Abstract
Pathogens and chemical contaminants in stormwater are major environmental and public health concerns. Characterizing the variability in composition and bioremediation functions of the microbial community from different sources of stormwater will help with efforts to properly manage water after it rains. To improve understanding of the variability and composition of the microbial community in run-off from different sources, we sampled stormwater over time from an outfall and receiving stream, along with run-off from different locations (rooftop, roadway) to identify microbial components associated with these urban waters. Community composition was variable in space and time for water samples from the same source. Even with this variability, we found taxonomic and functional groups differentially distributed in water samples collected during wet or dry weather or collected from different sources. The differentially distributed taxonomic and functional groups represent the unique characteristics of the source, such as when communities are exposed to iron in pipe material from the outfall or hydrocarbons flushed from various surfaces during rain events. Additionally, fecal indicator sequences from Clostridiales and Bacteroidales taxa made up a larger fraction of the microbial community from water collected under dry conditions. Our work characterizes the variability in microbial community composition and functions from a variety of urban water sources, with specific attention to communities from sources where water might be collected or treated with green infrastructure systems (e.g. rain gardens or biofilters). This will aid our understanding of the impact of human activities in urban environments on the surrounding water system.
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Data availability
Raw sequence reads have been submitted to the National Center for Biotechnology Information Sequence Read Archive under BioProject accession number PRJNA599168.
References
Ahmed W, Hodgers L, Sidhu JPS, Toze S (2012) Fecal indicators and zoonotic pathogens in household drinking water taps fed from rainwater tanks in Southeast Queensland. Australia Applied and Environmental Microbiology 78:219–226. https://doi.org/10.1128/Aem.06554-11
Ancion PY, Lear G, Neale M, Roberts K, Lewis GD (2014) Using biofilm as a novel approach to assess stormwater treatment efficacy. Water Res 49:406–415. https://doi.org/10.1016/j.watres.2013.10.023
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1046/j.1442-9993.2001.01070.x
Arnone RD, Walling JP (2007) Waterborne pathogens in urban watersheds. J Water Health 5:149–162. https://doi.org/10.2166/wh.2006.001
Baral D, Speicher A, Dvorak B, Admiraal D, Li X (2018) Quantifying the relative contributions of environmental sources to the microbial community in an urban stream under dry and wet weather conditions. Appl Environ Microb 84:e00896–e00818
Baun A, Eriksson E, Ledin A, Mikkelsen PS (2006) A methodology for ranking and hazard identification of xenobiotic organic compounds in urban stormwater. Sci Total Environ 370:29–38. https://doi.org/10.1016/j.scitotenv.2006.05.017
Berger AW, Valenca R, Miao Y, Ravi S, Mahendra S, Mohanty SK (2019) Biochar increases nitrate removal capacity of woodchip biofilters during high-intensity rainfall. Water Res 165:115008. https://doi.org/10.1016/j.watres.2019.115008
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581-+. https://doi.org/10.1038/Nmeth.3869
Charpe AU, Latkar MV, Chakrabarti T (2019) Biocementation: an eco-friendly approach to strengthen concrete. P I Civil Eng-Eng Su 172:438–449. https://doi.org/10.1680/jensu.18.00019
Chaudhary A, Kauser I, Ray A, Poretsky R (2018) Taxon-driven functional shifts associated with storm flow in an urban stream microbial community. Msphere 3:e00194–e00118. https://doi.org/10.1128/mSphere.00194-18
Chong MN, Sidhu J, Aryal R, Tang J, Gernjak W, Escher B, Toze S (2013) Urban stormwater harvesting and reuse: a probe into the chemical, toxicology and microbiological contaminants in water quality. Environ Monit Assess 185:6645–6652. https://doi.org/10.1007/s10661-012-3053-7
Clark SE, Steele KA, Spicher J, Siu CYS, Lalor MM, Pitt R, Kirby JT (2008) Roofing materials' contributions to storm-water runoff pollution. J Irrig Drainage Eng-ASCE 134:638–645. https://doi.org/10.1061/(asce)0733-9437(2008)134:5(638)
Davis AP, Shokouhian M, Sharma H, Minami C (2001) Laboratory study of biological retention for urban stormwater management. Water Environ Res 73:5–14. https://doi.org/10.2175/106143001x138624
Davis AP, Hunt WF, Traver RG, Clar M (2009) Bioretention technology: overview of current practice and future needs. J Environ Eng 135:109–117
Deeb M et al (2018) Soil and microbial properties of green infrastructure stormwater management systems. Ecol Eng 125:68–75. https://doi.org/10.1016/j.ecoleng.2018.10.017
DeSantis TZ et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microb 72:5069–5072. https://doi.org/10.1128/Aem.03006-05
Evans CA, Coombes PJ, Dunstan RH, Harrison T (2009) Extensive bacterial diversity indicates the potential operation of a dynamic micro-ecology within domestic rainwater storage systems. Sci Total Environ 407:5206–5215. https://doi.org/10.1016/j.scitotenv.2009.06.009
Field KG, Samadpour M (2007) Fecal source tracking, the indicator paradigm, and managing water quality. Water Res 41:3517–3538. https://doi.org/10.1016/j.watres.2007.06.056
Fisher JC, Eren AM, Green HC, Shanks OC, Morrison HG, Vineis JH, Sogin ML, McLellan SL (2015a) Comparison of sewage and animal fecal microbiomes by using oligotyping reveals potential human fecal indicators in multiple taxonomic groups. Appl Environ Microb 81:7023–7033. https://doi.org/10.1128/Aem.01524-15
Fisher JC, Newton RJ, Dila DK, McLellan SL (2015b) Urban microbial ecology of a freshwater estuary of Lake Michigan Elementa-Sci Anthrop 3:000064 https://doi.org/10.12952/journal.elementa.000064
Fraser AN, Zhang Y, Sakowski EG, Preheim SP (2018) Dynamics and functional potential of stormwater microorganisms colonizing sand filters. Water-Sui 10:1065. https://doi.org/10.3390/w10081065
Galfi H, Haapala J, Nordqvist K, Westerlund C, Blecken GT, Marsalek J, Viklander M (2016) Inter-event and intra-event variations of indicator bacteria concentrations in the storm sewer system of the city of ostersund. Sweden J Environ Eng 142:06016003. https://doi.org/10.1061/(Asce)Ee.1943-7870.0001067
Grebel JE, Mohanty SK, Torkelson AA, Boehm AB, Higgins CP, Maxwell RM, Nelson KL, Sedlak DL (2013) Engineered Infiltration Systems for Urban Stormwater Reclamation. Environ Eng Sci 30:437–454. https://doi.org/10.1089/ees.2012.0312
Hajj-Mohamad M et al (2019) Fecal contamination of storm sewers: evaluating wastewater micropollutants, human-specific Bacteroides 16S rRNA, and mitochondrial DNA genetic markers as alternative indicators of sewer cross connections. Sci Total Environ 659:548–560. https://doi.org/10.1016/j.scitotenv.2018.12.378
Hamilton K, Reyneke B, Waso M, Clements T, Ndlovu T, Khan W, DiGiovanni K, Rakestraw E, Montalto F, Haas CN, Ahmed W (2019) A global review of the microbiological quality and potential health risks associated with roof-harvested rainwater tanks. Npj Clean Water 2:7. https://doi.org/10.1038/s41545-019-0030-5
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley & Sons, Chicheester, UL, pp 115–147
Liu Y, Li J (2008) Role of Pseudomonas aeruginosa biofilm in the initial adhesion, growth and detachment of Escherichia coli in porous media. Environ Sci Technol 42:443–449. https://doi.org/10.1021/es071861b
Louca S, Parfrey LW, Doebeli M (2016) Decoupling function and taxonomy in the global ocean microbiome. Science 353:1272–1277. https://doi.org/10.1126/science.aaf4507
Mandal S, Van Treuren W, White RA, Eggesbo M, Knight R, Peddada SD (2015) Analysis of composition of microbiomes: a novel method for studying microbial composition. Microb Ecol Health Dis 26:27663. https://doi.org/10.3402/mehd.v26.27663
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads 17: 3. https://doi.org/10.14806/ej.17.1.200
McLellan SL, Eren AM (2014) Discovering new indicators of fecal pollution. Trends Microbiol 22:697–706. https://doi.org/10.1016/j.tim.2014.08.002
McLellan SL, Huse SM, Mueller-Spitz SR, Andreishcheva EN, Sogin ML (2010) Diversity and population structure of sewage-derived microorganisms in wastewater treatment plant influent. Environ Microbiol 12:378–392. https://doi.org/10.1111/j.1462-2920.2009.02075.x
McLellan SL, Fisher JC, Newton RJ (2015) The microbiome of urban waters. Int Microbiol 18:141–149. https://doi.org/10.2436/20.1501.01.244
Muller A, Osterlund H, Marsalek J, Viklander M (2020) The pollution conveyed by urban runoff: A review of sources. Sci Total Environ 709:18. https://doi.org/10.1016/j.scitotenv.2019.136125
Newman AP, Coupe SJ (2016) Biodegradation in Green Infrastructure Sustainable Surface Water Management:115–126 doi:doi:https://doi.org/10.1002/9781118897690.ch9
Newton RJ, Bootsma MJ, Morrison HG, Sogin ML, McLellan SL (2013) A microbial signature approach to identify fecal pollution in the waters off an urbanized coast of lake Michigan. Microb Ecol 65:1011–1023. https://doi.org/10.1007/s00248-013-0200-9
Normand P (2006) The families Frankiaceae, Geodermatophilaceae, Acidothermaceae and Sporichthyaceae. Prokaryotes: a handbook on the biology of Bacteria, Vol 3, Third edition: Archaea. Bacteria: Firmicutes, Actinomycetes. Springer. N Y. https://doi.org/10.1007/0-387-30743-5_26
Pandey PK, Kass PH, Soupir ML, Biswas S, Singh VP (2014) Contamination of water resources by pathogenic bacteria. Amb Express 4:51. https://doi.org/10.1186/s13568-014-0051-x
Parker EA, Rippy MA, Mehring AS, Winfrey BK, Ambrose RF, Levin LA, Grant SB (2017) Predictive power of clean bed filtration theory for fecal indicator bacteria removal in stormwater biofilters. Environ Sci Technol 51:5703–5712. https://doi.org/10.1021/acs.est.7b00752
Preheim SP et al (2016) Surveys, simulation and single-cell assays relate function and phylogeny in a lake ecosystem. Nat Microbiol 1:16130. https://doi.org/10.1038/Nmicrobiol.2016.130
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing,
Ramirez-Castillo FY, Loera-Muro A, Jacques M, Garneau P, Avelar-Gonzalez FJ, Harel J, Guerrero-Barrera AL (2015) Waterborne pathogens: detection methods and challenges. Pathogens 4:307–334. https://doi.org/10.3390/pathogens4020307
Rippy MA (2015) Meeting the criteria: linking biofilter design to fecal indicator bacteria removal. Wires Water 2:577–592. https://doi.org/10.1002/wat2.1096
Roberto AA, Van Gray JB, Engohang-Ndong J, Leff LG (2019) Distribution and co-occurrence of antibiotic and metal resistance genes in biofilms of an anthropogenically impacted stream. Sci Total Environ 688:437–449. https://doi.org/10.1016/j.scitotenv.2019.06.053
Roguet A, Eren AM, Newton RJ, McLellan SL (2018) Fecal source identification using random forest. Microbiome 6:185. https://doi.org/10.1186/s40168-018-0568-3
Roguet A, Esen ÖC, Eren AM, Newton RJ, McLellan SL (2020) FORENSIC: an online platform for fecal source identification. mSystems 5:e00869–e00819. https://doi.org/10.1128/mSystems.00869-19
Savichtcheva O, Okabe S (2006) Alternative indicators of fecal pollution: relations with pathogens and conventional indicators, current methodologies for direct pathogen monitoring and future application perspectives. Water Res 40:2463–2476. https://doi.org/10.1016/j.watres.2006.04.040
Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. Plos One 6:14. https://doi.org/10.1371/journal.pone.0027310
Schoen ME, Ashbolt NJ (2010) Assessing pathogen risk to swimmers at non-sewage impacted recreational beaches. Environ Sci Technol 44:2286–2291. https://doi.org/10.1021/es903523q
Sercu B, Van De Werfhorst LC, Murray J, Holden PA (2009) Storm drains are sources of human fecal pollution during dry weather in three urban southern california watersheds. Environ Sci Technol 43:293–298. https://doi.org/10.1021/es801505p
Soller JA, Schoen ME, Bartrand T, Ravenscroft JE, Ashbolt NJ (2010) Estimated human health risks from exposure to recreational waters impacted by human and non-human sources of faecal contamination. Water Res 44:4674–4691. https://doi.org/10.1016/j.watres.2010.06.049
Unger M, Collins MR (2008) Assessing Escherichia coli removal in the schmutzdecke of slow-rate biofilters. J Am Water Works Ass 100:60–73
Urzi C, Brusetti L, Salamone P, Sorlini C, Stackebrandt E, Daffonchio D (2001) Biodiversity of Geodermatophilaceae isolated from altered stones and monuments in the Mediterranean basin. Environ Microbiol 3:471–479. https://doi.org/10.1046/j.1462-2920.2001.00217.x
Wang CS, Wang F, Qin HP, Zeng XF, Li XR, Yu SL (2018) Effect of saturated zone on nitrogen removal processes in stormwater bioretention systems. Water-Sui 10:162. https://doi.org/10.3390/w10020162
Watkinson RJ, Morgan P (1990) Physiology of aliphatic hydrocarbon-degrading microorganisms. Biodegradation 1:79–92. https://doi.org/10.1007/Bf00058828
Wyckoff KN, Chen S, Steinman AJ, He Q (2017) Impact of roadway stormwater runoff on microbial contamination in the receiving stream. J Environ Qual 46:1065–1071. https://doi.org/10.2134/jeq2017.03.0116
Yang YY, Lusk MG (2018) Nutrients in urban stormwater runoff: current state of the science and potential mitigation options. Curr Pollut Rep 4:112–127. https://doi.org/10.1007/s40726-018-0087-7
Zhang JJ, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30:614–620. https://doi.org/10.1093/bioinformatics/btt593
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This work was funded by the Chemical, Bioengineering, Environmental and Transport Systems Division of the National Science Foundation Grant (Award No. 511915). ANF was also supported by an Integrative Graduate Education and Research Traineeship (IGERT) fellowship from the National Science Foundation, Division of Graduate Education, grant award number 1069213. Part of this research project was conducted using computational resources at the Maryland Advanced Research Computing Center (MARCC).
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All authors contributed to the study conception, design, data analysis, and funding acquisition. Material preparation, data collection, and experimental methodology were conducted by Andrea Fraser. The first draft of the paper was written by Andrea Fraser and all authors edited subsequent versions of the manuscript. All authors read and approved the final manuscript.
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Fraser, A.N., Preheim, S.P. Bacterial community composition and functional potential associated with a variety of urban stormwater sources. Urban Ecosyst 24, 1379–1390 (2021). https://doi.org/10.1007/s11252-021-01121-7
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DOI: https://doi.org/10.1007/s11252-021-01121-7