Pathway crosstalk enables degradation of aromatic compounds in marine Roseobacter clade bacteria

Abstract

Aromatic compounds are essential raw materials for almost all sectors of human societies but also persistent environmental pollutants recalcitrant to biodegradation. The ocean serves as a significant sink for these compounds, while their biological conversion routes remain poorly understood, hindering a comprehensive understanding of the marine carbon cycle and advancements in bioremediation and biological carbon upcycling. Here, we report the degradation pathway of aromatic molecules in the marine Roseobacter clade bacteria through multi-omics analysis and CRISPR-Cas-based genome editing. Using Roseovarius nubinhibens and 4-hydroxybenzoate (4HB) as representatives, we identified the transport of 4HB via TRAP, ABC, and MFS transporters. Then, we deciphered the integral β-ketoadipate pathway responsible for aromatic degradation. Next, we discovered a distinct pathway crosstalk at the final thiolation step, which serves as an intersection node of different pathways catalyzed by the 3-oxoadipyl-CoA thiolase from the β-ketoadipate pathway and the acetyl-CoA C-acetyltransferase and acetyl-CoA C-acyltransferase from the β-oxidation pathway. Finally, we proposed R. nubinhibens as a novel marine platform for systems-level interrogation and bioprospecting. Our study provides a foundation for leveraging Roseobacter clade bacteria as novel chassis for environmental and industrial innovations.