Integrated metabolomic, molecular, and morphological insights into the degradation of polychlorinated biphenyls (PCB) by priestia megaterium mapb-27

Abstract

Polychlorinated biphenyls (PCBs) are persistent organic pollutants that cause profound deleterious effects on the environment and human health. Exposure to PCBs and biphenyl can induce changes in cellular metabolite levels. However, metabolic responses to utilize and adapt to PCBs are not well understood. Therefore, this study meticulously examined the PCB degradation potential, gene expression, and metabolic responses of Priestia megaterium MAPB-27 exposed to biphenyl. MAPB-27 showed growth and chemotaxis toward PCB degradation intermediates such as biphenyl, dihydroxy biphenyl, benzoate, and catechol. We employed GC-MS/MS to elucidate disparities in the main metabolic pathways in the biphenyl-exposed MAPB-27 through variations in metabolite composition and PCB biodegradation, while Field-emission scanning electron microscopy (FESEM) was used to study cell morphology. GC-MS/MS analysis highlighted the degradation of trichlorobiphenyl, tetrachlorobiphenyl, pentachlorobiphenyl, and hexachlorobiphenyl by P. megaterium MAPB-27, exhibiting 92.5, 62.9, 3.7, and 2.4%, respectively. GC-MS/MS analysis identified 4-dihydroxy-2-oxo-valerate, benzoic acid, and 2,3-dihydroxybenzoic acid as the major degradative metabolites in MAPB-27. MAPB-27 extract also contains metabolites with a wide range of direct industrial applications, such as poly(3-hydroxybutyrate) (3-hydroxybutyrate), a biobased organic acid (3-hydroxypropionoic acid), and antibacterial and antifungal compounds (phenyllactic acid, 4-hydroxyphenyllactic acid, and β-sitosterol). Glyoxylate and dicarboxylate metabolism and fatty acid biosynthesis were observed to be the active metabolisms in MAPB-27 grown in biphenyl-supplemented Minimal Medium. Overall, the results of this study provided important insights into microbial adaptation to biphenyl and the biodegradation of PCB. Thus, the P. megaterium MAPB-27 strain can be used for the development of efficient PCB biodegradation strategies and for the exploration of industrial applications.