Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Universal microbial indicators provide surveillance of sewage contamination in harbours worldwide

Nature Water volume 2, pages 1061–1070 (2024)Cite this article

Subjects

Abstract

Human population pressures and activities pose unprecedented challenges to water resources in urban environments. However, standard methods of assessing microbial water quality have relied on the same cultured organisms for decades. We show that there is a conserved microbial assemblage in untreated sewage that can be exploited to improve global sewage surveillance. Among harbour and coastal water samples from 18 cities across 5 continents (n = 442), nearly half had evidence of sewage contamination using two human faecal bacteria as molecular indicators. In contrast, conventional measures using cultured Escherichia coli or enterococci only exceeded water quality limits in ~18% of samples, with less than half of these demonstrating sewage indicators. Contaminated locations also displayed a signature characteristic of microorganisms mainly derived from sewer infrastructure. Given the human health risk, loss of ecosystem services and economic costs associated with contaminated coastal waters, molecular approaches could provide more reliable information on sewage contamination of urban waterways.

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

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to the full article PDF.

USD 39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Study cities and levels of human Bacteroides measured by the HF183 marker.
Fig. 2: A radial network analysis of the most abundant sewage ASVs detected in city harbour waters.

Similar content being viewed by others

Data availability

Sequencing data are available in NCBI Bioproject no. PRJNA691369. The dataset of qPCR and culture results is available via Figshare at https://doi.org/10.6084/m9.figshare.24757185 (ref. 83).

References

  1. Martínez, M. L. et al. The coasts of our world: Ecological, economic and social importance. Ecol. Econ. 63, 254–272 (2007).

    Article  Google Scholar 

  2. Tuholske, C. et al. Mapping global inputs and impacts from of human sewage in coastal ecosystems. PLoS ONE 16, 1–16 (2021).

    Article  Google Scholar 

  3. Landrigan, P. J. et al. Human health and ocean pollution. Ann. Glob. Heal. 86, 151 (2020).

    Article  Google Scholar 

  4. Mora, C. et al. Over half of known human pathogenic diseases can be aggravated by climate change. Nat. Clim. Chang. 12, 869–875 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  5. Wear, S. L., Acuña, V., McDonald, R. & Font, C. Sewage pollution, declining ecosystem health, and cross-sector collaboration. Biol. Conserv. 255, 109010 (2021).

    Article  Google Scholar 

  6. Ferrario, F. et al. The effectiveness of coral reefs for coastal hazard risk reduction and adaptation. Nat. Commun. 5, 3794 (2014).

    Article  CAS  PubMed  Google Scholar 

  7. Olds, H. T. et al. High levels of sewage contamination released from urban areas after storm events: a quantitative survey with sewage specific bacterial indicators. PLoS Med. 15, e1002614 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  8. Korajkic, A., McMinn, B. R. & Harwood, V. J. Relationships between microbial indicators and pathogens in recreational water settings. Int. J. Environ. Res. Public Health 15, 2842 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. United States Environmental Protection Agency. Recreational Water Quality Criteria. Office of Water 820-F-12-058 (USEPA, 2012).

  10. World Health Organisation. Guidelines on Recreational Water Quality: Vol 1 Coastal and Fresh Waters. Licence: CC BY-NC-SA 3.0 IGO (World Health Organisation, 2021).

  11. McLellan, S. L. & Eren, A. M. Discovering new indicators of fecal pollution. Trends Microbiol. 22, 697–706 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Holcomb, D. A. & Stewart, J. R. Microbial indicators of fecal pollution: Recent progress and challenges in assessing water quality. Curr. Environ. Heal. Reports 7, 311–324 (2020).

    Article  Google Scholar 

  13. Ballesté, E. & Blanch, A. R. Persistence of Bacteroides species populations in a river as measured by molecular and culture techniques. Appl. Environ. Microbiol. 76, 7608–7616 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Walters, S. P., Yamahara, K. M. & Boehm, A. B. Persistence of nucleic acid markers of health-relevant organisms in seawater microcosms: implications for their use in assessing risk in recreational waters. Water Res. 43, 4929–4939 (2009).

    Article  CAS  PubMed  Google Scholar 

  15. Mayer, R. E. et al. Occurrence of human-associated Bacteroidetes genetic source tracking markers in raw and treated wastewater of municipal and domestic origin and comparison to standard and alternative indicators of faecal pollution. Water Res. 90, 265–276 (2016).

    Article  CAS  PubMed  Google Scholar 

  16. Lobos, A. E. et al. Persistence of sewage-associated genetic markers in advanced and conventional treated recycled water: implications for microbial source tracking in surface waters. mBio https://doi.org/10.1128/mbio.00655-24 (2024).

  17. Staley, Z. R., Boyd, R. J., Shum, P. & Edge, T. A. Microbial source tracking using quantitative and digital PCR to identify sources of fecal contamination in stormwater, river water, and beach water in a Great Lakes area of concern. Appl. Environ. Microbiol. 84, e01634–18 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Roguet, A., Eren, A. M., Newton, R. J. & McLellan, S. L. Fecal source identification using random forest. Microbiome 6, 185 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Unno, T. et al. Fecal pollution: new trends and challenges in microbial source tracking using next-generation sequencing. Environ. Microbiol. 20, 3132–3140 (2018).

    Article  PubMed  Google Scholar 

  20. Luna, G. M., Quero, G. M. & Perini, L. Next generation sequencing reveals distinct fecal pollution signatures in aquatic sediments across gradients of anthropogenic influence. Adv. Oceanogr. Limnol. 7, 115–124 (2016).

    Article  CAS  Google Scholar 

  21. Brown, C. M. et al. A high-throughput DNA-sequencing approach for determining sources of fecal bacteria in a Lake Superior estuary. Environ. Sci. Technol. 51, 8263–8271 (2017).

    Article  CAS  PubMed  Google Scholar 

  22. Lindner, B. G. et al. Toward shotgun metagenomic approaches for microbial source tracking sewage spills based on laboratory mesocosms. Water Res. 210, 117993 (2022).

    Article  CAS  PubMed  Google Scholar 

  23. Roguet, A., Newton, R. J., Eren, A. M. & McLellan, S. L. Guts of the urban ecosystem: microbial ecology of sewer infrastructure. mSystems 7, e00118–e00122 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Vandewalle, J. L. et al. Acinetobacter, Aeromonas and Trichococcus populations dominate the microbial community within urban sewer infrastructure. Environ. Microbiol. 14, 2538–2552 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Steinberg, P., Airoldi, L., Banks, J. & Leung, K. Introduction to the special issue on the World Harbour Project. Reg. Stud. Mar. Sci. 8, 217–219 (2016).

    Google Scholar 

  26. Tanner, E. L., Steinberg, P. D., Soares-Gomes, A. & Leung, K. M. Y. Introduction to the World Harbour Project Special Issue Part II—global harbours and ports: different locations, similar problems? Reg. Stud. Mar. Sci. 33, 100904 (2020).

    Google Scholar 

  27. United States Environmental Protection Agency. Method 1603: Escherichia coli (E. coli) in Water by Membrane Filtration Using Modified Membrane-Thermotolerant Escherichia coli Agar (Modified mTEC). Office of Water EPA-821-R-09-007 (USEPA, 2009).

  28. United States Environmental Protection Agency. Method 1600: Enterococci in Water by Membrane Filtration Using Membrane-Enterococcus Indoxyl-β-d-Glucoside Agar (mEI). Office of Water EPA-821-R-09-016 (USEPA, 2009).

  29. Templar, H. A., Dila, D. K., Bootsma, M. J., Corsi, S. R. & McLellan, S. L. Quantification of human-associated fecal indicators reveal sewage from urban watersheds as a source of pollution to Lake Michigan. Water Res. 100, 556–567 (2016).

    Article  CAS  PubMed  Google Scholar 

  30. Bernhard, A. E. & Field, K. G. A PCR assay to discriminate human and ruminant feces on the basis of host differences in Bacteroides–Prevotella genes encoding 16S rRNA. Appl. Environ. Microbiol. 66, 4571–4574 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Feng, S., Bootsma, M. & McLellan, S. L. Human-associated Lachnospiraceae genetic markers improve detection of fecal pollution sources in urban waters. Appl. Environ. Microbiol. 84, 1e00309–18 (2018).

    Article  Google Scholar 

  32. Xu, Z. & Knight, R. Dietary effects on human gut microbiome diversity. Br. J. Nutr. 113, S1–S5 (2015).

    Article  CAS  PubMed  Google Scholar 

  33. Zafar, H. & Saier, M. H. Gut Bacteroides species in health and disease. Gut Microbes 13, 1–20 (2021).

    Article  PubMed  Google Scholar 

  34. Gupta, V. K., Paul, S. & Dutta, C. Geography, ethnicity or subsistence-specific variations in human microbiome composition and diversity. Front. Microbiol. 8, 1162 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Newton, R. J. et al. Sewage reflects the microbiomes of human populations. mBio 6, e02574–14 (2015).

    Google Scholar 

  36. Wéry, N., Lhoutellier, C., Ducray, F., Delgenès, J. P. & Godon, J. J. Behaviour of pathogenic and indicator bacteria during urban wastewater treatment and sludge composting, as revealed by quantitative PCR. Water Res. 42, 53–62 (2008).

    Article  PubMed  Google Scholar 

  37. Srinivasan, S., Aslan, A., Xagoraraki, I., Alocilja, E. & Rose, J. B. Escherichia coli, enterococci and Bacteroides thetaiotaomicron qPCR signals through wastewater and septage treatment. Water Res. 45, 2561–2572 (2011).

    Article  CAS  PubMed  Google Scholar 

  38. Viau, E. & Peccia, J. Evaluation of the enterococci indicator in biosolids using culture-based and quantitative PCR assays. Water Res. 43, 4878–4887 (2009).

    Article  CAS  PubMed  Google Scholar 

  39. Ahmed, W., Gyawali, P., Feng, S. & McLellan, S. L. Host specificity and sensitivity of established and novel sewage-associated marker genes in human and nonhuman fecal samples. Appl. Environ. Microbiol. 14, e00641–19 (2019).

    Google Scholar 

  40. Feng, S., Ahmed, W. & McLellan, S. L. Ecological and technical mechanisms for cross reaction of human fecal indicators with animal hosts. Appl. Environ. Microbiol. 86, e02319 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Eichmiller, J. J., Hicks, R. E. & Sadowsky, M. J. Distribution of genetic markers of fecal pollution on a freshwater sandy shoreline in proximity to wastewater effluent. Environ. Sci. Technol. 47, 3395–3402 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Kay, D. et al. Faecal indicator organism concentrations in sewage and treated effluents. Water Res. 42, 442–454 (2008).

    Article  CAS  PubMed  Google Scholar 

  43. Teixeira, P. et al. Bacteroides spp. and traditional fecal indicator bacteria in water quality assessment—an integrated approach for hydric resources management in urban centers. J. Environ. Manage. 271, 110989 (2020).

    Article  PubMed  Google Scholar 

  44. United States Environmental Protection Agency. Report to Congress Impacts and Control of CSOs and SSOs. Office of Water EPA 833-R-04-001 (USEPA, 2004).

  45. Drury, B., Rosi-Marshall, E. & Kelly, J. J. Wastewater treatment effluent reduces the abundance and diversity of benthic bacterial communities in urban and suburban rivers. Appl. Environ. Microbiol. 79, 1897–1905 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Chu, B. T. T. et al. Metagenomics reveals the impact of wastewater treatment plants on the dispersal of microorganisms and genes in aquatic sediments. Appl. Environ. Microbiol. 84, e02168–17 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  47. Kitajima, M., Iker, B. C., Pepper, I. L. & Gerba, C. P. Relative abundance and treatment reduction of viruses during wastewater treatment processes—identification of potential viral indicators. Sci. Total Environ. 488–489, 290–296 (2014).

    Article  PubMed  Google Scholar 

  48. Lin, A. Y. C., Yu, T. H. & Lateef, S. K. Removal of pharmaceuticals in secondary wastewater treatment processes in Taiwan. J. Hazard. Mater. 167, 1163–1169 (2009).

    Article  CAS  PubMed  Google Scholar 

  49. Rogowska, J., Cieszynska-Semenowicz, M., Ratajczyk, W. & Wolska, L. Micropollutants in treated wastewater. Ambio 49, 487–503 (2020).

    Article  PubMed  Google Scholar 

  50. Codello, A. et al. A weight-of-evidence approach for identifying potential sources of untreated sewage inputs into a complex urbanized catchment. Environ. Pollut. 275, 116575 (2021).

    Article  CAS  PubMed  Google Scholar 

  51. Brumfield, K. D. et al. Metagenomic sequencing and quantitative real-time PCR for fecal pollution assessment in an urban watershed. Front. Water https://doi.org/10.3389/frwa.2021.626849 (2021).

  52. Mattioli, M. C., Sassoubre, L. M., Russell, T. L. & Boehm, A. B. Decay of sewage-sourced microbial source tracking markers and fecal indicator bacteria in marine waters. Water Res. 108, 106–114 (2017).

    Article  CAS  PubMed  Google Scholar 

  53. Dila, D. K. et al. Assessment of regional and local sources of contamination at urban beaches using hydrodynamic models and field-based monitoring. ES&T Water 2, 1715–1724 (2022).

    Article  CAS  Google Scholar 

  54. Goodwin, K. D., Schriewer, A., Jirik, A., Curtis, K. & Crumpacker, A. Consideration of natural sources in a bacteria TMDL—lines of evidence, including beach microbial source tracking. Environ. Sci. Technol. 51, 7775–7784 (2017).

    Article  CAS  PubMed  Google Scholar 

  55. McLellan, S. L., Huse, S. M., Mueller-Spitz, S. R., Andreishcheva, E. N. & Sogin, M. L. Diversity and population structure of sewage-derived microorganisms in wastewater treatment plant influent. Environ. Microbiol. 12, 378–392 (2010).

    Article  CAS  PubMed  Google Scholar 

  56. LaMartina, E. L., Mohaimani, A. A. & Newton, R. J. Urban wastewater bacterial communities assemble into seasonal steady states. Microbiome 9, 116 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. McLellan, S. L. et al. Sewage reflects the distribution of human faecal Lachnospiraceae. Environ. Microbiol. 15, 2213–2227 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. McLellan, S. L. & Roguet, A. The unexpected habitat in sewer pipes for the propagation of microbial communities and their imprint on urban waters. Curr. Opin. Biotechnol. 57, 34–41 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Feng, S. & McLellan, S. L. Highly specific sewage-derived Bacteroides quantitative PCR assays target sewage-polluted waters. Appl. Environ. Microbiol. 85, e02696–18 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Newton, R. J., Bootsma, M. J., Morrison, H. G., Sogin, M. L. & McLellan, S. L. A microbial signature approach to identify fecal pollution in the waters off an urbanized coast of Lake Michigan. Microb. Ecol. 65, 1011–1023 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Vadde, K. K., Feng, Q., Wang, J., McCarthy, A. J. & Sekar, R. Next-generation sequencing reveals fecal contamination and potentially pathogenic bacteria in a major inflow river of Taihu Lake. Environ. Pollut. 254, 113108 (2019).

    Article  CAS  PubMed  Google Scholar 

  62. An, X. L. et al. High-throughput diagnosis of human pathogens and fecal contamination in marine recreational water. Environ. Res. 190, 109982 (2020).

    Article  CAS  PubMed  Google Scholar 

  63. Larsen, T. A., Hoffmann, S., Lüthi, C., Truffer, B. & Maurer, M. Emerging solutions to the water challenges of an urbanizing world. Science 352, 928–933 (2016).

    Article  CAS  PubMed  Google Scholar 

  64. Newton, R. J. & McClary, J. S. The flux and impact of wastewater infrastructure microorganisms on human and ecosystem health. Curr. Opin. Biotechnol. 57, 145–150 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Reischer, G. H., Kasper, D. C., Steinborn, R., Mach, R. L. & Farnleitner, A. H. Quantitative PCR method for sensitive detection of ruminant fecal pollution in freshwater and evaluation of this method in alpine karstic regions. Appl. Environ. Microbiol. 72, 5610–5614 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Boehm, A. B. et al. Performance of forty-one microbial source tracking methods: a twenty-seven lab evaluation study. Water Res. 47, 6812–6828 (2013).

    Article  CAS  PubMed  Google Scholar 

  67. Zhang, Y., Wu, R., Lin, K., Wang, Y. & Lu, J. Performance of host-associated genetic markers for microbial source tracking in China. Water Res. 175, 115670 (2020).

    Article  CAS  PubMed  Google Scholar 

  68. Boukerb, A. M. et al. Comparative analysis of fecal microbiomes from wild waterbirds to poultry, cattle, pigs, and wastewater treatment plants for a microbial source tracking approach. Front. Microbiol. https://doi.org/10.3389/fmicb.2021.697553 (2021).

  69. Ballesté, E. et al. Implementation and integration of microbial source tracking in a river watershed monitoring plan. Sci. Total Environ. 736, 139573 (2020).

    Article  PubMed  Google Scholar 

  70. Mathai, P. P., Staley, C. & Sadowsky, M. J. Sequence-enabled community-based microbial source tracking in surface waters using machine learning classification: A review. J. Microbiol. Methods 177, 106050 (2020).

    Article  CAS  PubMed  Google Scholar 

  71. Raza, S., Kim, J., Sadowsky, M. J. & Unno, T. Microbial source tracking using metagenomics and other new technologies. J. Microbiol. 59, 259–269 (2021).

    Article  PubMed  Google Scholar 

  72. Tan, B. F. et al. Next-generation sequencing (NGS) for assessment of microbial water quality: current progress, challenges, and future opportunities. Front. Microbiol. 6, 1027 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  73. McClary-Gutierrez, J. S. et al. SARS-CoV-2 wastewater surveillance for public health action. Emerg. Infect. Dis. 27, 1–8 (2021).

    Article  PubMed  Google Scholar 

  74. Safford, H. R., Shapiro, K. & Bischel, H. N. Wastewater analysis can be a powerful public health tool—if it’s done sensibly. Proc. Natl Acad. Sci. USA 119, e2119600119 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Roguet, A., Esen, Ö. C., Eren, A. M., Newton, R. J. & McLellan, S. L. FORENSIC: an online platform for fecal source identification. mSystems 5, e00869-19 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  76. Demeter, K. et al. Have genetic targets for faecal pollution diagnostics and source tracking revolutionized water quality analysis yet? FEMS Microbiol. Rev. 47, fuad028 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. United States Environmental Protection Agency. Method 1611: Enterococci in Water by TaqMan® Quantitative Polymerase Chain Reaction (qPCR) Assay. Office of Water EPA-821-R-12-008 (USEPA, 2012).

  78. Sauer, E. P., Vandewalle, J. L., Bootsma, M. J. & McLellan, S. L. Detection of the human specific Bacteroides genetic marker provides evidence of widespread sewage contamination of stormwater in the urban environment. Water Res. 45, 4081–4091 (2011).

    Article  CAS  PubMed  Google Scholar 

  79. Dila, D. K. et al. Patterns of host-associated fecal indicators driven by hydrology, precipitation, and land use attributes in Great Lakes watersheds. Environ. Sci. Technol. 52, 11500–11509 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Li, J., McLellan, S. & Ogawa, S. Accumulation and fate of green fluorescent labeled Escherichia coli in laboratory-scale drinking water biofilters. Water Res. 40, 3023–3028 (2006).

    Article  CAS  PubMed  Google Scholar 

  81. Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Zuur, A. F., Ieno, E. N. & Elphick, C. S. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1, 3–14 (2010).

    Article  Google Scholar 

  83. McLellan, S. L. World Harbour Project water sample data. Figshare https://doi.org/10.6084/m9.figshare.24757185.v1 (2023).

Download references

Acknowledgements

We thank M. Bootsma from the School of Freshwater Sciences at the University of Wisconsin-Milwaukee for technical assistance with conducting qPCR on all samples. This study was part of the World Harbour Project (WHP). Support to the Sydney Institute of Marine Science for the WHP from The Ian Potter Foundation, The New South Wales Government’s Office of Science and Research, The James N Kirby Foundation, and an additional Foundation that wishes to remain anonymous, is acknowledged. S.L.M. acknowledges support from the Milwaukee Metropolitan Sewerage District for student fellowships, and E.W.X.L. and S.W. acknowledge support from the Singapore National Research Foundation and the Ministry of Education under the Research Centre of Excellence Programme. K.M.Y.L. and G.J.Z. thank the State Key Laboratory of Marine Pollution, which is funded by Innovation and Technology Commission of the Hong Kong SAR Government (project no. 9448002), and the City University of Hong Kong via the funding to support the UN-endorsed Global Estuaries Monitoring (GEM) Programme (project no. 9380128). J.M.O. and E.J.S. acknowledge support from Maryland Sea Grant for summer REU student support. Y.W.D. and M.L.L acknowledge support from National Natural Science Foundation of China (42025604).

Author information

Author notes

  1. Stephen E. Swearer

    Present address: Oceans Institute, University of Western Australia, Perth, Western Australia, Australia

Authors and Affiliations

  1. School of Freshwater Sciences, University of Wisconsin-Milwaukee, Milwaukee, WI, USA

    Sandra L. McLellan, Jill S. McClary-Gutierrez & Melissa K. Schussman

  2. School of Natural Sciences, Macquarie University, Sydney, New South Wales, Australia

    Anthony Chariton & Annachiara Codello

  3. School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales, Australia

    Ezequiel M. Marzinelli

  4. University of Maryland Center for Environmental Science, Horn Point Laboratory, Cambridge, MD, USA

    Judith M. O’Neil

  5. University of Maryland Center for Environmental Science, Institute of Marine and Environmental Technology, Baltimore, MD, USA

    Eric J. Schott

  6. Northeastern University Marine Science Center, Nahant, MA, USA

    Jennifer L. Bowen & Joe H. Vineis

  7. Univ Brest (UBO), CNRS, IFREMER, Laboratoire de Microbiologie des Environnements Extrêmes, Plouzané, France

    Lois Maignien, Clarisse Lemonnier & Morgan Perennou

  8. Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, Northern Territory, Australia

    Karen S. Gibb

  9. State Key Laboratory of Marine Pollution and Department of Chemistry and School of Energy and Environment, City University of Hong Kong, City University of Hong Kong, Hong Kong, China

    Guang-Jie Zhou & Kenneth M. Y. Leung

  10. Water Resources Research Center, University of Hawaii at Manoa, Honolulu, HI, USA

    Marek Kirs

  11. Microbiology Department, Southern California Coastal Water Research Project, Costa Mesa, CA, USA

    John F. Griffith & Joshua A. Steele

  12. School of BioSciences, University of Melbourne, Melbourne, Victoria, Australia

    Stephen E. Swearer & Allyson L. O’Brien

  13. Frontier Science Center for Deep Ocean Multispheres and Earth System, and Key Laboratory of Physical Oceanography, Ministry of Education, Ocean University of China, Qingdao, China

    Dehai Song

  14. Frontier Science Center for Deep Ocean Multispheres and Earth System, and State Key Laboratory of Marine Pollution and Department of Chemistry, Ministry of Education, Ocean University of China, Qingdao, China

    Shengkang Liang

  15. Shandong Provincial Key Laboratory of Biochemical Engineering, College of Biological Engineering, Qingdao University of Science and Technology, Qingdao, China

    Junfeng Li

  16. Hydrobiological Station ‘Umberto D’Ancona’, Department of Biology, University of Padova, Uo CoNISMa, Chioggia, Italy

    Laura Airoldi

  17. National Biodiversity Future Center, Palermo, Italy

    Laura Airoldi & Francesco P. Mancuso

  18. Department of Earth and Marine Sciences, University of Palermo, Palermo, Italy

    Francesco P. Mancuso

  19. Departamento de Biologia Marinha, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

    Paulo S. Salomon & Arthur W. Silva-Lima

  20. Departamento de Biologia Marinha, Universidade Federal Fluminense, São Domingos, Brazil

    Renato C. Pereira

  21. Civil and Environmental Engineering, Stanford Doerr School of Sustainability and School of Engineering, Stanford University, Stanford, CA, USA

    Alexandria B. Boehm

  22. Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, Singapore

    Elton W. X. Lim & Stefan Wuertz

  23. Centro de Investigación Marina, Departamento de Ecología e Biología Animal, Universidad de Vigo, Vigo, Spain

    Emilio Fernández & Eva Teira

  24. Key Laboratory of Mariculture, Ministry of Education, Fisheries College, Ocean University of China, Qingdao, China

    Ming-Ling Liao & Yun-Wei Dong

  25. Centre for Marine Science and Innovation, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales, Australia

    Peter D. Steinberg

  26. Sydney Institute of Marine Science, Mosman, New South Wales, Australia

    Peter D. Steinberg

Authors
  1. Sandra L. McLellan
    View author publications

    Search author on:PubMed Google Scholar

  2. Anthony Chariton
    View author publications

    Search author on:PubMed Google Scholar

  3. Annachiara Codello
    View author publications

    Search author on:PubMed Google Scholar

  4. Jill S. McClary-Gutierrez
    View author publications

    Search author on:PubMed Google Scholar

  5. Melissa K. Schussman
    View author publications

    Search author on:PubMed Google Scholar

  6. Ezequiel M. Marzinelli
    View author publications

    Search author on:PubMed Google Scholar

  7. Judith M. O’Neil
    View author publications

    Search author on:PubMed Google Scholar

  8. Eric J. Schott
    View author publications

    Search author on:PubMed Google Scholar

  9. Jennifer L. Bowen
    View author publications

    Search author on:PubMed Google Scholar

  10. Joe H. Vineis
    View author publications

    Search author on:PubMed Google Scholar

  11. Lois Maignien
    View author publications

    Search author on:PubMed Google Scholar

  12. Clarisse Lemonnier
    View author publications

    Search author on:PubMed Google Scholar

  13. Morgan Perennou
    View author publications

    Search author on:PubMed Google Scholar

  14. Karen S. Gibb
    View author publications

    Search author on:PubMed Google Scholar

  15. Guang-Jie Zhou
    View author publications

    Search author on:PubMed Google Scholar

  16. Kenneth M. Y. Leung
    View author publications

    Search author on:PubMed Google Scholar

  17. Marek Kirs
    View author publications

    Search author on:PubMed Google Scholar

  18. John F. Griffith
    View author publications

    Search author on:PubMed Google Scholar

  19. Joshua A. Steele
    View author publications

    Search author on:PubMed Google Scholar

  20. Stephen E. Swearer
    View author publications

    Search author on:PubMed Google Scholar

  21. Allyson L. O’Brien
    View author publications

    Search author on:PubMed Google Scholar

  22. Dehai Song
    View author publications

    Search author on:PubMed Google Scholar

  23. Shengkang Liang
    View author publications

    Search author on:PubMed Google Scholar

  24. Junfeng Li
    View author publications

    Search author on:PubMed Google Scholar

  25. Laura Airoldi
    View author publications

    Search author on:PubMed Google Scholar

  26. Francesco P. Mancuso
    View author publications

    Search author on:PubMed Google Scholar

  27. Paulo S. Salomon
    View author publications

    Search author on:PubMed Google Scholar

  28. Arthur W. Silva-Lima
    View author publications

    Search author on:PubMed Google Scholar

  29. Renato C. Pereira
    View author publications

    Search author on:PubMed Google Scholar

  30. Alexandria B. Boehm
    View author publications

    Search author on:PubMed Google Scholar

  31. Elton W. X. Lim
    View author publications

    Search author on:PubMed Google Scholar

  32. Stefan Wuertz
    View author publications

    Search author on:PubMed Google Scholar

  33. Emilio Fernández
    View author publications

    Search author on:PubMed Google Scholar

  34. Eva Teira
    View author publications

    Search author on:PubMed Google Scholar

  35. Ming-Ling Liao
    View author publications

    Search author on:PubMed Google Scholar

  36. Yun-Wei Dong
    View author publications

    Search author on:PubMed Google Scholar

  37. Peter D. Steinberg
    View author publications

    Search author on:PubMed Google Scholar

Contributions

S.L.M., A. Chariton and P.D.S. designed the study. A. Condello managed the project, collected samples and performed laboratory testing. S.L.M., A. Chariton, A. Condello, J.S.M.-G., M.K.S. E.M.M., J.M.O. and E.J.S. analysed the data. S.L.M. drafted the manuscript. P.D.S., E.M.M., J.M.O., E.J.S., K.S.G. and K.M.Y.L. edited the draft manuscript. J.S.M.-G., J.L.B., J.H.V., L.M., C.L., M.P., K.S.G., G.-J.Z., K.M.Y.L., M.K., J.F.G., J.A.S., S.E.S., A.L.O., D.S., S.L., J.L., L.A., F.P.M., P.S.S., A.W.S.-L., R.C.P., A.B.B., E.W.X.L., S.W., E.F., E.T., M.-L.L. and Y.-W.D. conducted site-specific study design, collected samples, performed laboratory analysis and reviewed and edited the final manuscript. Lead authors from Milwaukee and Sydney listed by contribution, followed by authors arranged by cities in alphabetical order and corresponding author listed last.

Corresponding authors

Correspondence to Sandra L. McLellan or Peter D. Steinberg.

Ethics declarations

Competing interests

The authors declare they have no competing interests.

Peer review

Peer review information

Nature Water thanks Valerie Harwood and Kostas Konstantinidis for their contribution to the peer review of this work.

Additional information

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

Supplementary information

Supplementary Information

Supplementary Figs. 1–4, Tables 1–9 and Maps containing a list of all sample sites, coordinates and accompanying maps.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

McLellan, S.L., Chariton, A., Codello, A. et al. Universal microbial indicators provide surveillance of sewage contamination in harbours worldwide. Nat Water 2, 1061–1070 (2024). https://doi.org/10.1038/s44221-024-00315-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Version of record:

  • Issue date:

  • DOI: https://doi.org/10.1038/s44221-024-00315-5

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology