From Northwest Passage shores to molecular pathways: Comparative transcriptomic responses of a novel Arctic marine fuel-degrading Flavobacterium species

ABSTRACT Accelerated sea-ice decline is opening the Arctic to increased shipping, elevating the risk of marine fuel spills in fragile ecosystems where extreme cold and remoteness limit cleanup options. While microbial biodegradation is the primary removal mechanism, the metabolic strategies of abundant polar taxa remain poorly understood, particularly those lacking canonical degradation genes. We characterized the hydrocarbon degradation mechanisms of Flavobacterium sp. strain R2B_3I, a psychrotolerant isolate from high Arctic beach sediments in Resolute Bay, Nunavut, Canada. During three-month incubations with ultra-low sulfur fuel oil at 4 °C, R2B_3I mounted a systems-level response involving the upregulation of diverse non-canonical oxidoreductases, membrane remodeling systems, cold-shock, and oxidative stress defenses. Crucially, this strain achieved efficient degradation in the complete absence of alkB alkane hydroxylases, challenging the reliance on alkB as a universal biomarker for hydrocarbon biodegradation. Transcriptomic analysis revealed distinct temporal shifts, linking specific gene clusters to the degradation of complex petroleum mixtures under environmentally relevant conditions. These results demonstrate that Flavobacterium, a dominant genus in polar oceans, utilize a “cryptic” metabolic network to process hydrocarbons, effectively bypassing the pathways typically monitored in environmental surveys. By uncovering alternative mechanisms, our study revises current models of microbial oil degradation, highlighting the overlooked potential of non-canonical degraders in determining the fate of marine fuel spills in a warming Arctic. Competing Interest Statement The authors have declared no competing interest. Footnotes INSTITUTIONAL EMAIL ADDRESS: Nastasia J. Freyria: nastasia.freyria{at}mcgill.ca Antoine-Olivier Lirette: a-o.lirette{at}hotmail.com Charles W. Greer: cwgreer0{at}gmail.com Lyle G. Whyte: lyle.whyte{at}mcgill.ca