Pharmaceutical Biotransformation is Influenced by Photosynthesis and Microbial Nitrogen Cycling in a Benthic Wetland Biomat

In shallow, open-water engineered
wetlands, design parameters
select
for a photosynthetic microbial biomat capable of robust pharmaceutical
biotransformation, yet the contributions of specific microbial processes
remain unclear. Here, we combined genome-resolved metatranscriptomics
and oxygen profiling of a field-scale biomat to inform laboratory
inhibition microcosms amended with a suite of pharmaceuticals. Our
analyses revealed a dynamic surficial layer harboring oxic–anoxic
cycling and simultaneous photosynthetic, nitrifying, and denitrifying
microbial transcription spanning nine bacterial phyla, with unbinned
eukaryotic scaffolds suggesting a dominance of diatoms. In the laboratory,
photosynthesis, nitrification, and denitrification were broadly decoupled
by incubating oxic and anoxic microcosms in the presence and absence
of light and nitrogen cycling enzyme inhibitors. Through combining
microcosm inhibition data with field-scale metagenomics, we inferred
microbial clades responsible for biotransformation associated with
membrane-bound nitrate reductase activity (emtricitabine, trimethoprim,
and atenolol), nitrous oxide reduction (trimethoprim), ammonium oxidation
(trimethoprim and emtricitabine), and photosynthesis (metoprolol).
Monitoring of transformation products of atenolol and emtricitabine
confirmed that inhibition was specific to biotransformation and highlighted
the value of oscillating redox environments for the further transformation
of atenolol acid. Our findings shed light on microbial processes contributing
to pharmaceutical biotransformation in open-water wetlands with implications
for similar nature-based treatment systems.