Plasticity of Streptomyces coelicolor Membrane Composition Under Different Growth Conditions and During Development

Abstract

Streptomyces coelicolor is a model actinomycete that is well known for the diversity of its secondary metabolism and its complex life cycle. As a soil inhabitant, it is exposed to heterogeneous and frequently changing environmental circumstances. In the present work, we studied the effect of diverse growth conditions and phosphate depletion on its lipid profile and the relationship between membrane lipid composition and development in S. coelicolor. The lipid profile from cultures grown on solid media, which is closer to the natural habitat of this microorganism, does not resemble the previously reported lipid composition from liquid grown cultures of S. coelicolor. Wide variations were also observed across different media, growth phases, and developmental stages indicating active membrane remodeling. Ornithine lipids (OL) are phosphorus-free polar lipids that were accumulated mainly during sporulation stages, but were also major components of the membrane under phosphorus limitation. In contrast, phosphatidylethanolamine, which had been reported as one of the major polar lipids in the genus Streptomyces, is almost absent under these conditions. We identified one of the genes responsible for the synthesis of OL (SCO0921) and found that its inactivation causes the absence of OL, precocious morphological development and actinorhodin production. Our observations indicate a remarkable plasticity of the membrane composition in this bacterial species, reveal a higher metabolic complexity than expected, and suggest a relationship between cytoplasmic membrane components and the differentiation programs in S. coelicolor.

Knowns and unknowns of membrane lipid synthesis in streptomycetes

“…1). These two anionic lipids have been found in S. coelicolor and S. hygroscopicus [14, 21, 32] and may be more widespread in this genus. It is possible that both MLCL and DLCL are derived from CL by partial deacylation, but no phospholipase with this activity has yet been found in bacteria.…”

“…It is possible that both MLCL and DLCL are derived from CL by partial deacylation, but no phospholipase with this activity has yet been found in bacteria. Both MLCL and DLCL have been found as major components in some growth conditions in S. coelicolor [14], and CL synthase is an essential gene in this same species [13], so perhaps these CL-related molecules are required for some cellular processes in streptomycetes.…”

“…Two separate spots corresponding to OL were found in S. hygroscopicus [31]. In the model streptomycete S. coelicolor, OL has also been associated to phosphate starvation and is accumulated during aerial hyphae erection and sporulation [14]. Even considering all those reports, OL was frequently ignored in systematics as a component of streptomycete membranes [30], perhaps due to its apparent absence in some species or to its conditional synthesis associated with phosphorus limitation.…”

“…3), and it has been corroborated that SCO0921 (OlsB) is required for OL synthesis in S. coelicolor [14]. SCO0920 is predicted to code for OlsA, since it is well conserved, is in an apparent operon with olsB , and the encoded protein has an acyltransferase domain [14]. Homologues to olsB and olsA are widespread in actinomycetes.…”

“…Some phospholipid biosynthesis pathways have been studied in the genus Mycobacterium , where several essential genes involved in phospholipid synthesis have been discovered [11, 12]. Recent research has also discovered essential lipids in Streptomyces [13] and a remarkable variability in the composition of its cytoplasmic membrane [14]. …”