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Global diversity and biogeography of bacterial communities in wastewater treatment plants

Nature Microbiology volume 4, pages 1183–1195 (2019)Cite this article

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An Author Correction to this article was published on 14 November 2019

This article has been updated

Abstract

Microorganisms in wastewater treatment plants (WWTPs) are essential for water purification to protect public and environmental health. However, the diversity of microorganisms and the factors that control it are poorly understood. Using a systematic global-sampling effort, we analysed the 16S ribosomal RNA gene sequences from ~1,200 activated sludge samples taken from 269 WWTPs in 23 countries on 6 continents. Our analyses revealed that the global activated sludge bacterial communities contain ~1 billion bacterial phylotypes with a Poisson lognormal diversity distribution. Despite this high diversity, activated sludge has a small, global core bacterial community (n = 28 operational taxonomic units) that is strongly linked to activated sludge performance. Meta-analyses with global datasets associate the activated sludge microbiomes most closely to freshwater populations. In contrast to macroorganism diversity, activated sludge bacterial communities show no latitudinal gradient. Furthermore, their spatial turnover is scale-dependent and appears to be largely driven by stochastic processes (dispersal and drift), although deterministic factors (temperature and organic input) are also important. Our findings enhance our mechanistic understanding of the global diversity and biogeography of activated sludge bacterial communities within a theoretical ecology framework and have important implications for microbial ecology and wastewater treatment processes.

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Fig. 1: The GWMC captures microbial diversity of globally distributed WWTPs.
Fig. 2: Abundance, composition and functional importance of the global core OTUs in activated sludge.
Fig. 3: Comparing bacterial community compositions across continents and with other habitats.
Fig. 4: Spatial turnover of the activated sludge bacterial communities.
Fig. 5: Environmental drivers of the activated sludge community composition.

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Data availability

The sample metadata are available in Supplementary Table 1. Sequences are available from the NCBI Sequence Read Archive with accession number PRJNA509305. OTU tables and representative sequences of the OTUs are available on the GWMC website (http://gwmc.ou.edu/data-disclose.html).

Code availability

R codes on the statistical analyses are available at https://github.com/Linwei-Wu/Global-bacterial-diversity-in-WWTPs.

Change history

  • 14 November 2019

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

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Acknowledgements

The authors thank T. Allen, A. Al-Omari, R. Bart, D. Crowley, G. Harwood, T. Hensley, S.-J. Huitric, M. M. L. Martins, A. Mena, B. Pathak, S. Pereira, D. E. Sauble, M. Taylor, P. Truong, D. VanderSchuur, A. Vieira and D. Zambrano for helping with sampling and metadata collection. This work was supported by the Tsinghua University Initiative Scientific Research Program (No. 20161080112), the National Scientific Foundation in China (51678335), the State Key Joint Laboratory of Environmental Simulation and Pollution Control (18L02ESPC) in China, and the Office of the Vice President for Research at the University of Oklahoma. Lin.W. and B.Z. were generously supported by the China Scholarship Council (CSC). J.Z. (jzhou@ou.edu) and D.N. (ningdaliang@ou.edu) serve as GWMC contacts.

Author information

Author notes

  1. These authors contributed equally: Linwei Wu, Daliang Ning, Bing Zhang.

  2. A full list of Global Water Microbiome Consortium members appears at the end of the paper.

Authors and Affiliations

  1. State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, China

    Linwei Wu, Daliang Ning, Bing Zhang, Xiaoyu Shan, Qiuting Zhang, Yunfeng Yang, Daliang Ning, Xiaoyu Shan, Linwei Wu, Yunfeng Yang, Haowei Yue, Bing Zhang, Qiuting Zhang, Jizhong Zhou, Xianghua Wen, Xianghua Wen & Jizhong Zhou

  2. Institute for Environmental Genomics, Department of Microbiology and Plant Biology, and School of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK, USA

    Linwei Wu, Daliang Ning, Bing Zhang, Ping Zhang, Joy D. Van Nostrand, Naijia Xiao, Ya Zhang, Lauren Hale, Daliang Ning, Renmao Tian, Joy D. Van Nostrand, Linwei Wu, Liyou Wu, Naijia Xiao, Bing Zhang, Ping Zhang, Ya Zhang, Jizhong Zhou & Jizhong Zhou

  3. Consolidated Core Laboratory, University of Oklahoma, Norman, OK, USA

    Daliang Ning, Naijia Xiao, Daliang Ning & Naijia Xiao

  4. College of Resource and Environment Southwest University, Chongqing, China

    Yong Li & Yong Li

  5. Alkek Center for Metagenomics and Microbiome Research, Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, TX, USA

    Ping Zhang & Ping Zhang

  6. School of Engineering, Newcastle University, Newcastle upon Tyne, UK

    Mathew Robert Brown, Mathew Robert Brown & Thomas P. Curtis

  7. School of Environment, Northeastern Normal University, Changchun, China

    Zhenxin Li & Zhenxin Li

  8. Department of Energy, Environmental and Chemical Engineering, Washington University in St Louis, St Louis, MO, USA

    Fangqiong Ling

  9. Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, Research Network ‘Chemistry meets Microbiology’, University of Vienna, Vienna, Austria

    Julia Vierheilig, Julia Vierheilig, Michael Wagner & Michael Wagner

  10. Karl Landsteiner University of Health Sciences, Division of Water Quality and Health, Krems, Austria and Interuniversity Cooperation Centre for Water and Health, Krems, Austria

    Julia Vierheilig & Julia Vierheilig

  11. Department of Civil and Environmental Engineering, Northwestern University, Evanston, IL, USA

    George F. Wells & George F. Wells

  12. Institute for Marine Science and Technology, Shandong University, Qingdao, China

    Ye Deng, Qichao Tu, Ye Deng & Qichao Tu

  13. Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, China

    Ye Deng, Aijie Wang & Aijie Wang

  14. Environmental Biotechnology Laboratory, The University of Hong Kong, Hong Kong, China

    Tong Zhang & Tong Zhang

  15. Environmental Microbiomics Research Center, School of Environmental Science and Engineering, Sun Yat-Sen University, Guangzhou, China

    Zhili He & Zhili He

  16. Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology, Guangzhou, China

    Zhili He & Zhili He

  17. Advanced Water Management Centre, The University of Queensland, Brisbane, Queensland, Australia

    Miriam Agullo-Barcelo, Philip Bond, Jurg Keller & Jurg Keller

  18. Department of Chemistry and Bioscience, Center for Microbial Communities, Aalborg University, Aalborg, Denmark

    Per H. Nielsen & Per H. Nielsen

  19. Department of Civil and Environmental Engineering, Rice University, Houston, TX, USA

    Pedro J. J. Alvarez, Mengyan Li & Pedro J. J. Alvarez

  20. Department of Civil and Environmental Engineering, Stanford University, Stanford, CA, USA

    Craig S. Criddle, Richard G. Luthy, Sung-Geun Woo & Craig S. Criddle

  21. Center for Microbial Ecology, Michigan State University, East Lansing, MI, USA

    James M. Tiedje & James M. Tiedje

  22. Department of Civil and Environmental Engineering, The University of Tennessee, Knoxville, TN, USA

    Si Chen, Qiang He & Qiang He

  23. Institute for a Secure and Sustainable Environment, The University of Tennessee, Knoxville, TN, USA

    Qiang He & Qiang He

  24. Department of Civil and Environmental Engineering, University of Washington, Seattle, WA, USA

    David A. Stahl & David A. Stahl

  25. Department of Civil and Environmental Engineering, College of Engineering, University of California, Berkeley, CA, USA

    Lisa Alvarez-Cohen & Lisa Alvarez-Cohen

  26. Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

    Lisa Alvarez-Cohen, Lisa Alvarez-Cohen & Jizhong Zhou

  27. Biodesign Swette Center for Environmental Biotechnology, Arizona State University, Tempe, AZ, USA

    Prathap Parameswaran, Bruce E. Rittmann, Michelle Young & Bruce E. Rittmann

  28. Environmental Microbiology and Biotechnology Laboratory, Engineering School of Environmental and Natural Resources, Engineering Faculty, Universidad del Valle–Sede Meléndez, Cali, Colombia

    Dany Acevedo & Janeth Sanabria

  29. Department of Environmental Science, Policy, and Management, University of California, Berkeley, CA, USA

    Gary L. Andersen

  30. Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

    Gary L. Andersen

  31. Universidade Federal de Minas Gerais, Departamento de Engenharia Sanitária e Ambiental, Belo Horizonte, Brazil

    Juliana Calabria de Araujo, Cintia Dutra Leal & Jizhong Zhou

  32. Department of Environmental Health Sciences, The University of Michigan, Ann Arbor, MI, USA

    Kevin F. Boehnke, Rebecca K. Brewster & Chuanwu Xi

  33. Hampton Roads Sanitation District (HRSD), Virginia Beach, VA, USA

    Charles B. Bott & Amanda Ford

  34. Microbial Ecology Laboratory, Microbial Biochemistry and Genomics Department, Biological Research Institute “Clemente Estable”, Montevideo, Uruguay

    Patricia Bovio, Angela Cabezas, Claudia Etchebehere & Thomas P. Curtis

  35. Institute of Water and Wastewater Technology, Durban University of Technology, Durban, South Africa

    Faizal Bux & Sheena Kumari

  36. Aix-Marseille University CNRS IRD, MIO UM110 Mediterranean Institute of Oceanography, Marseille, France

    Léa Cabrol

  37. Escuela de Ingenieria Bioquimica, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile

    Léa Cabrol

  38. Microbial Community Engineering Laboratory, Department of Civil Engineering and Applied Mechanics, McGill University, Montreal, Québec, Canada

    Dominic Frigon & Shameem Jauffur

  39. Department of Chemical and Biological Engineering, Northwestern University, Evanston, IL, USA

    James S. Griffin

  40. School of Civil and Environmental Engineering, Cornell University, Ithaca, NY, USA

    April Z. Gu

  41. Vatten and Miljö i Väst AB (VIVAB), Falkenberg, Sweden

    Moshe Habagil & Alexander Keucken

  42. Norman Water Reclamation Facility, Norman, OK, USA

    Steven D. Hardeman

  43. Golden Heart Utilities, Fairbanks, AK, USA

    Marc Harmon

  44. Karlsruhe Institute of Technology, Engler-Bunte-Institut, Water Chemistry and Water Technology, Karlsruhe, Germany

    Harald Horn & Stephanie West

  45. Department of Civil and Environmental Engineering, University of Missouri, Columbia, MO, USA

    Zhiqiang Hu

  46. Department of Building, Civil and Environmental Engineering, Concordia University, Montreal, Québec, Canada

    Shameem Jauffur

  47. Department of Environmental Microbiology, Eawag, Dübendorf, Switzerland

    David R. Johnson & Deborah Patsch

  48. Water Resources Engineering, Faculty of Engineering, Lund University, Lund, Sweden

    Alexander Keucken

  49. Luxembourg Centre for Systems Biomedicine, University of Luxembourg, Belvaux, Luxembourg

    Laura A. Lebrun & Paul Wilmes

  50. Department of Civil and Environmental Engineering, Yonsei University, Seoul, South Korea

    Jangho Lee, Minjoo Lee & Joonhong Park

  51. Advanced Environmental Biotechnology Centre, Nanyang Environment and Water Research Institute, Nanyang Technological University, Singapore, Singapore

    Zarraz M. P. Lee & Yu Liu

  52. Department of Civil Engineering, University of Nebraska, Lincoln, NE, USA

    Xu Li & Amin Mohebbi

  53. Infrastructure and Environment Research Division, School of Engineering, University of Glasgow, Glasgow, UK

    Fangqiong Ling & William T. Sloan

  54. School of Civil and Environmental Engineering, Nanyang Technological University, Singapore, Singapore

    Yu Liu

  55. Plant Biotechnology Program, Federal University of Rio de Janeiro, UFRJ, Rio de Janeiro, Brazil

    Leda C. Mendonça-Hagler

  56. Federal University of Ceará, UFC, Ceará, Brazil

    Francisca Gleire Rodriguez de Menezes & Oscarina Viana de Sousa

  57. University of Tennessee, Center for Environmental Biotechnology, Knoxville, TN, USA

    Arthur J. Meyers

  58. Department of Civil Engineering, Construction Management and Environmental Engineering, Northern Arizona University, Flagstaff, AZ, USA

    Amin Mohebbi

  59. UCIBIO, REQUIMTE, Departamento de Química, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal

    Adrian Oehmen

  60. CSIRO Land and Water, Ecosciences Precinct, Dutton Park, Queensland, Australia

    Andrew Palmer, Jatinder Sidhu & Kylie Smith

  61. Departamento de Química, Universidade de São Paulo, Faculdade de Filosofia Ciências e Letras de Ribeirão Preto—FFCLRP, Ribeirão Preto, Brazil

    Valeria Reginatto

  62. Department of Civil, Construction, and Environmental Engineering, North Carolina State University, Raleigh, NC, USA

    Francis L. de los Reyes III & Joseph E. Weaver

  63. Grupo de Investigación en Procesos Anaerobios, Instituto de Ingeniería, Universidad Nacional Autónoma de México, México, Mexico

    Adalberto Noyola & Daniel De los Cobos Vasconcelos

  64. CNR-IRSA, National Research Council, Water Research Institute, Rome, Italy

    Simona Rossetti

  65. Tryon Creek and Columbia Blvd Wastewater Treatment Plants, Bureau of Environmental Services, City of Portland, OR, USA

    Kyle Stephens

  66. Department of Civil and Environmental Engineering, Northeastern University, Boston, MA, USA

    Nicholas B. Tooker

  67. Scion Research, Christchurch, New Zealand

    Steve Wakelin

  68. School of Engineering, University of Guelph, Guelph, Ontario, Canada

    Bei Wang & Hongde Zhou

  69. Department of Environmental Engineering, National Cheng Kung University, Tainan City, China

    Jer-Horng Wu

  70. State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Institute of Microbiology, Guangzhou, China

    Meiying Xu

  71. Department of Civil and Environmental Engineering, University of Hawaii at Manoa, Honolulu, HI, USA

    Tao Yan & Qian Zhang

  72. State Key Laboratory of Environmental Aquatic Chemistry, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, China

    Min Yang & Yu Zhang

  73. Department of Civil Engineering, University of Arkansas, Fayetteville, AR, USA

    Wen Zhang

Authors
  1. Linwei Wu
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  2. Daliang Ning
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  3. Bing Zhang
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  4. Yong Li
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  5. Ping Zhang
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  6. Xiaoyu Shan
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  7. Qiuting Zhang
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  8. Mathew Robert Brown
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  9. Zhenxin Li
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  10. Joy D. Van Nostrand
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  11. Fangqiong Ling
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  12. Naijia Xiao
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  13. Ya Zhang
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  14. Julia Vierheilig
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  15. George F. Wells
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  16. Yunfeng Yang
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  17. Ye Deng
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  18. Qichao Tu
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  19. Aijie Wang
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  20. Tong Zhang
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  21. Zhili He
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  22. Jurg Keller
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  23. Per H. Nielsen
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  24. Pedro J. J. Alvarez
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  25. Craig S. Criddle
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  26. Michael Wagner
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  27. James M. Tiedje
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  28. Qiang He
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  29. Thomas P. Curtis
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  30. David A. Stahl
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  31. Lisa Alvarez-Cohen
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  32. Bruce E. Rittmann
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  33. Xianghua Wen
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  34. Jizhong Zhou
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Consortia

Global Water Microbiome Consortium

  • Dany Acevedo
  • , Miriam Agullo-Barcelo
  • , Pedro J. J. Alvarez
  • , Lisa Alvarez-Cohen
  • , Gary L. Andersen
  • , Juliana Calabria de Araujo
  • , Kevin F. Boehnke
  • , Philip Bond
  • , Charles B. Bott
  • , Patricia Bovio
  • , Rebecca K. Brewster
  • , Faizal Bux
  • , Angela Cabezas
  • , Léa Cabrol
  • , Si Chen
  • , Craig S. Criddle
  • , Ye Deng
  • , Claudia Etchebehere
  • , Amanda Ford
  • , Dominic Frigon
  • , Janeth Sanabria
  • , James S. Griffin
  • , April Z. Gu
  • , Moshe Habagil
  • , Lauren Hale
  • , Steven D. Hardeman
  • , Marc Harmon
  • , Harald Horn
  • , Zhiqiang Hu
  • , Shameem Jauffur
  • , David R. Johnson
  • , Jurg Keller
  • , Alexander Keucken
  • , Sheena Kumari
  • , Cintia Dutra Leal
  • , Laura A. Lebrun
  • , Jangho Lee
  • , Minjoo Lee
  • , Zarraz M. P. Lee
  • , Yong Li
  • , Zhenxin Li
  • , Mengyan Li
  • , Xu Li
  • , Fangqiong Ling
  • , Yu Liu
  • , Richard G. Luthy
  • , Leda C. Mendonça-Hagler
  • , Francisca Gleire Rodriguez de Menezes
  • , Arthur J. Meyers
  • , Amin Mohebbi
  • , Per H. Nielsen
  • , Daliang Ning
  • , Adrian Oehmen
  • , Andrew Palmer
  • , Prathap Parameswaran
  • , Joonhong Park
  • , Deborah Patsch
  • , Valeria Reginatto
  • , Francis L. de los Reyes III
  • , Bruce E. Rittmann
  • , Adalberto Noyola
  • , Simona Rossetti
  • , Xiaoyu Shan
  • , Jatinder Sidhu
  • , William T. Sloan
  • , Kylie Smith
  • , Oscarina Viana de Sousa
  • , David A. Stahl
  • , Kyle Stephens
  • , Renmao Tian
  • , James M. Tiedje
  • , Nicholas B. Tooker
  • , Qichao Tu
  • , Joy D. Van Nostrand
  • , Daniel De los Cobos Vasconcelos
  • , Julia Vierheilig
  • , Michael Wagner
  • , Steve Wakelin
  • , Aijie Wang
  • , Bei Wang
  • , Joseph E. Weaver
  • , George F. Wells
  • , Stephanie West
  • , Paul Wilmes
  • , Sung-Geun Woo
  • , Linwei Wu
  • , Jer-Horng Wu
  • , Liyou Wu
  • , Chuanwu Xi
  • , Naijia Xiao
  • , Meiying Xu
  • , Tao Yan
  • , Yunfeng Yang
  • , Min Yang
  • , Michelle Young
  • , Haowei Yue
  • , Bing Zhang
  • , Ping Zhang
  • , Qiuting Zhang
  • , Ya Zhang
  • , Tong Zhang
  • , Qian Zhang
  • , Wen Zhang
  • , Yu Zhang
  • , Hongde Zhou
  • , Jizhong Zhou
  • , Xianghua Wen
  • , Thomas P. Curtis
  • , Qiang He
  • , Zhili He
  •  & Mathew Robert Brown

Contributions

All authors contributed experimental assistance and intellectual input to this study. The original concept was conceived by J.Z. Experimental strategies and sampling design were developed by J.Z., X.W., T.P.C., Q.H., Z. He. and D.N. Sample collections were coordinated by Q.H., D.N., X.W., T.P.C., B.Z., M.R.B., G.F.W., J.Z. and other GWMC members. J.D.V.N and D.N. managed shipping. Y. Li., B.Z., ZX.L., D.N. and some GWMC members (F.B., S.K., J.V., A.N., D.D.C.V., C.E., L.C., J.C.A., C.D.L., L.C.M-H., A.C., P. Bovio. and D.A.) did DNA extraction. P.Z. performed DNA sequencing with the help from Liy.W. Data analyses were performed by Lin.W., D.N., J.Z., B.Z., X.S., Q.Z., F.L., N.X. and R.T. with help from Y.D., Q.T., T.Z., Ya.Z and A.W. The manuscript was written by Lin.W., J.Z. and D.N. with the help from B.E.R., L.A.-C., M.W., C.S.C., D.A.S., G.F.W., J.M.T., P.J.J.A., J.K., J.V., P.H.N., R.G.L., X.W., Z. He. and Y.Y.

Corresponding authors

Correspondence to Qiang He, Thomas P. Curtis, Xianghua Wen or Jizhong Zhou.

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Competing interests

The authors declare no competing interests.

Additional information

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Supplementary information

Supplementary Information

Supplementary Figures 1–7, Supplementary Table 2, Supplementary Tables 4–10, Supplementary Table 13 and Supplementary References.

Reporting Summary

Supplementary Table 1

Summary of metadata.

Supplementary Table 3

OTUs identified as core community at the global scale or within each continent.

Supplementary Table 11

Diversity of Nitrosomonas species across WWTPs.

Supplementary Table 12

The diversity of Candidatus Accumulimonas, Candidatus Accumulibacter and Tetrasphaera species across WWTPs.

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Wu, L., Ning, D., Zhang, B. et al. Global diversity and biogeography of bacterial communities in wastewater treatment plants. Nat Microbiol 4, 1183–1195 (2019). https://doi.org/10.1038/s41564-019-0426-5

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