A highly coordinated cell wall degradation machine governs spore morphogenesis in Bacillus subtilis.
How proteins catalyze morphogenesis is an outstanding question in developmental biology. In bacteria, morphogenesis is intimately linked to remodeling the cell wall exoskeleton. Here, we investigate the mechanisms by which the mother cell engulfs the prospective spore during sporulation in Bacillus subtilis. A membrane-anchored protein complex containing two cell wall hydrolases plays a central role in this morphological process. We demonstrate that one of the proteins (SpoIIP) has both amidase and endopeptidase activities, such that it removes the stem peptides from the cell wall and cleaves the cross-links between them. We further show that the other protein (SpoIID) is the founding member of a new family of lytic transglycosylases that degrades the glycan strands of the peptidoglycan into disaccharide units. Importantly, we show that SpoIID binds the cell wall, but will only cleave the glycan strands after the stem peptides have been removed. Finally, we demonstrate that SpoIID also functions as an enhancer of SpoIIP activity. Thus, this membrane-anchored enzyme complex is endowed with complementary, sequential, and stimulatory activities. These activities provide a mechanism for processive cell wall degradation, supporting a model in which circumferentially distributed degradation machines function as motors pulling the mother cell membranes around the forespore.
Morlot
Cecile
C
Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA.
Uehara
Tsuyoshi
T
Marquis
Kathleen A
KA
Bernhardt
Thomas G
TG
Rudner
David Z
DZ
D000581:Amidohydrolases / Q000378:metabolism; D000595:Amino Acid Sequence; D001412:Bacillus subtilis / Q000201:enzymology / Q000502:physiology*; D001426:Bacterial Proteins / Q000737:chemistry / Q000378:metabolism; D002473:Cell Wall / Q000378:metabolism*; D004268:DNA-Binding Proteins / Q000737:chemistry / Q000378:metabolism; D010450:Endopeptidases / Q000378:metabolism; D008969:Molecular Sequence Data; D011134:Polysaccharides / Q000378:metabolism; D016415:Sequence Alignment; D013171:Spores, Bacterial / Q000502:physiology; D014157:Transcription Factors / Q000737:chemistry / Q000378:metabolism
D001426:Bacterial Proteins; D004268:DNA-Binding Proteins; D011134:Polysaccharides; C071977:SpoIIID protein, Bacillus; D014157:Transcription Factors; D010450:Endopeptidases; D000581:Amidohydrolases; C019665:amidase