Spo0A links de novo fatty acid synthesis to sporulation and biofilm development in Bacillus subtilis

Abstract

SummaryDuring sporulation in Bacillus subtilis, the committedcell undergoes substantial membrane rearrangements to generate two cells of different sizes and fates: the mother cell and the forespore. Here, we demonstrate that the master transcription factor Spo0A reactivates lipid synthesis during development. Maximal Spo0A-dependent lipid synthesis occurs during the key stages of asymmetric division and forespore engulfment. Spo0A reactivates the accDA operon that encodes the carboxylase component of the acetylCoA carboxylase enzyme, which catalyses the first and rate-limiting step in de novo lipid biosynthesis, malonyl-CoA formation. The disruption of the Spo0A-binding box in the promoter region of accDA impairs its transcriptional reactivation and blocks lipid synthesis. The Spo0A-insensitive accDA 0A cells were proficient in planktonic growth but defective in sporulation (s E activation) and biofilm development (cell cluster formation and water repellency). Exogenous fatty acid supplementation to accDA 0A cells overcomes their inability to synthesize lipids during development and restores sporulation and biofilm proficiencies. The transient exclusion of the lipid synthesis regulon from the forespore and the known compartmentalization of Spo0A and ACP in the mother cell suggest that de novo lipid synthesis is confined to the mother cell. The significance of the Spo0A-controlled de novo lipid synthesis during B. subtilis development is discussed.

Neuraminidase A-Exposed Galactose Promotes Streptococcus pneumoniae Biofilm Formation during Colonization

“…Spo0A, a transcriptional regulator of spore formation in B. subtilis, has also been identified as a regulator of de novo fatty acid synthesis and was found to be required for biofilm formation. The inability of an Spo0A-deficient mutant to form biofilms in vitro was restored by exogenous fatty acid supplementation (69). Likewise, fatty acid kinase A has been shown to be an important determinant of biofilm formation in Staphylococcus aureus strain USA300 (70).…”

The Role of Lipid Domains in Bacterial Cell Processes

“…In B. subtilis , the phospholipid composition remained relatively unchanged during exponential growth, but the amount of PG slightly decreased while the amount of PE slightly increased during stationary growth. It has also been shown that the phospholipid composition of the forespore membrane changes during early stages of sporulation in B. subtilis [14]. …”

“…These sigma factors, subunits of RNA polymerase, recognize specific sets of promoter sequences and allow transcription of different genes. Recently, it was discovered that Spo0A reactivates de novo fatty acid and phospholipids synthesis for membrane biogenesis during transient genetic asymmetry and after asymmetric cell division [14]. These authors suggested that de novo lipid synthesis was asymmetrically excluded from the forespore (Figure 1D).…”

A model of cell-wall dynamics during sporulation inBacillus subtilis

“…Similar to Ref. 1, we focused on the cell wall, but in the ESI † we also considered the role of the membrane [14] (Figs. S1a-b in ESI †).…”

“…The mother cell synthesizes considerable amounts of membrane, also required for compartment-specific expression of transcription factors [14,21]. To study the effect of membrane synthesis on the cell wall, we extended the minimal model in the ESI † to include the membrane surface areas (Fig.…”