Wastewater microorganisms impact microbial diversity and important ecological functions of stream periphyton

Carles, Louis; Wullschleger, Simon; Joss, Adriano; Eggen, Rik I.L.; Schirmer, Kristin; Schuwirth, Nele; Stamm, Christian; Tlili, Ahmed

doi:10.1016/j.watres.2022.119119

Cited by 15 publications

(14 citation statements)

References 75 publications

(123 reference statements)

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“…To investigate the functional genes involved in TrOC biotransformations, we conducted deep shotgun metagenomic sequencing (up to 200 million reads per sample, Table S1) for 75 samples including WW-grown biofilms, WW, and stream water. In line with previous 16S rRNA sequencing results (Carles et al, 2022), shotgun metagenomic analysis demonstrated the microbial community structures of the biofilms, WW, and stream water samples were significantly influenced by the ratio of treated WW relative to stream water (Figure S5). Specifically, in our metagenomic analysis of the biofilm samples, we observed the relative abundance of Chloroflexota, Desulfobacterota, and Myxococcota increased from 0% to 80% treated WW (log 2 Fold-change > 2; normalized mean baseline counts > 240, Figure S5).…”

Section: Resultssupporting

confidence: 89%

“…Specifically, in our metagenomic analysis of the biofilm samples, we observed the relative abundance of Chloroflexota, Desulfobacterota, and Myxococcota increased from 0% to 80% treated WW (log 2 Fold-change > 2; normalized mean baseline counts > 240, Figure S5). In agreement with the 16S rRNA analysis by (Carles et al, 2022), Cyanobacteria relative abundance decreased with increasing treated WW%.…”

Section: Resultssupporting

confidence: 87%

“…Biofilms were grown on glass slides placed in these flow-through channels for four weeks. Biofilms from different glass slides within the same channel were scraped independently to form biological replicates (n=4 for each treatment) and suspended in 400 mL of artificial river water (Carles et al, 2022(Carles et al, , 2021Desiante et al, 2022).…”

Section: Biofilm Samplingmentioning

confidence: 99%

“…Freshwater biofilms are ideal systems for investigating TrOC biotransformation processes due to their complex microbial community composition and critical ecological function in aquatic environments (Battin et al, 2016; Desiante et al, 2021). Most biofilm studies have been conducted using marker gene sequencing to profile taxonomic composition and community shifts that correlate with TrOC biotransformations in treated wastewater (Carles et al, 2022, 2021; Desiante et al, 2022; Mansfeldt et al, 2020; Tien et al, 2013). Metagenomics and metatranscriptomics analyses have recently deepened the resolution of community analysis to identify functional shifts in TrOC-exposed engineered wetland biomats, yet the molecular mechanisms of TrOC biotransformations in freshwater biofilms or biomats remain poorly studied relative to other systems such as enriched soil consortia (Vasileiadis et al, 2022) or activated sludge (Rich and Helbling, 2023; Vasileiadis et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

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Substrate promiscuity of xenobiotic-transforming hydrolases from stream biofilms impacted by treated wastewater

Yu,

Trottmann,

Schärer

et al. 2023

Preprint

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Organic contaminants enter aquatic ecosystems from various sources, including through the effluents of wastewater treatment plants. Freshwater biofilms play a major role in the removal of organic contaminants from receiving water bodies, but knowledge of the molecular mechanisms driving contaminant biotransformations in complex biofilm communities remains limited. Previously, we demonstrated that biofilms in experimental flume systems grown at higher ratios of treated wastewater (WW) to stream water displayed an increased biotransformation potential for a number of organic contaminants. Specifically, we identified a positive correlation between WW percentage and biofilm biotransformation rates for the widely-used insect repellent,N,N-diethyl-meta-toluamide (DEET). Here, we conducted deep shotgun sequencing of flume biofilms and identified a positive correlation between WW percentage and metagenomic read abundances of DEET hydrolase (DH) homologs. To test the causality of this association, we constructed a targeted metagenomic library of DH homologs from flume biofilms. We screened our complete metagenomic library for activity with four different substrates and a subset thereof with 183 WW-related organic compounds. The majority of active hydrolases in our library preferred aliphatic and aromatic ester substrates while, remarkably, only a single reference enzyme was capable of DEET hydrolysis. Of the 626 total enzyme-substrate combinations tested, approximately 5% were active enzyme-substrate pairs. Metagenomic DH family homologs revealed a broad substrate promiscuity spanning 22 different compounds when summed across all enzymes tested. We biochemically characterized the most promiscuous and active enzymes identified based on metagenomic analysis from uncultivatedRhodospirillaceaeandPlanctomycetaceae. In addition to uncovering new DH family enzymes, we exemplified a framework for linking metagenome-guided hypothesis generation with experimental validation. Overall, this study expands the scope of known enzymatic contaminant biotransformations for metagenomic hydrolases from WW-receiving stream biofilm communities.SynopsisWe aimed to connect contaminant biotransformations to their responsible enzymes within complex microbiomes by testing substrate specificity of enzymes from stream metagenomes for their activity with 183 wastewater-relevant organic contaminants.

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Section: Resultssupporting

confidence: 89%

Section: Resultssupporting

confidence: 87%

Section: Biofilm Samplingmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Substrate promiscuity of xenobiotic-transforming hydrolases from stream biofilms impacted by treated wastewater

Yu,

Trottmann,

Schärer

et al. 2023

Preprint

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“…The taxonomic composition of biofilms grown in UF WW was more similar to that of biofilms grown in 0% WW than to biofilms grown in non-UF WW, suggesting that biotic factors from WWTPs play a greater role in changes in the stream biofilm community than abiotic factors (Figure 2, Figure S3). Metagenomic taxonomic analysis demonstrated that WW alters stream biofilm composition, supporting previous studies that some microorganisms from WW are able to colonize and modify biofilm community composition [27]. To leverage the shotgun metagenomic data, we investigated whether treatment also altered the composition of functional enzyme diversity (see Methods).…”

Section: Biotic Factors Are More Dominant Than Abiotic Factors For Al...supporting

confidence: 62%

Disentangling abiotic and biotic effects of treated wastewater on stream biofilm resistomes enables the discovery of a new planctomycete beta-lactamase

Attrah,

Schärer,

Esposito

et al. 2023

Preprint

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Antibiotic resistance, mediated by environmental reservoirs, poses a threat to human and animal health. Aquatic biofilms impacted by treated wastewater (WW) are known environmental reservoirs for antibiotic resistance, but it remains unclear if primarily biotic or abiotic factors from WW influence the abundance and dissemination of antibiotic resistance genes within biofilm communities. To disentangle these factors, natural biofilms were previously grown in flume systems with different proportions of stream water and either ultrafiltered or non-ultrafiltered treated WW. In this study, we conducted deep shotgun metagenomic sequencing of 75 biofilm, stream, and WW samples from these flume systems and compared microbiome and resistome composition. Our analysis revealed a strong relationship between the resistome and prokaryotic microbiome composition which was also associated with experimental treatment. Within biofilm communities exposed to increasing percentages of WW, we observed a decrease in the relative abundances of Cyanobacteriota and Verrucomicrobiota, while Bacteroidota increased. Notably, several antibiotic resistance genes (ARGs) exhibited a significant increase in abundance in biofilms grown with increasing WW%, while a small number of sulfonamide and beta-lactamase ARGs showed higher abundance when biofilms were instead grown in ultrafiltered WW. Overall, our results pointed toward the dominance of biotic over abiotic factors in determining ARG abundances in WW-impacted stream biofilms. However, some ARGs exhibited divergent abundance patterns through proposed gene family-specific mechanisms. To investigate these gene families experimentally, we biochemically characterized a new, sequence-divergent beta-lactamase from planctomycetes abundant in stream biofilms and in WW. This ARG discovery is noteworthy, not only due to its unusual source organism belonging to the phylum Planctomycetota, but also because it was not detected by standard computational ARG tools. This underpins the need for continued development of ARG detection methods using workflows within silicosequence and structure analysis coupled toin vitrofunctional characterization. In summary, this study assessed the relative importance of biotic and abiotic factors in the context of WW discharge and its impact on antibiotic resistance genes in aquatic ecosystems.

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Microbial community structure and diversity attached to the periphyton in different urban aquatic habitats

Yang,

Zhou,

Pang

et al. 2024

Environ Monit Assess

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Wastewater microorganisms impact microbial diversity and important ecological functions of stream periphyton

Cited by 15 publications

References 75 publications

Substrate promiscuity of xenobiotic-transforming hydrolases from stream biofilms impacted by treated wastewater

Substrate promiscuity of xenobiotic-transforming hydrolases from stream biofilms impacted by treated wastewater

Disentangling abiotic and biotic effects of treated wastewater on stream biofilm resistomes enables the discovery of a new planctomycete beta-lactamase

Microbial community structure and diversity attached to the periphyton in different urban aquatic habitats

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