Skip to main content

Dynamics of size-fractionated bacterial communities during the coastal dispersal of treated municipal effluents

Applied Microbiology and Biotechnology volume 100, pages 5839–5848 (2016)Cite this article

Abstract

Everyday huge amount of treated municipal wastewater is discharged into the coastal seawater. However, microbial biomarkers for the municipal effluent instead of the fecal species from raw sewage have not been proposed. Meanwhile, bacterial taxa for degrading large amounts of input organics have not been fully understood. In this study, raw effluent and serial water samples were collected from the coastal dispersal of two sewage treatment plants in Xiamen, China. Free-living (FL) and particle-associated (PA) bacterial communities were analyzed via high-throughput sequencing of 16S rRNA gene and quantitative PCR to measure bacterial abundance. The PA bacterial communities in our samples exhibited higher cell abundance, alpha diversity, and population dynamics than the FL bacterial communities, which supports greater environmental significance of the PA bacterial communities. Two non-fecal but typical genera in activated sludge, Zoogloea and Dechloromonas, exhibited decreased but readily detectable abundance along the effluent dispersal distance. Furthermore, the dominating microbial species near the outfalls were related to well-known marine indigenous taxa, such as SAR11 clade, OM60 clade, low-GC Actinobacteria, and unclassified Flavobacteriales, as well as the less understood taxa like Pseudohongiella and Microbacteriaceae. It is interesting that these taxa exhibited two types of correlation patterns with COD concentration. Our study suggested Zoogloea as a potential indicator of municipal effluents and also proposed potential utilizers of residual effluent COD in marine environments.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Al-Bahry SN, Mahmoud IY, Al-Belushi KI, Elshafie AE, Al-Harthy A, Bakheit CK (2009) Coastal sewage discharge and its impact on fish with reference to antibiotic resistant enteric bacteria and enteric pathogens as bio-indicators of pollution. Chemosphere 77:1534–1539

    CAS  Article  PubMed  Google Scholar 

  • Anderson KL, Whitlock JE, Harwood VJ (2005) Persistence and differential survival of fecal indicator bacteria in subtropical waters and sediments. Appl Environ Microbiol 71:3041–3048

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Cai L, Ju F, Zhang T (2014) Tracking human sewage microbiome in a municipal wastewater treatment plant. Appl Microbiol Biotechnol 98:3317–3326

    CAS  Article  PubMed  Google Scholar 

  • Chandler DP (1998) Redefining relativity: quantitative PCR at low template concentrations for industrial and environmental microbiology. J Ind Microbiol Biotech 21:128–140

    CAS  Article  Google Scholar 

  • Connon SA, Giovannoni SJ (2002) High-throughput methods for culturing microorganisms in very-low-nutrient media yield diverse new marine isolates. Appl Environ Microbiol 68:3878–3885

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Crump BC, Baross JA, Simenstad CA (1998) Dominance of particle-attached bacteria in the Columbia River estuary, USA. Aquat Microb Ecol 14:7–18

    Article  Google Scholar 

  • D’Ambrosio L, Ziervogel K, MacGregor B, Teske A, Arnosti C (2014) Composition and enzymatic function of particle-associated and free-living bacteria: a coastal/offshore comparison. ISME J 8:2167–2179

    Article  PubMed  Google Scholar 

  • DeLong EF, Franks DG, Alldredge AL (1993) Phylogenetic diversity of aggregate attached vs. free-living marine bacterial assemblages. Limnol Oceanogr 38:924–934

    Article  Google Scholar 

  • Dias FF, Bhat JV (1964) Microbial ecology of activated sludge. I. Dominant bacteria. Appl Microbiol 12:412–417

    CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Gan HM, Hudson AO, Rahman AYA, Chan KG, Savka MA (2013) Comparative genomic analysis of six bacteria belonging to the genus Novosphingobium: insights into marine adaptation, cell-cell signaling and bioremediation. BMC Genomics 14:431

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Ghai R, Mizuno CM, Picazo A, Camacho A, Rodriguez-Valera F (2013) Metagenomics uncovers a new group of low GC and ultra-small marine Actinobacteria. Sci Rep 3:2471

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghiglione JF, Mevel G, Pujo-Pay M, Mousseau L, Lebaron P, Goutx M (2007) Diel and seasonal variations in abundance, activity, and community structure of particle-attached and free-living bacteria in NW Mediterranean Sea. Microb Ecol 54:217–231

    CAS  Article  PubMed  Google Scholar 

  • Gilbert JA, Steele JA, Caporaso JG, Steinbrück L, Reeder J, Temperton B, Huse S, McHardy AC, Knight R, Joint I, Somerfield P, Fuhrman JA, Field D (2012) Defining seasonal marine microbial community dynamics. ISME J 6:298–308

    CAS  Article  PubMed  Google Scholar 

  • Guo F, Ju F, Cai L, Zhang T (2013) Taxonomic precision of different hypervariable regions of 16S rRNA gene and annotation methods for functional bacterial groups in biological wastewater treatment. PLoS One 8(10):e76185

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Hahn MW (2009) Description of seven candidate species affiliated with the phylum Actinobacteria, representing planktonic freshwater bacteria. Int J Syst Evol Microbiol 59:112–117

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Hammer Ø, Harper D, Ryan P (2001) PAST: Paleontological Statistics Software Package for education and data analysis. Palaeontogia Electronica 4(1):1–9

    Google Scholar 

  • Hollibaugh JT, Wong PS, Murrell MC (2000) Similarity of particle-associated and free-living bacterial communities in northern San Francisco Bay, California. Aquat Microb Ecol 21:103–114

    Article  Google Scholar 

  • Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:1889–1898

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environl Microbiol 79:5112–5120

    CAS  Article  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environl Microbiol 71:8228–8235

    CAS  Article  Google Scholar 

  • Michotey V, Guasco S, Boeuf D, Morezzi N, Durieux B, Charpy L, Bonin P (2012) Spatio-temporal diversity of free-living and particle-attached prokaryotes in the tropical lagoon of Ahe atoll (Tuamotu Archipelago) and its surrounding oceanic waters. Mar Pollut Bull 65:525–537

    CAS  Article  PubMed  Google Scholar 

  • Mohit V, Archambault P, Toupoint N, Lovejoy C (2014) Phylogenetic differences in attached and free-living bacterial communities in a temperate coastal lagoon during summer, revealed via high-throughput 16S rRNA gene sequencing. Appl Environl Microbiol 80:2071–2083

    Article  Google Scholar 

  • Morris RM, Rappe MS, Connon SA, Vergin KL, Siebold WA, Carlson CA, Giovannoni SJ (2002) SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420:806–810

    CAS  Article  PubMed  Google Scholar 

  • Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environl Microbiol 59:695–700

    CAS  Google Scholar 

  • Parveen B, Reveilliez JP, Mary I, Ravet V, Bronner G, Mangot JF, Domaizon I, Debroas D (2011) Diversity and dynamics of free-living and particle-associated Betaproteobacteria and Actinobacteria in relation to phytoplankton and zooplankton communities. FEMS Microbiol Ecol 77:461–476

    CAS  Article  PubMed  Google Scholar 

  • Richardot M, Debroas D, Thouvenot A, Romagoux JC, Berthon JL, Devaux J (1999) Proteolytic and glycolytic activities in size-fractionated surface water samples from an oligotrophic reservoir in relation to plankton communities. Aquat Sci 61:279–292

    CAS  Article  Google Scholar 

  • Riemann L, Winding A (2001) Community dynamics of free-living and particle-associated bacterial assemblages during a freshwater phytoplankton bloom. Microbial Ecol 42:274–285

    CAS  Article  Google Scholar 

  • Rippy M, Franks P, Feddersen F, Guza R, Moore D (2013) Physical dynamics controlling variability in nearshore fecal pollution: fecal indicator bacteria as passive particles. Mar Pollut Bull 66:151–157

    CAS  Article  PubMed  Google Scholar 

  • Rizzo L, Manaia C, Merlin C, Schwartz T, Dagot C, Ploy MC, Michael I, Fatta-Kassinos D (2013) Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci Total Environ 447:345–360

    CAS  Article  PubMed  Google Scholar 

  • Rösel S, Grossart H-P (2012) Contrasting dynamics in activity and community composition of free-living and particle-associated bacteria in spring. Aquat Microb Ecol 66:169–181

    Article  Google Scholar 

  • Rosselló-Mora RA, Wagner M, Amann R, Schleifer KH (1995) The abundance of Zoogloea ramigera in sewage treatment plants. Appl Environ Microbiol 61:702–707

    PubMed  PubMed Central  Google Scholar 

  • Sánchez O, Gasol JM, Massana R, Mas J, Pedrós-Alió C (2007) Comparison of different denaturing gradient gel electrophoresis primer sets for the study of marine bacterioplankton communities. Appl Environl Microbiol 73:5962–5967

    Article  Google Scholar 

  • Sassoubre LM, Yamahara KM, Boehm AB (2015) Temporal stability of the microbial community in sewage-polluted seawater exposed to natural sunlight cycles and marine microbiota. Appl Environl Microbiol 81:2107–2116

    CAS  Article  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environl Microbiol 75:7537–7541

    CAS  Article  Google Scholar 

  • 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Simon M (1987) Biomass and production of small and large free living and attached bacteria in Lake Constance. Limnol Oceanogr 32:591–607

    CAS  Article  Google Scholar 

  • Stewart JR, Gast RJ, Fujioka RS, Solo-Gabriele HM, Meschke JS, Amaral-Zettler LA, Del Castillo E, Polz MF, Collier TK, Strom MS, Sinigalliano CD, Moeller PD, Holland AF (2008) The coastal environment and human health: microbial indicators, pathogens, sentinels and reservoirs. Environ Heal 7(Suppl 2):S3

    Article  Google Scholar 

  • Tam N (1998) Effects of wastewater discharge on microbial populations and enzyme activities in mangrove soils. Environ Pollut 102:233–242

    CAS  Article  Google Scholar 

  • Unanue M, Ayo B, Azúa I, Barcina I, Iriberri J (1992) Temporal variability of attached and free-living bacteria in coastal waters. Microb Ecol 23:27–39

    CAS  Article  PubMed  Google Scholar 

  • Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499

    CAS  Article  Google Scholar 

  • Wakelin SA, Colloff MJ, Kookana RS (2008) Effect of wastewater treatment plant effluent on microbial function and community structure in the sediment of a freshwater stream with variable seasonal flow. Appl Environl Microbiol 74:2659–2668

    CAS  Article  Google Scholar 

  • Wang G, Fan J, Wu H, Zhang X, Li G, Zhang H, Yang X, Ye F, Xiang W, Li X (2013) Nonhongiella spirulinensis gen. nov., sp. nov., a bacterium isolated from a cultivation pond of Spirulina platensis in Sanya, China. Antonie Van Leeuwenhoek 104:933–939

    CAS  Article  PubMed  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environl Microbiol 73:5261–5267

    CAS  Article  Google Scholar 

  • Wéry N, Monteil C, Pourcher AM, Godon JJ (2010) Human-specific fecal bacteria in wastewater treatment plant effluents. Water Res 44:1873–1883

    Article  PubMed  Google Scholar 

  • Xu H, Zhang W, Jiang Y, Yang EJ (2014) Use of biofilm-dwelling ciliate communities to determine environmental quality status of coastal waters. Sci Total Environ 470:511–518

    Article  PubMed  Google Scholar 

  • Yamahara KM, Sassoubre LM, Goodwin KD, Boehm AB (2012) Occurrence and persistence of bacterial pathogens and indicator organisms in beach sand along the California coast. Appl Environl Microbiol 78:1733–1745

    CAS  Article  Google Scholar 

  • Yan S, Fuchs BM, Lenk S, Harder J, Wulf J, Jiao NZ, Amann R (2009) Biogeography and phylogeny of the NOR5/OM60 clade of Gammaproteobacteria. Syst Appl Microbiol 32:124–139

    CAS  Article  PubMed  Google Scholar 

  • Zhang R, Liu B, Lau SC, Ki JS, Qian PY (2007) Particle-attached and free-living bacterial communities in a contrasting marine environment: Victoria Harbor, Hong Kong. FEMS Microbiol Ecol 61:496–508

    CAS  Article  PubMed  Google Scholar 

  • Zhang T, Shao MF, Ye L (2012) 454 Pyrosequencing reveals bacterial diversity of activated sludge from 14 sewage treatment plants. ISME J 6:1137–1147

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Projects of Public Science and Technology Research Funds of Ocean Sector of China (201205009), Research Project for Young Teachers of Fujian Province (JA14001), the Fundamental Research Funds for the Central Universities (2013121050), and Fujian Provincial Public Welfare Projects (2016R1101006-3).

Author information

Affiliations

  1. Fujian Provincial Key Laboratory of Coastal Ecology and Environmental Studies, Xiamen University & Fujian Institute of Oceanography, Xiamen, 361005, China

    SiGuang Liu, YuanRong Luo & LingFeng Huang

  2. Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, College of the Environment and Ecology, Xiamen University, Xiamen, 361005, China

    YuanRong Luo & LingFeng Huang

  3. Laboratory of Marine Chemistry, Fujian Institute of Oceanography, Xiamen, 361000, China

    SiGuang Liu

Authors
  1. SiGuang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. YuanRong Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. LingFeng Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to YuanRong Luo.

Ethics declarations

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

ESM 1

(PDF 291 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Liu, S., Luo, Y. & Huang, L. Dynamics of size-fractionated bacterial communities during the coastal dispersal of treated municipal effluents. Appl Microbiol Biotechnol 100, 5839–5848 (2016). https://doi.org/10.1007/s00253-016-7408-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-016-7408-9

Keywords

  • Bacterial indicator
  • Community structure
  • Diversity
  • Marine environment
  • Pollutant