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Spatio-temporal variations in the physiological profiles of streambed bacterial communities: implication of wastewater treatment plant effluents

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Abstract

The effluents of wastewater treatment plants (WWTPs) represent a complex mixture of nutrients and toxic substances, thus, the potential exists for the effluents to significantly impact the biochemical characteristics and bacterial communities of the receiving water. We examined spatial and seasonal patterns, and the impact of effluents on microbial biomass, bacterial community structure, and metabolic diversity on a fourth-order stream. We took triplicate sediment samples at five different locations along a 5000 m transect over three sampling periods. We quantified bacterial community structure as community-level physiological profiles and microbial biomass with phospholipid phosphate analysis. Our findings highlight the worrisome impacts of effluents on microbial biomass and bacterial metabolic diversity on the receiving water. Microbial biomass was significantly higher at the WWTP outfall compared to upstream and downstream sites and correlated positively with sediment physicochemical parameters. Furthermore, our data revealed significant spatial differences in bacterial community structure in the context of WWTP impact. High nutrient availability (lower carbon/nitrogen ratios) at the outfall increased site-specific bacterial metabolic diversity in winter but decreased the same in fall. Seasonal changes in the sedimentary microbial biomass and bacterial carbon substrate utilization were evident regardless of the spatial variations or impacts of the wastewater effluents. Communities in fall showed more versatile substrate utilization patterns than the winter communities. These results suggest that WWTP effluents significantly increased microbial biomass and highlight its mixed effects on bacterial community structure and metabolic diversity. Also, our data underscore a close association between sedimentary physicochemical parameters and the associated microbial functional activities.

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Fig. 1
Fig. 2
Fig. 3

taken from Biolog EcoPlates of the sedimentary bacterial community structure of the Big Walnut Creek seasonal sampling site. The percentage in parentheses after the principal components indicate the percentage of total variance explained by each principal component. Scores are plotted by site and month. Se September 2019; Oc October 2019; Fe February 2020

Fig. 4
Fig. 5
Fig. 6

source utilization response, per site across sampling period at 120-h OD590 for the different guilds. A&A amines and amides; AA amino acids; C&AA carboxylic and acetic acids; Carb carbohydrates and Poly polymers

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References

  • Akinwole P, Kaplan L, Findlay R (2021) Elucidating stream bacteria utilizing terrestrial dissolved organic matter. World J Microbiol Biotechnol 37(2):1–13

    Article  CAS  Google Scholar 

  • Araya R, Tani K, Takagi T, Yamaguchi N, Nasu M (2003) Bacterial activity and community composition in stream water and biofilm from an urban river determined by fluorescent in situ hybridization and DGGE analysis. FEMS Microbiol Ecol 43(1):111–119

    Article  CAS  PubMed  Google Scholar 

  • Aristi I, von Schiller D, Arroita M, Barceló D, Ponsatí L, García-Galán MJ, Sabater S, Elosegi A, Acuña V (2015) Mixed effects of effluents from a wastewater treatment plant on river ecosystem metabolism: Subsidy or stress? Freshw Biol 60(7):1398–1410

    Article  CAS  Google Scholar 

  • Artigas J, Romani AM, Gaudes A, Munoz I, Sabater S (2009) Organic matter availability structures microbial biomass and activity in a Mediterranean stream. Freshw Biol 54(10):2025–2036

    Article  CAS  Google Scholar 

  • Battin TJ, Besemer K, Bengtsson MM, Romani AM, Packmann AI (2016) The ecology and biogeochemistry of stream biofilms. Nat Rev Microbiol 14:251–263

    Article  CAS  PubMed  Google Scholar 

  • Battin TJ, Kaplan LA, Newbold JD, Hendricks SP (2003) A mixing model analysis of stream solute dynamics and the contribution of a hyporheic zone to ecosystem function. Freshw Biol 48(6):995–1014

    Article  Google Scholar 

  • Böckelmann U, Manz W, Neu TR, Szewzyk U (2000) Characterization of the microbial community of lotic organic aggregates (‘river snow’) in the Elbe River of Germany by cultivation and molecular methods. FEMS Microbiol Ecol 33(2):157–170

    Article  Google Scholar 

  • Brummer IHM, Fehr W, Wagner-Dobler I (2000) Biofilm community structure in polluted rivers: abundance of dominant phylogenetic groups over a complete annual cycle. Appl Environ Microbiol 66:3078–3082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bueno MJM, Gomez MJ, Herrera S, Hernando MD, Agüera A, Fernández-Alba AR (2012) Occurrence and persistence of organic emerging contaminants and priority pollutants in five sewage treatment plants of Spain: two years pilot survey monitoring. Environ Pollut 164:267–273

    Article  CAS  PubMed  Google Scholar 

  • Button M, Nivala J, Weber KP, Aubron T, Müller RA (2015) Microbial community metabolic function in subsurface flow constructed wetlands of different designs. Ecol Eng 80:162–171

    Article  Google Scholar 

  • Cebron A, Coci M, Garnier J, Laanbroek HJ (2004) Denaturing gradient gel electrophoretic analysis of ammonia-oxidizing bacterial community structure in the lower seine river: impact of paris wastewater effluents. Appl Environ Microbiol 70(11):6726–6737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chevremont AC, Boudenne JL, Coulomb B, Farnet AM (2013) Impact of watering with UV-LED-treated wastewater on microbial and physico-chemical parameters of soil. Water Res 47(6):1971–1982

    Article  CAS  PubMed  Google Scholar 

  • Dang Q, Tan W, Zhao X, Li D, Li Y, Yang T, Li R, Zu G, Xi B (2019) Linking the response of soil microbial community structure in soils to long-term wastewater irrigation and soil depth. Sci Total Environ 688:26–36

    Article  CAS  PubMed  Google Scholar 

  • Drury B, Rosi-Marshall E, Kelly JJ (2013) Wastewater treatment effluent reduces the abundance and diversity of benthic bacterial communities in urban and suburban rivers. Appl Environ Microbiol 79(6):1897–1905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elósegui A, Arana X, Basaguren A, Pozo J (1995) Self-purification processes along a medium-sized stream. Environ Manage 19(6):931–939

    Article  Google Scholar 

  • Englert D, Zubrod JP, Schulz R, Bundschuh M (2013) Effects of municipal wastewater on aquatic ecosystem structure and function in the receiving stream. Sci Total Environ 454–455:401–410

    Article  PubMed  CAS  Google Scholar 

  • Feris KP, Ramsey PW, Frazar C, Rillig MC, Gannon JE, Holben WE (2003) Structure and seasonal dynamics of hyporheic zone microbial communities in free-stone rivers of the western United States. Microb Ecol 46:200–215

    CAS  PubMed  Google Scholar 

  • Findlay RH, King GM, Watling L (1989) Efficacy of phospholipid analysis in determining microbial biomass in sediments. Appl Environ Microbiol 55(11):2888–2893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Findlay S, Tank J, Dye S, Valett HM, Mulholland PJ, McDowell WH, Bowden WB (2002) A cross-system comparison of bacterial and fungal biomass in detritus pools of headwater streams. Microb Ecol 43(1):55–66

    Article  CAS  PubMed  Google Scholar 

  • Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57(8):2351–2359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gremm TJ, Kaplan LA (1998) Dissolved carbohydrate concentration, composition, and bioavailability to microbial heterotrophs in stream water. Acta Hydrochim Hydrobiol 26(3):167–171

    Article  CAS  Google Scholar 

  • Gryta A, Frąc M, Oszust K (2014) The Application of the Biolog EcoPlate approach in ecotoxicological evaluation of dairy sewage sludge. Appl Biochem Biotechnol 174(4):1434–1443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo Z, Han J, Li J, Xu Y, Wang X (2019) Effects of long-term fertilization on soil organic carbon mineralization and microbial community structure. PLOS One 14(1):e0211163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harbott EL, Grace MR (2005) Extracellular enzyme response to bioavailability of dissolved organic C in streams of varying catchment urbanization. J North Am Benthol Soc 24(3):588–601

    Article  Google Scholar 

  • Harch BD, Correll RL, Meech W, Kirkby CA, Pankhurst CE (1997) Using the Gini coefficient with BIOLOG substrate utilisation data to provide an alternative quantitative measure for comparing bacterial soil communities. J Microbiol Methods 30(1):91–101

    Article  CAS  Google Scholar 

  • Hullar MA, Kaplan LA, Stahl DA (2006) Recurring seasonal dynamics of microbial communities in stream habitats. Appl Environ Microbiol 72(1):713–722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jałowiecki Ł, Chojniak JM, Dorgeloh E, Hegedusova B, Ejhed H, Magnér J, Płaza GA (2016) Microbial community profiles in wastewaters from onsite wastewater treatment systems technology. PLOS One 11(1):e0147725

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Khan FA, Söderquist B, Jass J (2019) Prevalence and diversity of antibiotic resistance genes in swedish aquatic environments impacted by household and hospital wastewater. Front Microbiol 10:688

    Article  PubMed  PubMed Central  Google Scholar 

  • Kunhikrishnan A, Choppala G, Seshadri B, Wijesekara H, Bolan NS, Mbene K, Kim WI (2017) Impact of wastewater derived dissolved organic carbon on reduction, mobility, and bioavailability of As(V) and Cr(VI) in contaminated soils. J Environ Manage 186:183–191

    Article  CAS  PubMed  Google Scholar 

  • Ma X, Liu M, Li Z (2015) Changes in microbial properties and community composition in acid soils receiving wastewater from concentrated animal farming operations. Appl Soil Ecol 90:11–17

    Article  Google Scholar 

  • Magesan GN, Williamson JC, Yeates GW, Lloyd-Jones AR (2000) Wastewater C: N ratio effects on soil hydraulic conductivity and potential mechanisms for recovery. Bioresour Technol 71(1):21–27

    Article  CAS  Google Scholar 

  • Manz W, Eisenbrecher M, Neu TR, Szewzyk U (1998) Abundance and spatial organization of Gram-negative sulfate-reducing bacteria in activated sludge investigated by in situ probing with specific 16S rRNA targeted oligonucleotides. FEMS Microbiol Ecol 25(1):43–61

    Article  CAS  Google Scholar 

  • Mosher JJ, Findlay RH (2011) Direct and indirect influence of parental bedrock on streambed microbial community structure in forested streams. Appl Environ Microbiol 77(21):7681–7688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muñiz S, Lacarta J, Pata MP, Jiménez JJ, Navarro E (2014) Analysis of the diversity of substrate utilisation of soil bacteria exposed to cd and earthworm activity using generalised additive models. PLOS One 9(1):e85057

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nagy ZM, Gruiz K, Molnár M, Fenyvesi É (2013) Comparative evaluation of microbial and chemical methods for assessing 4-chlorophenol biodegradation in soil. Period Polytech Chem Eng 57(1–2):25–35

    Article  CAS  Google Scholar 

  • Nájera AF, Serwecińska L, Szklarek S, Mankiewicz-Boczek J (2020) Characterization and comparison of microbial communities in sequential sedimentation-biofiltration systems for removal of nutrients in urban rivers. Ecol Eng 149:105796

    Article  Google Scholar 

  • Nega M, Braun B, Künzel S, Szewzyk U (2019) Evaluating the impact of wastewater effluent on microbial communities in the Panke, an Urban River. Water 11(5):888

    Article  CAS  Google Scholar 

  • Oest A, Alsaffar A, Fenner M, Azzopardi D, Tiquia-Arashiro SM (2018) Patterns of change in metabolic capabilities of sediment microbial communities in river and lake ecosystems. Int J Microbiol 2018

  • Olapade OA, Leff LG (2004) Seasonal dynamics of bacterial assemblages in epilithic biofilms in a northeastern Ohio stream. J North Am Benthol Soc 23(4):686–700

    Article  Google Scholar 

  • Sabater F, Butturini A, MartÍ E, Muñoz I, Romaní A, Wray J, Sabater S (2000) Effects of riparian vegetation removal on nutrient retention in a Mediterranean stream. J North Am Benthol Soc 19(4):609–620

    Article  Google Scholar 

  • Sabri NA, Schmitt H, Van der Zaan B, Gerritsen HW, Zuidema T, Rijnaarts HHM, Langenhoff AAM (2020) Prevalence of antibiotics and antibiotic resistance genes in a wastewater effluent-receiving river in the Netherlands. J Environ Chem Eng 8(1):102245

    Article  CAS  Google Scholar 

  • Schloter M, Dilly O, Munch JC (2003) Indicators for evaluating soil quality. Agric Ecosyst Environ 98(1):255–262

    Article  Google Scholar 

  • Sekiguchi H, Watanabe M, Nakahara T, Xu B, Uchiyama H (2002) Succession of bacterial community structure along the Changjiang River determined by denaturing gradient gel electrophoresis and clone library analysis. Appl Environ Microbiol 68:5142–5150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suberkropp K (1997) Annual production of leaf-decaying fungi in a woodland stream. Freshw Biol 38(1):169–178

    Article  Google Scholar 

  • Tao Y, Dai T, Huang B, Wen D (2017) The impact of wastewater treatment effluent on microbial biomasses and diversities in coastal sediment microcosms of Hangzhou Bay. Mar Pollut Bull 114(1):355–363r

    Article  CAS  PubMed  Google Scholar 

  • Tank JL, Rosi-Marshall EJ, Griffiths NA, Entrekin SA, Stephen ML (2010) A review of allochthonous organic matter dynamics and metabolism in streams. J North Am Benthol Soc 29(1):118–146

    Article  Google Scholar 

  • Tiquia SM (2010) Metabolic diversity of the heterotrophic microorganisms and potential link to pollution of the Rouge River. Environ Pollut 158(5):1435–1443

    Article  CAS  PubMed  Google Scholar 

  • Tiquia SM, Schleibak M, Schlaff J, Floyd C, Benipal B, Zakhem E, Murray KS (2008) Microbial community profiling and characterization of some heterotrophic bacterial isolates from river waters and shallow groundwater wells along the Rouge River. Southeast Michigan Environ Tech 29(6):651–663

    Article  CAS  Google Scholar 

  • Treves DS, Xia B, Zhou J, Tiedje JM (2003) A two-species test of the hypothesis that spatial isolation influences microbial diversity in soil. Microb Ecol 45(1):20–28

    Article  CAS  PubMed  Google Scholar 

  • Urakawa H, Ali J, Ketover RD, Talmage SD, Garcia JC, Campbell IS, Parsons ML (2013) Shifts of bacterioplankton metabolic profiles along the salinity gradient in a subtropical estuary. ISRN 2013

  • Von Schiller D, Martí E, Riera JL, Ribot M, Marks JC, Sabater F (2008) Influence of land use on stream ecosystem function in a Mediterranean catchment. Freshw Biol 53(12):2600–2612

    Article  CAS  Google Scholar 

  • Wakelin SA, Colloff MJ, Kookana RS (2008) Effect of wastewater treatment plant effluent on microbial function and community structure in the sediment of a freshwater stream with variable seasonal flow. Appl Environ Microbiol 74(9):2659–2668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Shi J, Wang H, Lin Q, Chen X, Chen Y (2007a) The influence of soil heavy metals pollution on soil microbial biomass, enzyme activity, and community composition near a copper smelter. Ecotoxicol Environ Saf 67(1):75–81

    Article  CAS  PubMed  Google Scholar 

  • Wang YP, Houlton BZ, Field CB (2007b) A model of biogeochemical cycles of carbon, nitrogen, and phosphorus including symbiotic nitrogen fixation and phosphatase production. Global Biogeochem Cycles 21(1)

  • Wang M, Shen W, Yan L, Wang X-H, Xu H (2017) Stepwise impact of urban wastewater treatment on the bacterial community structure, antibiotic contents, and prevalence of antimicrobial resistance. Environ Pollut 231:1578–1585

    Article  CAS  PubMed  Google Scholar 

  • Weber KP, Legge RL (2009) One-dimensional metric for tracking bacterial community divergence using sole carbon source utilization patterns. J Microbiol Method 79(1):55–61

    Article  CAS  Google Scholar 

  • Westgate PJ, Park C (2010) Evaluation of proteins and organic nitrogen in wastewater treatment effluents. Environ Sci Technol 44(14):5352–5357

    Article  CAS  PubMed  Google Scholar 

  • Zeglin LH (2015) Stream microbial diversity in response to environmental changes: review and synthesis of existing research. Front Microbiol 6:454

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank Wendy Tomamichel and Beth Wilkerson of DePauw University for laboratory support and for reproducing DEM map/Fig. 1 respectively. DePauw University students; Anya Sanders and Emma Arndt helped with sample collections and processing. We also thank Steve Taylor for initial ground-truthing and site identification of the Big Walnut Creek.

Funding

Funding was provided by DePauw Science Research Fellows Program (to MD and SA), the Douglas A. and Phyllis G. Smith Endowed Fund for Student-Faculty Research, and the Faculty Development Program (to AG and PA), and Asher Fund in the sciences (to PA).

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  1. Biology Department, DePauw University, Greencastle, IN, 46135, USA

    Philips Akinwole, Amerti Guta, Madeline Draper & Sophia Atkinson

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  1. Philips Akinwole
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Correspondence to Philips Akinwole.

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Akinwole, P., Guta, A., Draper, M. et al. Spatio-temporal variations in the physiological profiles of streambed bacterial communities: implication of wastewater treatment plant effluents. World J Microbiol Biotechnol 37, 136 (2021). https://doi.org/10.1007/s11274-021-03106-2

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