ACS Publications. Most Trusted. Most Cited. Most Read
Differential Decay of Wastewater Bacteria and Change of Microbial Communities in Beach Sand and Seawater Microcosms
My Activity

Figure 1Loading Img
    Article

    Differential Decay of Wastewater Bacteria and Change of Microbial Communities in Beach Sand and Seawater Microcosms
    Click to copy article linkArticle link copied!

    View Author Information
    Department of Civil and Environmental Engineering, University of Hawaii at Manoa, Honolulu, Hawaii 96822, United States
    *Phone: 808-956-6024. Fax: 808-956-5014. E-mail: [email protected]
    Other Access OptionsSupporting Information (1)

    Environmental Science & Technology

    Cite this: Environ. Sci. Technol. 2015, 49, 14, 8531–8540
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.est.5b01879
    Published June 30, 2015
    Copyright © 2015 American Chemical Society

    Abstract

    Click to copy section linkSection link copied!
    Abstract Image

    Laboratory microcosm experiments were conducted to determine the decay kinetics of wastewater bacteria and the change of microbial communities in beach sand and seawater. Cultivation-based methods showed that common fecal indicator bacteria (FIBs; Escherichia coli, enterococci, and Clostridium perfringens) exhibited biphasic decay patterns in all microcosms. Enterococci and C. perfringens, but not E. coli, showed significantly smaller decay rates in beach sand than in seawater. Cultivation-independent qPCR quantification of 16S rRNA gene also showed significantly slower decrease of total bacterial densities in beach sand than in seawater. Microbial community analysis by next-generation sequencing (NGS) further illustrated that the decreasing relative abundance of wastewater bacteria was contrasted by the increase in indigenous beach sand and seawater microbiota, and the overall microbial community dynamics corresponded well with the decay of individual FIB populations. In summary, the differential decay of wastewater bacteria in beach sand and in seawater provides a kinetic explanation to the often-observed higher abundance of FIBs in beach sand, and the NGS-based microbial community analysis can provide valuable insights to understanding the fate of wastewater bacteria in the context of indigenous microbial communities in natural environments.

    Copyright © 2015 American Chemical Society

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. Add or change your institution or let them know you’d like them to include access.

    Supporting Information

    Click to copy section linkSection link copied!

    Additional information on persisting FIB concentrations and microbial diversity indices in the beach sand and seawater microcossms. The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.5b01879.

    Terms & Conditions

    Electronic Supporting Information files are available without a subscription to ACS Web Editions. The American Chemical Society holds a copyright ownership interest in any copyrightable Supporting Information. Files available from the ACS website may be downloaded for personal use only. Users are not otherwise permitted to reproduce, republish, redistribute, or sell any Supporting Information from the ACS website, either in whole or in part, in either machine-readable form or any other form without permission from the American Chemical Society. For permission to reproduce, republish and redistribute this material, requesters must process their own requests via the RightsLink permission system. Information about how to use the RightsLink permission system can be found at http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    Click to copy section linkSection link copied!
    Citation Statements
    Explore this article's citation statements on scite.ai

    This article is cited by 56 publications.

    1. Ke Yuan, Lan Lin, Xiuqin Xie, Zhiqiang Zhao, Ligang Hu, Tiangang Luan, Baowei Chen. Differential Characteristics of Waterborne Bacterial Pathogens and Virulence Factors between Suspended Particulate Matters and Aqueous Phase in the Pearl River and Pearl River Estuary. ACS ES&T Water 2023, 3 (5) , 1341-1351. https://doi.org/10.1021/acsestwater.3c00016
    2. Sumeth Wongkiew, Zhen Hu, Jae Woo Lee, Kartik Chandran, Hua Thai Nhan, Kyle Rafael Marcelino, Samir Kumar Khanal. Nitrogen Recovery via Aquaponics–Bioponics: Engineering Considerations and Perspectives. ACS ES&T Engineering 2021, 1 (3) , 326-339. https://doi.org/10.1021/acsestengg.0c00196
    3. Sumeth Wongkiew, Mee-Rye Park, Kartik Chandran, Samir Kumar Khanal. Aquaponic Systems for Sustainable Resource Recovery: Linking Nitrogen Transformations to Microbial Communities. Environmental Science & Technology 2018, 52 (21) , 12728-12739. https://doi.org/10.1021/acs.est.8b04177
    4. Ming Zhi Wu, Denis M. O’Carroll, Laura J. Vogel, and Clare E. Robinson . Effect of Low Energy Waves on the Accumulation and Transport of Fecal Indicator Bacteria in Sand and Pore Water at Freshwater Beaches. Environmental Science & Technology 2017, 51 (5) , 2786-2794. https://doi.org/10.1021/acs.est.6b05985
    5. Andrew F. Brouwer, Marisa C. Eisenberg, Justin V. Remais, Philip A. Collender, Rafael Meza, and Joseph N. S. Eisenberg . Modeling Biphasic Environmental Decay of Pathogens and Implications for Risk Analysis. Environmental Science & Technology 2017, 51 (4) , 2186-2196. https://doi.org/10.1021/acs.est.6b04030
    6. Jiaqian Li, Mohan Bai, Yaodong He, Suisui Wang, Guangyi Wang. Decay kinetics of human-associated pathogens in the marine microcosms reveals their new dynamics and potential indicators in the coastal waters of northern China. Environmental Pollution 2024, 362 , 124936. https://doi.org/10.1016/j.envpol.2024.124936
    7. Deepak Kumar Prasad, Rishabh Shukla, Shaikh Ziauddin Ahammad. Antibiotic resistance in the Ganga River: Investigation of antibiotic resistant bacteria and antibiotic resistance genes, and public health risk assessment. Journal of Environmental Chemical Engineering 2024, 12 (6) , 114931. https://doi.org/10.1016/j.jece.2024.114931
    8. Yossi Cohen, Julia Johnke, Alfred Abed-Rabbo, Zohar Pasternak, Antonis Chatzinotas, Edouard Jurkevitch. Unbalanced predatory communities and a lack of microbial degraders characterize the microbiota of a highly sewage-polluted Eastern-Mediterranean stream. FEMS Microbiology Ecology 2024, 100 (6) https://doi.org/10.1093/femsec/fiae069
    9. Maria Steadmon, Melia Takakusagi, Tracy N. Wiegner, Mikayla Jones, Louise M. Economy, Jazmine Panelo, Lynn A. Morrison, Matt C. I. Medeiros, Kiana L. Frank. Detection and modeling of Staphylococcus aureus and fecal bacteria in Hawaiian coastal waters and sands. Water Environment Research 2024, 96 (5) https://doi.org/10.1002/wer.11037
    10. Man Yue Lam, Reza Ahmadian. Enhancing hydro-epidemiological modelling of nearshore coastal waters with source-receptor connectivity study. Environmental Pollution 2024, 345 , 123431. https://doi.org/10.1016/j.envpol.2024.123431
    11. Hua Zou, Jiangtao He, Yanjia Chu, Baoshi Xu, Wei Li, Shiwen Huang, Xiangyu Guan, Fei Liu, Haiyan Li. Revealing discrepancies and drivers in the impact of lomefloxacin on groundwater denitrification throughout microbial community growth and succession. Journal of Hazardous Materials 2024, 465 , 133139. https://doi.org/10.1016/j.jhazmat.2023.133139
    12. Mandy Lok Yi Tang, Stanley Chun Kwan Lau. Effects of chlorination on the survival of sewage bacteria in seawater microcosms. Environmental Microbiology Reports 2024, 16 (1) https://doi.org/10.1111/1758-2229.13216
    13. Michael J. Ormsby, Hannah L. White, Rebecca Metcalf, David M. Oliver, Nicholas A. Feasey, Richard S. Quilliam. Enduring pathogenicity of African strains of Salmonella on plastics and glass in simulated peri-urban environmental waste piles. Journal of Hazardous Materials 2024, 461 , 132439. https://doi.org/10.1016/j.jhazmat.2023.132439
    14. Rebecca Metcalf, Lauren F. Messer, Hannah L. White, Michael J. Ormsby, Sabine Matallana-Surget, Richard S. Quilliam. Evidence of interspecific plasmid uptake by pathogenic strains of Klebsiella isolated from microplastic pollution on public beaches. Journal of Hazardous Materials 2024, 461 , 132567. https://doi.org/10.1016/j.jhazmat.2023.132567
    15. Wenjing Ren, Yucheng Feng. Persistence of human- and cattle-associated Bacteroidales and mitochondrial DNA markers in freshwater mesocosms. Science of The Total Environment 2023, 899 , 165742. https://doi.org/10.1016/j.scitotenv.2023.165742
    16. Warish Ahmed, Sudhi Payyappat, Michele Cassidy, Nathan Harrison, Colin Besley. Reduction of human fecal markers and enteric viruses in Sydney estuarine waters receiving wet weather overflows. Science of The Total Environment 2023, 896 , 165008. https://doi.org/10.1016/j.scitotenv.2023.165008
    17. Leonie Suter, Simon Wotherspoon, So Kawaguchi, Rob King, Anna J. MacDonald, Georgia M. Nester, Andrea M. Polanowski, Ben Raymond, Bruce E. Deagle. Environmental DNA of Antarctic krill ( Euphausia superba ): Measuring DNA fragmentation adds a temporal aspect to quantitative surveys. Environmental DNA 2023, 5 (5) , 945-959. https://doi.org/10.1002/edn3.394
    18. Maria Steadmon, Kebang Ngiraklang, Macy Nagata, Keanu Masga, Kiana L. Frank. Effects of water turbidity on the survival of Staphylococcus aureus in environmental fresh and brackish waters. Water Environment Research 2023, 95 (9) https://doi.org/10.1002/wer.10923
    19. Rebecca Metcalf, Hannah L. White, Michael J. Ormsby, David M. Oliver, Richard S. Quilliam. From wastewater discharge to the beach: Survival of human pathogens bound to microplastics during transfer through the freshwater-marine continuum. Environmental Pollution 2023, 319 , 120955. https://doi.org/10.1016/j.envpol.2022.120955
    20. Osvalda De Giglio, Marcella Narracci, Francesca Apollonio, Francesco Triggiano, Maria Immacolata Acquaviva, Carmela Caroppo, Giusy Diella, Antonella Di Leo, Fabrizio Fasano, Santina Giandomenico, Lucia Spada, Rosa Anna Cavallo, Maria Teresa Montagna. Microbiological and chemical characteristics of beaches along the Taranto Gulf (Ionian Sea, Southern Italy). Environmental Monitoring and Assessment 2022, 194 (6) https://doi.org/10.1007/s10661-022-10103-x
    21. Kara Dean, Jade Mitchell. Identifying water quality and environmental factors that influence indicator and pathogen decay in natural surface waters. Water Research 2022, 211 , 118051. https://doi.org/10.1016/j.watres.2022.118051
    22. Amit Kumar, Daphne H. P. Ng, Sakcham Bairoliya, Bin Cao, . The Dark Side of Microbial Processes: Accumulation of Nitrate During Storage of Surface Water in the Dark and the Underlying Mechanism. Microbiology Spectrum 2022, 10 (1) https://doi.org/10.1128/spectrum.02232-21
    23. Lavane Kim, Tao Yan, Van Toan Pham. Inactivation of Escherichia coli enhanced by anaerobic microbial iron reduction. Environmental Science and Pollution Research 2021, 28 (45) , 63614-63622. https://doi.org/10.1007/s11356-020-11209-w
    24. Yoshihiro Suzuki, Hiroki Shimizu, Takahiro Kuroda, Yusuke Takada, Kei Nukazawa. Plant debris are hotbeds for pathogenic bacteria on recreational sandy beaches. Scientific Reports 2021, 11 (1) https://doi.org/10.1038/s41598-021-91066-w
    25. Amity G. Zimmer-Faust, Joshua A. Steele, Xianyi Xiong, Christopher Staley, Madison Griffith, Michael J. Sadowsky, Margarita Diaz, John F. Griffith. A Combined Digital PCR and Next Generation DNA-Sequencing Based Approach for Tracking Nearshore Pollutant Dynamics Along the Southwest United States/Mexico Border. Frontiers in Microbiology 2021, 12 https://doi.org/10.3389/fmicb.2021.674214
    26. Marcos T. Carneiro, Daniel V. Perez, Renato C. Feitosa, Lorena G. P. Macena, Marize P. Miagostovich, Julio C. Wasserman. Escherichia coli Capacity to Repopulate Microcosms Under Osmotic/U.V. Synergic Stress in Tropical Waters. Current Microbiology 2021, 78 (2) , 756-764. https://doi.org/10.1007/s00284-020-02319-2
    27. Warish Ahmed, Simon Toze, Cameron Veal, Paul Fisher, Qian Zhang, Zhigang Zhu, Christopher Staley, Michael J. Sadowsky. Comparative decay of culturable faecal indicator bacteria, microbial source tracking marker genes, and enteric pathogens in laboratory microcosms that mimic a sub-tropical environment. Science of The Total Environment 2021, 751 , 141475. https://doi.org/10.1016/j.scitotenv.2020.141475
    28. Marcos Tavares Carneiro, Daniel Vidal Perez, Renato Castiglia Feitosa, Julio Cesar Wasserman. Separation of Escherichia coli from natural samples for identification of sources and microcosm inoculation. Brazilian Journal of Microbiology 2020, 51 (4) , 2015-2020. https://doi.org/10.1007/s42770-020-00374-2
    29. Prince P. Mathai, Christopher Staley, Michael J. Sadowsky. Sequence-enabled community-based microbial source tracking in surface waters using machine learning classification: A review. Journal of Microbiological Methods 2020, 177 , 106050. https://doi.org/10.1016/j.mimet.2020.106050
    30. Keita Yanagimoto, Kosei Uematsu, Takaya Yamagami, Eiji Haramoto. The Circulation of Type F Clostridium perfringens among Humans, Sewage, and Ruditapes philippinarum (Asari Clams). Pathogens 2020, 9 (8) , 669. https://doi.org/10.3390/pathogens9080669
    31. Meredith B. Nevers, Muruleedhara N. Byappanahalli, Cindy H. Nakatsu, Julie L. Kinzelman, Mantha S. Phanikumar, Dawn A. Shively, Ashley M. Spoljaric. Interaction of bacterial communities and indicators of water quality in shoreline sand, sediment, and water of Lake Michigan. Water Research 2020, 178 , 115671. https://doi.org/10.1016/j.watres.2020.115671
    32. Jinsoo Kim, Sangrim Kang, Hyun-Sook Kim, Sungchul Kim, Sang-Seob Lee, . Pilot plant study on nitrogen and phosphorus removal in marine wastewater by marine sediment with sequencing batch reactor. PLOS ONE 2020, 15 (5) , e0233042. https://doi.org/10.1371/journal.pone.0233042
    33. Andrew F. Brouwer, Marisa C. Eisenberg, Nancy G. Love, Joseph N.S. Eisenberg. Phenotypic variations in persistence and infectivity between and within environmentally transmitted pathogen populations impact population-level epidemic dynamics. BMC Infectious Diseases 2019, 19 (1) https://doi.org/10.1186/s12879-019-4054-8
    34. Asja Korajkic, Pauline Wanjugi, Lauren Brooks, Yiping Cao, Valerie J. Harwood. Persistence and Decay of Fecal Microbiota in Aquatic Habitats. Microbiology and Molecular Biology Reviews 2019, 83 (4) https://doi.org/10.1128/MMBR.00005-19
    35. Ananda Tiwari, Ari Kauppinen, Tarja Pitkänen. Decay of Enterococcus faecalis, Vibrio cholerae and MS2 Coliphage in a Laboratory Mesocosm Under Brackish Beach Conditions. Frontiers in Public Health 2019, 7 https://doi.org/10.3389/fpubh.2019.00269
    36. Angelos Hannides, Nicole Elko, Kenneth Humiston. The state of understanding of the effects of beach nourishment activities on coastal biogeochemical processes and conditions. Shore & Beach 2019, , 46-57. https://doi.org/10.34237/1008734
    37. Hernando Sánchez Moreno, Hernando José Bolívar-Anillo, Zamira E. Soto-Varela, Yani Aranguren, Camila Pichón Gonzaléz, Diego Andrés Villate Daza, Giorgio Anfuso. Microbiological water quality and sources of contamination along the coast of the Department of Atlántico (Caribbean Sea of Colombia). Preliminary results. Marine Pollution Bulletin 2019, 142 , 303-308. https://doi.org/10.1016/j.marpolbul.2019.03.054
    38. Warish Ahmed, Qian Zhang, Sonya Kozak, David Beale, Pradip Gyawali, Michael J. Sadowsky, Stuart Simpson. Comparative decay of sewage-associated marker genes in beach water and sediment in a subtropical region. Water Research 2019, 149 , 511-521. https://doi.org/10.1016/j.watres.2018.10.088
    39. Cataldo De Blasio. Balances on Microbial Fermentation. 2019, 221-231. https://doi.org/10.1007/978-3-030-11599-9_16
    40. Claudia Esmeralda León-López, José Alfredo Arreola-Lizárraga, Gustavo Padilla-Arredondo, Jorge Eduardo Chávez-Villalba, Renato Arturo Mendoza-Salgado, Lía Celina Méndez-Rodríguez, Jaqueline García-Hernández. Temporal variability of enterococci and associated sources at three subtropical recreational beaches. Oceanological and Hydrobiological Studies 2018, 47 (4) , 327-336. https://doi.org/10.1515/ohs-2018-0031
    41. Yoshihiro Suzuki, Kotaro Teranishi, Tomonori Matsuwaki, Kei Nukazawa, Yoshitoshi Ogura. Effects of bacterial pollution caused by a strong typhoon event and the restoration of a recreational beach: Transitions of fecal bacterial counts and bacterial flora in beach sand. Science of The Total Environment 2018, 640-641 , 52-61. https://doi.org/10.1016/j.scitotenv.2018.05.265
    42. Alison WS Luk, Sabrina Beckmann, Mike Manefield. Dependency of DNA extraction efficiency on cell concentration confounds molecular quantification of microorganisms in groundwater. FEMS Microbiology Ecology 2018, 94 (10) https://doi.org/10.1093/femsec/fiy146
    43. Thirumahal Muthukrishnan, Raeid M. M. Abed. Effects of Irrigation on Alkane Biodegradation of Oil-Contaminated Desert Soils. Environmental Processes 2018, 5 (3) , 631-648. https://doi.org/10.1007/s40710-018-0325-4
    44. Warish Ahmed, Christopher Staley, Thomas Kaiser, Michael J. Sadowsky, Sonya Kozak, David Beale, Stuart Simpson. Decay of sewage-associated bacterial communities in fresh and marine environmental waters and sediment. Applied Microbiology and Biotechnology 2018, 102 (16) , 7159-7170. https://doi.org/10.1007/s00253-018-9112-4
    45. C. Schang, A. Lintern, P. L. M. Cook, G. Rooney, R. Coleman, H. M. Murphy, A. Deletic, D. McCarthy. Escherichia coli survival and transfer in estuarine bed sediments. River Research and Applications 2018, 34 (6) , 606-614. https://doi.org/10.1002/rra.3281
    46. Stephanie DeFlorio-Barker, Benjamin F Arnold, Elizabeth A Sams, Alfred P Dufour, John M Colford, Steven B Weisberg, Kenneth C Schiff, Timothy J Wade. Child environmental exposures to water and sand at the beach: Findings from studies of over 68,000 subjects at 12 beaches. Journal of Exposure Science & Environmental Epidemiology 2018, 28 (2) , 93-100. https://doi.org/10.1038/jes.2017.23
    47. Wenjing Zhang, Yongbo Pan, Jun Yang, Huihuang Chen, Bridget Holohan, Jamie Vaudrey, Senjie Lin, George B. McManus. The diversity and biogeography of abundant and rare intertidal marine microeukaryotes explained by environment and dispersal limitation. Environmental Microbiology 2018, 20 (2) , 462-476. https://doi.org/10.1111/1462-2920.13916
    48. Amit Kumar, Daphne Ng, Bin Cao. Fate of Enterococcus faecalis in stormwater matrices under ultraviolet-A (365 nm) irradiation. Environmental Science: Water Research & Technology 2018, 4 (5) , 639-643. https://doi.org/10.1039/C8EW00010G
    49. Ayron M. Strauch. Relative change in stream discharge from a tropical watershed improves predictions of fecal bacteria in near-shore environments. Hydrological Sciences Journal 2017, 62 (9) , 1381-1393. https://doi.org/10.1080/02626667.2017.1310381
    50. David Mantilla-Calderon, Pei-Ying Hong, . Fate and Persistence of a Pathogenic NDM-1-Positive Escherichia coli Strain in Anaerobic and Aerobic Sludge Microcosms. Applied and Environmental Microbiology 2017, 83 (13) https://doi.org/10.1128/AEM.00640-17
    51. Daniela Romão, Christopher Staley, Filipa Ferreira, Raquel Rodrigues, Raquel Sabino, Cristina Veríssimo, Ping Wang, Michael Sadowsky, João Brandão. Next-generation sequencing and culture-based techniques offer complementary insights into fungi and prokaryotes in beach sands. Marine Pollution Bulletin 2017, 119 (1) , 351-358. https://doi.org/10.1016/j.marpolbul.2017.04.036
    52. W. Ahmed, K.A. Hamilton, A. Vieritz, D. Powell, A. Goonetilleke, M.T. Hamilton, T. Gardner. Microbial risk from source-separated urine used as liquid fertilizer in sub-tropical Australia. Microbial Risk Analysis 2017, 5 , 53-64. https://doi.org/10.1016/j.mran.2016.11.005
    53. Gregory D. O’Mullan, M. Elias Dueker, Andrew R. Juhl. Challenges to Managing Microbial Fecal Pollution in Coastal Environments: Extra-Enteric Ecology and Microbial Exchange Among Water, Sediment, and Air. Current Pollution Reports 2017, 3 (1) , 1-16. https://doi.org/10.1007/s40726-016-0047-z
    54. Qian Zhang, Jessica J. Eichmiller, Christopher Staley, Michael J. Sadowsky, Satoshi Ishii. Correlations between pathogen concentration and fecal indicator marker genes in beach environments. Science of The Total Environment 2016, 573 , 826-830. https://doi.org/10.1016/j.scitotenv.2016.08.122
    55. Roberto Abreu, Celso Figueira, Daniela Romão, João Brandão, M. Conceição Freitas, César Andrade, Graça Calado, Carmen Ferreira, Ana Campos, Susana Prada. Sediment characteristics and microbiological contamination of beach sand – A case–study in the archipelago of Madeira. Science of The Total Environment 2016, 573 , 627-638. https://doi.org/10.1016/j.scitotenv.2016.08.160
    56. Christopher Staley, Michael J. Sadowsky, . Regional Similarities and Consistent Patterns of Local Variation in Beach Sand Bacterial Communities throughout the Northern Hemisphere. Applied and Environmental Microbiology 2016, 82 (9) , 2751-2762. https://doi.org/10.1128/AEM.00247-16

    Environmental Science & Technology

    Cite this: Environ. Sci. Technol. 2015, 49, 14, 8531–8540
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.est.5b01879
    Published June 30, 2015
    Copyright © 2015 American Chemical Society

    Article Views

    1830

    Altmetric

    -

    Citations

    Learn about these metrics

    Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.

    Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.

    The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.