zhou (2011). Seasonal and spatial diversity of microbial communities in marine sediments of the South China Sea. Antonie van Leeuwenhoek, 100(3): 317–331 https://doi.org/10.1007/s10482-011-9587-9 pmid: 21604204
12	A Ehrig, R H Müller, W Babel (1997). Isolation of phenoxy herbicide‐degrading Rhodoferax species from contaminated building material. Acta Biotechnologica, 17(4): 351–356 https://doi.org/10.1002/abio.370170411
13	R El Zrelli, L Rabaoui, M Ben Alaya, N Daghbouj, S Castet, P Besson, S Michel, N Bejaoui, P Courjault-Radé (2018). Seawater quality assessment and identification of pollution sources along the central coastal area of Gabes Gulf (SE Tunisia): Evidence of industrial impact and implications for marine environment protection. Marine Pollution Bulletin, 127: 445–452 https://doi.org/10.1016/j.marpolbul.2017.12.012 pmid: 29475683
14	S K Fagervold, S Bourgeois, A M Pruski, F Charles, P Kerhervé, G Vétion, P E Galand (2014). River organic matter shapes microbial communities in the sediment of the Rhône prodelta. ISME Journal, 8(11): 2327–2338 https://doi.org/10.1038/ismej.2014.86 pmid: 24858780
15	M È Garneau, W F Vincent, R Terrado, C Lovejoy (2009). Importance of particle-associated bacterial heterotrophy in a coastal Arctic ecosystem. Journal of Marine Systems, 75(1–2): 185–197 https://doi.org/10.1016/j.jmarsys.2008.09.002
16	J A Gilbert, D Field, P Swift, S Thomas, D Cummings, B Temperton, K Weynberg, S Huse, M Hughes, I Joint, P J Somerfield, M Mühling (2010). The taxonomic and functional diversity of microbes at a temperate coastal site: A ‘multi-omic’ study of seasonal and diel temporal variation. PLoS One, 5(11): e15545 https://doi.org/10.1371/journal.pone.0015545 pmid: 21124740
17	B S Halpern, S Walbridge, K A Selkoe, C V Kappel, F Micheli, C D’Agrosa, J F Bruno, K S Casey, C Ebert, H E Fox, R Fujita, D Heinemann, H S Lenihan, E M P Madin, M T Perry, E R Selig, M Spalding, R Steneck, R Watson (2008). A global map of human impact on marine ecosystems. Science, 319(5865): 948–952 https://doi.org/10.1126/science.1149345 pmid: 18276889
18	A Hu, X Yang, N Chen, L Hou, Y Ma, C P Yu (2014). Response of bacterial communities to environmental changes in a mesoscale subtropical watershed, Southeast China. Science of the Total Environment, 472: 746–756 https://doi.org/10.1016/j.scitotenv.2013.11.097 pmid: 24333997
19	S Jechalke, A G Franchini, F Bastida, P Bombach, M Rosell, J Seifert, M von Bergen, C Vogt, H H Richnow (2013). Analysis of structure, function, and activity of a benzene-degrading microbial community. FEMS Microbiology Ecology, 85(1): 14–26 https://doi.org/10.1111/1574-6941.12090 pmid: 23398624
20	C O Jeon, W Park, W C Ghiorse, E L Madsen (2004). Polaromonas naphthalenivorans sp. nov., a naphthalene-degrading bacterium from naphthalene-contaminated sediment. International Journal of Systematic and Evolutionary Microbiology, 54(1): 93–97 https://doi.org/10.1099/ijs.0.02636-0 pmid: 14742464
21	E L Johnston, L H Hedge, M Mayer-Pinto (2015). The urgent global need to understand port and harbour ecosystems. Marine and Freshwater Research, 66(12): i–ii https://doi.org/10.1071/MFv66n12_ED
22	N O Jørgensen, K K Brandt, O Nybroe, M Hansen (2010). Vogesella mureinivorans sp. nov., a peptidoglycan-degrading bacterium from lake water. International Journal of Systematic and Evolutionary Microbiology, 60(10): 2467–2472 https://doi.org/10.1099/ijs.0.018630-0 pmid: 19946047
23	V Kasalický, Y Zeng, K Piwosz, K Šimek, H Kratochvilová, M Koblížek (2017). Aerobic anoxygenic photosynthesis is commonly present within the genus limnohabitans. Applied and Environmental Microbiology, 84(1): e02116–e02117 https://doi.org/10.1128/AEM.02116-17 pmid: 29030444
24	S Kumar, M Herrmann, A Blohm, I Hilke, T Frosch, S E Trumbore, K Küsel (2018). Thiosulfate- and hydrogen-driven autotrophic denitrification by a microbial consortium enriched from groundwater of an oligotrophic limestone aquifer. FEMS Microbiology Ecology, 94(10): fiy141 https://doi.org/10.1093/femsec/fiy141 pmid: 30052889
25	Y Li, C Lin, Y Wang, X Gao, T Xie, R Hai, X Wang, X Zhang (2017). Multi-criteria evaluation method for site selection of industrial wastewater discharge in coastal regions. Journal of Cleaner Production, 161: 1143–1152 https://doi.org/10.1016/j.jclepro.2017.05.030
26	J Liu, X Chen, H Y Shu, X R Lin, Q X Zhou, T Bramryd, W S Shu, L N Huang (2018). Microbial community structure and function in sediments from e-waste contaminated rivers at Guiyu area of China. Environmental Pollution, 235: 171–179 https://doi.org/10.1016/j.envpol.2017.12.008 pmid: 29288930
27	J Liu, H Yang, M Zhao, X H Zhang (2014). Spatial distribution patterns of benthic microbial communities along the Pearl Estuary, China. Systematic and Applied Microbiology, 37(8): 578–589 https://doi.org/10.1016/j.syapm.2014.10.005 pmid: 25467555
28	S Liu, Y Liu, G Yang, S Qiao, C Li, Z Zhu, X Shi (2012). Distribution of major and trace elements in surface sediments of Hangzhou Bay in China. Acta Oceanologica Sinica, 31(4): 89–100 https://doi.org/10.1007/s13131-012-0223-y
29	Y Liu, X Xia, S Chen, J Jia, T Cai (2017). Morphological evolution of Jinshan trough in Hangzhou Bay (China) from 1960 to 2011. Estuarine, Coastal and Shelf Science, 198(SI): 367–377 https://doi.org/10.1016/j.ecss.2016.11.004
30	Z P Liu, B J Wang, Y H Liu, S J Liu (2005). Novosphingobium taihuense sp. nov., a novel aromatic-compound-degrading bacterium isolated from Taihu Lake, China. International Journal of Systematic and Evolutionary Microbiology, 55(3): 1229–1232 https://doi.org/10.1099/ijs.0.63468-0 pmid: 15879260
31	Y Long, X Jiang, Q Guo, B Li, S Xie (2017). Sediment nitrite-dependent methane-oxidizing microorganisms temporally and spatially shift in the Dongjiang River. Applied Microbiology and Biotechnology, 101(1): 401–410 https://doi.org/10.1007/s00253-016-7888-7 pmid: 27726022
32	A Makhdoumi-Kakhki, M A Amoozegar, B Kazemi, L PaiC, A Ventosa (2012). Prokaryotic diversity in Aran-Bidgol salt lake, the largest hypersaline playa in Iran. Microbes and Environments, 27(1): 87–93 https://doi.org/10.1264/jsme2.ME11267 pmid: 22185719
33	H Masuda, Y Shiwa, H Yoshikawa, G J Zylstra (2014). Draft genome sequence of the versatile alkane-degrading bacterium Aquabacterium sp. strain NJ1. Genome Announcements, 2(6): e01271-14 https://doi.org/10.1128/genomeA.01271-14 pmid: 25477416
34	T E Mattes, A K Alexander, P M Richardson, A C Munk, C S Han, P Stothard, N V Coleman (2008). The genome of Polaromonas sp. strain JS666: insights into the evolution of a hydrocarbon- and xenobiotic-degrading bacterium, and features of relevance to biotechnology. Applied and Environmental Microbiology, 74(20): 6405–6416 https://doi.org/10.1128/AEM.00197-08 pmid: 18723656
35	S R Miller, A L Strong, K L Jones, M C Ungerer (2009). Bar-coded pyrosequencing reveals shared bacterial community properties along the temperature gradients of two alkaline hot springs in Yellowstone National Park. Applied and Environmental Microbiology, 75(13): 4565–4572 https://doi.org/10.1128/AEM.02792-08 pmid: 19429553
36	M V Monferrán, J R Echenique, D A Wunderlin (2005). Degradation of chlorobenzenes by a strain of Acidovorax avenae isolated from a polluted aquifer. Chemosphere, 61(1): 98–106 https://doi.org/10.1016/j.chemosphere.2005.03.003 pmid: 16157172
37	M T Montgomery, R B Coffin, T J Boyd, J P Smith, S E Walker, C L Osburn (2011). 2,4,6-Trinitrotoluene mineralization and bacterial production rates of natural microbial assemblages from coastal sediments. Environmental Pollution, 159(12): 3673–3680 https://doi.org/10.1016/j.envpol.2011.07.018 pmid: 21839558
38	A Muhammetoglu, O B Yalcin, T Ozcan (2012). Prediction of wastewater dilution and indicator bacteria concentrations for marine outfall systems. Marine Environmental Research, 78: 53–63 https://doi.org/10.1016/j.marenvres.2012.04.005 pmid: 22622074
39	V S Naidu (2013). Estimation of near-field and far-field dilutions for site selection of effluent outfall in a coastal region—a case study. Journal of Coastal Research, 292(6): 1326–1340 https://doi.org/10.2112/JCOASTRES-D-11-00159.1
40	S Ntougias (2014). Phylogeny and ecophysiological features of prokaryotes isolated from temporary saline tidal pools. Annals of Microbiology, 64(2): 599–609 https://doi.org/10.1007/s13213-013-0693-y
41	Y Peng, W Yang, K Yue, B Tan, C Huang, Z Xu, X Ni, L Zhang, F Wu (2018). Temporal dynamics of phosphorus during aquatic and terrestrial litter decomposition in an alpine forest. Science of the Total Environment, 642: 832–841 https://doi.org/10.1016/j.scitotenv.2018.06.135 pmid: 29925055
42	V H Pham, S W Jeong, J Kim (2015). Aquabacterium olei sp. nov., an oil-degrading bacterium isolated from oil-contaminated soil. International Journal of Systematic and Evolutionary Microbiology, 65(10): 3597–3602 https://doi.org/10.1099/ijsem.0.000458 pmid: 26297008
43	K K Salinero, K Keller, W S Feil, H Feil, S Trong, G Di Bartolo, A Lapidus (2009). Metabolic analysis of the soil microbe Dechloromonas aromatica str. RCB: indications of a surprisingly complex life-style and cryptic anaerobic pathways for aromatic degradation. BMC Genomics, 10(1): 351 https://doi.org/10.1186/1471-2164-10-351 pmid: 19650930
44	N Segata, J Izard, L Waldron, D Gevers, L Miropolsky, W S Garrett, C Huttenhower (2011). Metagenomic biomarker discovery and explanation. Genome Biology, 12(6): R60 https://doi.org/10.1186/gb-2011-12-6-r60 pmid: 21702898
45	C Shen, J Xiong, H Zhang, Y Feng, X Lin, X Li, W Liang, H Chu (2013). Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biology & Biochemistry, 57: 204–211 https://doi.org/10.1016/j.soilbio.2012.07.013
46	D R Singleton, L Guzman Ramirez, M D Aitken (2009). Characterization of a polycyclic aromatic hydrocarbon degradation gene cluster in a phenanthrene-degrading Acidovorax strain. Applied and Environmental Microbiology, 75(9): 2613–2620 https://doi.org/10.1128/AEM.01955-08 pmid: 19270134
47	J H Sohn, K K Kwon, J H Kang, H B Jung, S J Kim (2004). Novosphingobium pentaromativorans sp. nov., a high-molecular-mass polycyclic aromatic hydrocarbon-degrading bacterium isolated from estuarine sediment. International Journal of Systematic and Evolutionary Microbiology, 54(5): 1483–1487 https://doi.org/10.1099/ijs.0.02945-0 pmid: 15388699
48	J C Stegen, X Lin, J K Fredrickson, X Chen, D W Kennedy, C J Murray, M L Rockhold, A Konopka (2013). Quantifying community assembly processes and identifying features that impose them. ISME Journal, 7(11): 2069–2079 https://doi.org/10.1038/ismej.2013.93 pmid: 23739053
49	Z Su, T Dai, Y Tang, Y Tao, B Huang, Q Mu, D Wen (2018). Sediment bacterial community structures and their predicted functions implied the impacts from natural processes and anthropogenic activities in coastal area. Marine Pollution Bulletin, 131(Pt A): 481–495 https://doi.org/10.1016/j.marpolbul.2018.04.052 pmid: 29886974
50	B Subha, Y C Song, J H Woo (2015). Optimization of biostimulant for bioremediation of contaminated coastal sediment by response surface methodology (RSM) and evaluation of microbial diversity by pyrosequencing. Marine Pollution Bulletin, 98(1–2): 235–246 https://doi.org/10.1016/j.marpolbul.2015.06.042 pmid: 26139459
51	M Y Sun, K A Dafforn, E L Johnston, M V Brown (2013). Core sediment bacteria drive community response to anthropogenic contamination over multiple environmental gradients. Environmental Microbiology, 15(9): 2517–2531 https://doi.org/10.1111/1462-2920.12133 pmid: 23647974
52	R Sun, Y Sun, Q X Li, X Zheng, X Luo, B Mai (2018). Polycyclic aromatic hydrocarbons in sediments and marine organisms: Implications of anthropogenic effects on the coastal environment. Science of the Total Environment, 640–641: 264–272 https://doi.org/10.1016/j.scitotenv.2018.05.320 pmid: 29859442
53	Y Tao, T Dai, B Huang, D Wen (2017). The impact of wastewater treatment effluent on microbial biomasses and diversities in coastal sediment microcosms of Hangzhou Bay. Marine Pollution Bulletin, 114(1): 355–363 https://doi.org/10.1016/j.marpolbul.2016.09.047 pmid: 27707472
54	J Van Eldere (2003). Multicentre surveillance of Pseudomonas aeruginosa susceptibility patterns in nosocomial infections. Journal of Antimicrobial Chemotherapy, 51(2): 347–352 https://doi.org/10.1093/jac/dkg102 pmid: 12562701
55	P P Wong, I J Losada, J P Gattuso, J Hinkel, A Khattabi, K L Mcinnes, Y Saito, A Sallenger (2014). Climate Change. Cambridge: Cambridge University Press, 361–409
56	S Xie, W Sun, C Luo, A M Cupples (2011). Novel aerobic benzene degrading microorganisms identified in three soils by stable isotope probing. Biodegradation, 22(1): 71–81 https://doi.org/10.1007/s10532-010-9377-5 pmid: 20549308
57	Y Xie, L Chen, R Liu (2017). AOX contamination status and genotoxicity of AOX-bearing pharmaceutical wastewater. Journal of Environmental Sciences-China, 52: 170–177 https://doi.org/10.1016/j.jes.2016.04.014 pmid: 28254035
58	Y W Xie, L J Chen, R Liu, J P Tian (2018). AOX contamination in Hangzhou Bay, China: Levels, distribution and point sources. Environmental Pollution, 235: 462–469 https://doi.org/10.1016/j.envpol.2017.12.089 pmid: 29316521
59	J Xiong, X Ye, K Wang, H Chen, C Hu, J Zhu, D Zhang (2014). The biogeography of the sediment bacterial community responds to a nitrogen pollution gradient in the East China Sea. Applied and Environmental Microbiology: AEM, 80(6): 1919–1925
60	Y Zeng, V Kasalicky, K Simek, M Koblizeka (2012). Genome sequences of two freshwater betaproteobacterial isolates, Limnohabitans species strains Rim28 and Rim47, indicate their capabilities as both photoautotrophs and ammonia oxidizers. Journal of Bacteriology, 194(22): 6302–6303 https://doi.org/10.1128/JB.01481-12 pmid: 23105051
61	F Zhang, X Sun, Y Zhou, C Zhao, Z Du, R Liu (2017). Ecosystem health assessment in coastal waters by considering spatio-temporal variations with intense anthropogenic disturbance. Environmental Modelling & Software, 96: 128–139 https://doi.org/10.1016/j.envsoft.2017.06.052
62	X Zhang, S Xu, C Li, L Zhao, H Feng, G Yue, Z Ren, G Cheng (2014a). The soil carbon/nitrogen ratio and moisture affect microbial community structures in alkaline permafrost-affected soils with different vegetation types on the Tibetan plateau. Research in Microbiology, 165(2): 128–139 https://doi.org/10.1016/j.resmic.2014.01.002 pmid: 24463013
63	Y Zhang, L Chen, R Sun, T Dai, J Tian, R Liu, D Wen (2014b). Effect of wastewater disposal on the bacterial and archaeal community of sea sediment in an industrial area in China. FEMS Microbiology Ecology, 88(2): 320–332 https://doi.org/10.1111/1574-6941.12298 pmid: 24697989
64	Y Zhang, L Chen, R Sun, T Dai, J Tian, W Zheng, D Wen (2016a). Population and diversity of ammonia-oxidizing archaea and bacteria in a pollutants’ receiving area in Hangzhou Bay. Applied Microbiology and Biotechnology, 100(13): 6035–6045 https://doi.org/10.1007/s00253-016-7421-z pmid: 26960319
65	Y Zhang, L Chen, R Sun, T Dai, J Tian, W Zheng, D Wen (2016b). Temporal and spatial changes of microbial community in an industrial effluent receiving area in Hangzhou Bay. Journal of Environmental Sciences-China, 44: 57–68 https://doi.org/10.1016/j.jes.2015.11.023 pmid: 27266302
66	Zhejiang Province Ocean and Fisheries Bureau (2007). Specifications for Oceanographic Survey—Part 4: Survey of Chemical Parameters in Sea Water. Beijing: Standards Press of China (in Chinese)
67	Zhejiang Province Ocean and Fisheries Bureau (2017). Marine Environmental Bulletin in Zhejiang Province of 2016. Hangzhou: Marine and Fishery Bureau in Zhejiang (in Chinese)
68	L Zinger, L A Amaral-Zettler, J A Fuhrman, M C Horner-Devine, S M Huse, D B M Welch, J B Martiny, M Sogin, A Boetius, A Ramette (2011). Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems. PLoS One, 6(9): e24570 https://doi.org/10.1371/journal.pone.0024570 pmid: 21931760
69	H Zouch, F Karray, F Armougom, S Chifflet, A Hirschler-Réa, H Kharrat, L Kamoun, W Ben Hania, B Ollivier, S Sayadi, M Quéméneur (2017). Microbial diversity in sulfate-reducing marine sediment enrichment cultures associated with anaerobic biotransformation of coastal stockpiled phosphogypsum (Sfax, Tunisia). Frontiers in Microbiology, 8(1583): 1–11 https://doi.org/10.3389/fmicb.2017.01583 pmid: 28871244

[1]

FSE-19100-OF-ZYH_suppl_1

Download

[1]	Fan Lu, Tianyu Hu, Shunyan Wei, Liming Shao, Pinjing He. Bioaerosolization behavior along sewage sludge biostabilization[J]. Front. Environ. Sci. Eng., 2021, 15(3): 45-.
[2]	Yue Hu, Ding Dong, Kun Wan, Chao Chen, Xin Yu, Huirong Lin. Potential shift of bacterial community structure and corrosion-related bacteria in drinking water distribution pipeline driven by water source switching[J]. Front. Environ. Sci. Eng., 2021, 15(2): 28-.
[3]	Jiuhui Qu, Hongchen Wang, Kaijun Wang, Gang Yu, Bing Ke, Han-Qing Yu, Hongqiang Ren, Xingcan Zheng, Ji Li, Wen-Wei Li, Song Gao, Hui Gong. Municipal wastewater treatment in China: Development history and future perspectives[J]. Front. Environ. Sci. Eng., 2019, 13(6): 88-.
[4]	Lian Yang, Qinxue Wen, Zhiqiang Chen, Ran Duan, Pan Yang. Impacts of advanced treatment processes on elimination of antibiotic resistance genes in a municipal wastewater treatment plant[J]. Front. Environ. Sci. Eng., 2019, 13(3): 32-.
[5]	Wanqi Qi, Weiying Li, Junpeng Zhang, Xuan Wu, Jie Zhang, Wei Zhang. Effect of biological activated carbon filter depth and backwashing process on transformation of biofilm community[J]. Front. Environ. Sci. Eng., 2019, 13(1): 15-.
[6]	Xiaohui Wang, Shuai Du, Tao Ya, Zhiqiang Shen, Jing Dong, Xiaobiao Zhu. Removal of tetrachlorobisphenol A and the effects on bacterial communities in a hybrid sequencing biofilm batch reactor-constructed wetland system[J]. Front. Environ. Sci. Eng., 2019, 13(1): 14-.
[7]	Jun Li, Wentao Li, Gan Luo, Yan Li, Aimin Li. Effect of nitrobenzene on the performance and bacterial community in an expanded granular sludge bed reactor treating high-sulfate organic wastewater[J]. Front. Environ. Sci. Eng., 2019, 13(1): 6-.
[8]	Zechong Guo, Lei Gao, Ling Wang, Wenzong Liu, Aijie Wang. Enhanced methane recovery and exoelectrogen-methanogen evolution from low-strength wastewater in an up-flow biofilm reactor with conductive granular graphite fillers[J]. Front. Environ. Sci. Eng., 2018, 12(4): 13-.
[9]	Liguo Zhang, Qiaoying Ban, Jianzheng Li. Microbial community dynamics at high organic loading rates revealed by pyrosequencing during sugar refinery wastewater treatment in a UASB reactor[J]. Front. Environ. Sci. Eng., 2018, 12(4): 4-.
[10]	Feng Wang, Weiying Li, Yue Li, Junpeng Zhang, Jiping Chen, Wei Zhang, Xuan Wu. Molecular analysis of bacterial community in the tap water with different water ages of a drinking water distribution system[J]. Front. Environ. Sci. Eng., 2018, 12(3): 6-.
[11]	Jiaxuan YANG, Jun MA, Dan SONG, Xuedong ZHAI, Xiujuan KONG. Impact of preozonation on the bioactivity and biodiversity of subsequent biofilters under low temperature conditions—A pilot study[J]. Front. Environ. Sci. Eng., 2016, 10(4): 5-.
[12]	ZHAO Yangguo, WANG Aijie, REN Nanqi, ZHAO Yan. Microbial community structure in different wastewater treatment processes characterized by single-strand conformation polymorphism (SSCP) technique[J]. Front.Environ.Sci.Eng., 2008, 2(1): 116-121.
[13]	LI Xiaodong, ZENG Guangming, HUANG Guohe, LI Jianbing, JIANG Ru. Short-term prediction of the influent quantity time series of wastewater treatment plant based on a chaos neural network model[J]. Front.Environ.Sci.Eng., 2007, 1(3): 334-338.

Viewed

Full text

Abstract

Cited

Shared

Discussed