Proteomic and metabolic profiling reveals molecular phenotype associated with chemotrophic growth of JA2 on L-tryptophan.

strain JA2 is an anoxygenic phototrophic bacterium, able to grow under different growth modes. Particularly under chemotrophic conditions, it produces novel Trp-melanin, anthocyanin-like, and pyomelanin pigments. However, the underlying molecular adaptations of strain JA2 that lead to the formation of novel metabolites under chemotrophic conditions remain unexplored. The present study used iTRAQ-based global proteomic and metabolite profiling to unravel the biochemical processes operating under the L-tryptophan-fed chemotrophic state. Exometabolite profiling of L-tryptophan fed chemotrophic cultures revealed production of diverse indolic metabolites, many of which are hydroxyindole derivatives, along with unique pigmented metabolites. Proteomic profiling revealed a global shift in the proteome and detected 2411 proteins, corresponding to 61.8% proteins expressed. Proteins related to signalling, transcription-coupled translation, stress, membrane transport, and metabolism were highly differentially regulated. Extensive rewiring of amino acid, fatty acid, lipid, and energy metabolism was observed under L-tyrptophan fed chemotrophic conditions. Moreover, energy conservation and cell protection strategies such as efflux pumps involved in the efflux of aromatic compounds were activated. The study demonstrated a correlation between some of the detected indole derivatives and the up-regulation of proteins associated with L-tryptophan catabolism, indicating a possible role of aromatic mono/dioxygenases in the formation of hydroxyindole derivatives and pigments under chemotrophic conditions. The overall study revealed metabolic flexibility in utilizing aromatic compounds and molecular adaptations of strain JA2 under the chemotrophic state.