title: Microbial degradation of organic micropollutants in hyporheic zone sediments
Creators: name: Rutere, Cyrus
Publisher: name: University of Bayreuth
Year: 2020
Subjects: subject: Hyporheic zone
subject: sediments
subject: organic micropollutants
subject: biodegradation
subject: microbial ecology
subject: aquatic ecosystems
subject: 500

description: The hyporheic zone is the water-saturated streambed sediment layer characterized by the simultaneous occurrence of multiple physical, biological, and chemical processes. The hyporheic zone contributes to the self-purification capacity of streams by removing point and nonpoint source pollutants mainly via microbial activity. However, such potentials, associated microbial communities, and impacts on microbial community structure are largely unknown for specific widely distributed compounds of environmental concern. Thus, pollutant removal potentials in hyporheic zone sediments were investigated using the non-steroidal anti-inflammatory drug ibuprofen. Ibuprofen biodegradation in oxic sediment microcosms amended with ibuprofen, or ibuprofen and acetate was determined. Unsupplemented and heat-sterilized sediments served as controls. Ibuprofen biotransformation occurred via 1-, 2-, 3-hydroxy and carboxy-ibuprofen as transient primary transformation products. Quantitative PCR analysis revealed a significantly higher 16S rRNA abundance in ibuprofen-amended relative to un-amended incubations. Time-resolved amplicon Illumina MiSeq sequencing targeting 16S rRNA genes and 16S rRNA revealed a clear effect of ibuprofen on the microbial community structure and many new ibuprofen responsive taxa affiliating with Acidobacteria, Actinobacteria, Bacteroidetes, Gemmatimonadetes, Latescibacteria and Proteobacteria. This was confirmed by specific 16S rRNA gene expression analysis of representative taxa. Two strains utilizing ibuprofen as sole carbon and energy source of the genera Novosphingobium and Pseudomonas were isolated and will serve as model organisms for elucidating ibuprofen degradation pathways. Redox gradients along the streambed depth profile impact pollutant removal. Microbial removal of the beta-blocker metoprolol, in the redox-delineated hyporheic zones was investigated using oxic and anoxic sediment microcosms. Biotransformation of metoprolol occurred under both incubation conditions. In the oxic microcosms, metoprolol was transformed mainly to metoprolol acid, while under anoxic conditions, metoprolol acid and hydroxy metoprolol were formed, indicating dissimilar metabolic pathways for metoprolol degradation under the contrasting incubation conditions. The transformation products were subsequently completely degraded under both conditions. The responsive taxa associated with metoprolol degradation were affiliated with the Proteobacteria and Bacteroidetes under oxic conditions, and Proteobacteria, Acidobacteria, Chloroflexi, Firmicutes and Gemmatimonadetes under anoxic conditions. The organic matter content influences multiple biogeochemical reactions. The effect of organic carbon on the fate of 13 trace organic compounds (TrOCs) was investigated using sediments differing in the total organic carbon content (TOC). Oxic sediment microcosms with low and high TOC content differed in the biotransformation and sorption removal efficiencies of the TrOCs. Significantly higher biotic removal efficiencies of compounds such as ibuprofen, ketoprofen and acesulfame were observed in high relative to low TOC sediments. The removal efficiency via biotransformation was generally higher than by sorption for all compounds tested except for propranolol for which complete removal occurred via both mechanisms. Acesulfame removal via sorption was marginal. Quantitative PCR and 16S rRNA gene amplicon Illumina MiSeq sequencing suggested that higher removal efficiencies of most compounds correlated with high bacterial abundance, diversity, and high TOC. The bacterial community in high-TOC sediment samples was more stable to TrOC additions compared to the community in low TOC sediments. Latter communities were characterized by a decline in the relative abundance of most phyla except Proteobacteria. Bacterial families enriched in the presence of TrOCs relative to unamended controls included Methylophilaceae, Caldilineaceae, Acidimicrobiaceae, Xanthobacteriaceae, Hydrogenophiliaceae, Rhodospirillaceae Gemmatimonadaceae and Rhodocyclaceae, suggesting either resistance to or stimulation by suplemental TrOCs. Bedform features such as ripples and dunes alter hyporheic exchange fluxes and porewater residence times. The contribution of bedform features and microbial diversity on the attenuation of TrOCs was investigated by measuring the dissipation half-lives (DT50s) of 31 TrOCs (mainly pharmaceuticals) under different combinations of bacterial diversity and bedforms using 20 recirculating flumes in a central composite face factorial design. Using targeted and suspect screening, quantitative PCR and time-resolved amplicon Illumina MiSeq sequencing, a set of DT50s and microbial transformation products were determined. About 20 compounds responded significantly to bacterial diversity and four to both diversity and hyporheic flow. Bacterial taxa abundant in microbial communities supporting biodegradation of the test compounds included Acidobacteria (groups 6, 17, and 22), Actinobacteria (Nocardioides and Illumatobacter), Bacteroidetes (Terrimonas and Flavobacterium) and diverse Proteobacteria (Pseudomonadaceae, Sphingomonadaceae, and Xanthomonadaceae). The collective results indicated that the hyporheic zone sustains (i) efficient biotic (trace) organic pollutant degradation of diverse compounds, and (ii) hitherto unknown microbial communities catalyzing (trace) organic pollutant removal. Results further suggest that (iii) TOC content affects removal efficiency of some TrOCs by directly impacting the microbial community dynamics and associated biotransformation processes, (iv) microbial diversity is the primary driver of biotransformation processes in the hyporheic zone, and (v) the interplay of the physical, biological, and chemical processes contributes to improved attenuation of TrOCs in the hyporheic zone. Thus, the hyporheic zone is a reservoir of hitherto unknown microbial biodiversity providing an essential ecosystem service.