Complementary Biotransformation of Antimicrobial Triclocarban Obviously Mitigates Nitrous Oxide Emission toward Sustainable Microbial Denitrification

Abstract

Sustainable nitrogen cycle is an essential biogeochemical process that ensures ecosystem safety and byproduct greenhouse gas nitrous oxide reduction. Antimicrobials are always co-occurring with anthropogenic reactive nitrogen sources. However, their impacts on the ecological safety of microbial nitrogen cycle remain poorly understood. Here, a denitrifying bacterial strain Paracoccus denitrificans PD1222 was exposed to a widespread broad-spectrum antimicrobial triclocarban (TCC) at environmental concentrations. The denitrification was hindered by TCC at 25 μg L–1 and was completely inhibited once the TCC concentration exceeded 50 μg L–1. Importantly, the accumulation of N2O at 25 μg L–1 of TCC was 813 times as much as the control group without TCC, which attributed to the significantly downregulated expression of nitrous oxide reductase and the genes related to electron transfer, iron, and sulfur metabolism under TCC stress. Interestingly, combining TCC-degrading denitrifying Ochrobactrum sp. TCC-2 with strain PD1222 promoted the denitrification process and mitigated N2O emission by 2 orders of magnitude. We further consolidated the importance of complementary detoxification by introducing a TCC-hydrolyzing amidase gene tccA from strain TCC-2 into strain PD1222, which successfully protected strain PD1222 against the TCC stress. This study highlights an important link between TCC detoxification and sustainable denitrification and suggests a necessity to assess the ecological risks of antimicrobials in the context of climate change and ecosystem safety.

Ecological Trait-Based Digital Categorization of Microbial Genomes for Denitrification Potential

“…For example, a recent report experimentally combined two denitrifying bacteria strains, Paracoccus denitrificans PD1222 and Ochrobactrum sp. TCC-2, to mitigate nitrous oxide emission and detoxify triclocarban, a widespread broad-spectrum antimicrobial [91]. Our microbial denitrification dataset contains 96 strains of Paracoccus and 77 strains of Ochrobactrum (including those previously classified as the Bacillus genus).…”

“…The presence of antimicrobial resistance genes has been documented in strains of Arcobacteraceae [94]. Antimicrobials such as triclocarban that occur with anthropogenic reactive nitrogen sources in the environment can affect the efficiency of denitrification [91]. There is a need to investigate denitrifying Arcobacteraceae for effects of antimicrobials on denitrification rates.…”

Groundwater redox dynamics across the terrestrial-aquatic interface of Lake Erie coastal ecosystems

“…Aquifer charging and discharging regimes can alter the redox state of groundwater and promote chemical reactions that affect concentrations of dissolved constituents. For instance, denitrification is a preferable microbial metabolic pathway in the absence of dissolved oxygen due to high energetic yields, removing nitrate and eventually producing nitrous oxide (Zhang et al 2023). The biogeochemistry of iron and sulfur also plays a vital role in redoximorphic systems, mediating important transformations and reactions within these environments (Fan et al 2017;Frohne et al 2011;Fulda et al 2013).…”