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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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.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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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.

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 Brown
    • , Matthew 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 Gómez
  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 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 Robles
    •  & 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

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Consortia

  1. Global Water Microbiome Consortium

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.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.R., 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.

Competing interests

The authors declare no competing interests.

Corresponding authors

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

Supplementary information

  1. Supplementary Information

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

  2. Reporting Summary

  3. Supplementary Table 1

    Summary of metadata.

  4. Supplementary Table 3

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

  5. Supplementary Table 11

    Diversity of Nitrosomonas species across WWTPs.

  6. Supplementary Table 12

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

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/s41564-019-0426-5