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Unlike the majority of actinomycete secondary metabolic pathways, the biosynthesis of peptidoglycan glycosyltransferase inhibitor moenomycin in  Streptomyces ghanaensis  does not involve any cluster-situated regulators (CSRs). This raises questions about the regulatory signals that initiate and sustain moenomycin production. We now show that three pleiotropic regulatory genes for  Streptomyces  morphogenesis and antibiotic production— bldA ,  adpA  and  absB —exert multi-layered control over moenomycin biosynthesis in native and heterologous producers. The  bldA  gene for tRNA Leu  UAA  is required for the translation of rare UUA codons within two key moenomycin biosynthetic genes ( moe ),  moeO5  and  moeE5 . It also indirectly influences moenomycin production by controlling the translation of the UUA-containing  adpA  and, probably, other as-yet-unknown repressor gene(s). AdpA binds key  moe  promoters and activates them. Furthermore, AdpA interacts with the  bldA  promoter, thus impacting translation of  bldA -dependent mRNAs—that of  adpA  and several  moe  genes. Both  adpA  expression and moenomycin production are increased in an  absB- deficient background, most probably because AbsB normally limits  adpA  mRNA abundance through ribonucleolytic cleavage. Our work highlights an underappreciated strategy for secondary metabolism regulation, in which the interaction between structural genes and pleiotropic regulators is  not  mediated by CSRs. This strategy might be relevant for a growing number of CSR-free gene clusters unearthed during actinomycete genome mining.

Pleiotropic regulatory genes bldA , adpA and absB are implicated in production of phosphoglycolipid antibiotic moenomycin