Interactions between a Methanogenic Archaeon and Synthetic Musk Tonalide: A Balance of Cellular Inhibition and Detoxifying Biotransformation

Abstract

The widespread use of synthetic musks, such as tonalide (AHTN), has led to their accumulation in anaerobic environments, such as sludge and sediments, raising concerns about their ecological impact. While methanogenic archaea are key ecological players in these environments, their responses to synthetic musks remain poorly understood. This study provides a systematic investigation of the interaction between AHTN and model methanogenic archaeon Methanosarcina acetivorans C2A. We found that AHTN toxicity is dependent on concentration, with 2 mg/L significantly inhibiting methanogenesis and growth by inducing oxidative stress and compromising cell membrane integrity. Despite this effect, M. acetivorans C2A was found to partially biotransform AHTN, achieving a value of 17.75% within 36 h. Using GC-MS/MS, six mono- and dihydroxylated metabolites were tentatively identified, indicating oxidation as the primary transformation mechanism. Notably, ecotoxicity modeling (ECOSAR) predicted these metabolites to be substantially less toxic than the parent AHTN, suggesting that this biotransformation is a detoxification pathway. These findings present the first evidence of archaeally mediated biotransformation of AHTN, revealing a dual role for methanogens as both targets of pollution and active agents in its natural attenuation.