The Role of Mre Factors and Cell Division in Peptidoglycan Growth in the Multicellular Cyanobacterium Anabaena

Peptidoglycan surrounds the bacterial cell, being essential for the determination of the bacterium-specific morphology and survival. Peptidoglycan growth has been thoroughly investigated in some model rod-shaped bacteria, and more recently some representatives with disparate morphologies became into focus, revealing that patterns of peptidoglycan growth are much more diverse than previously anticipated. Anabaena forms filaments of communicated cells exhibiting features of multicellular organisms, such as the production of morphogens and coupled circadian oscillations. Bacteria in general serve two main tasks: cell growth and division. Both processes include peptidoglycan extension to allow cell expansion and to form the poles of the daughter cells, respectively. The cyanobacterium Anabaena forms filaments of communicated cells in which the outer membrane and the peptidoglycan sacculus, which is engrossed in the intercellular regions between contiguous cells, are continuous along the filament. During the growth of Anabaena, peptidoglycan incorporation was weak at the cell periphery. During cell division, midcell peptidoglycan incorporation matched the localization of the divisome, and incorporation persisted in the intercellular septa, even after the division was completed. MreB, MreC, and MreD were located throughout the cell periphery and, in contrast to other bacteria, also to the divisome all along midcell peptidoglycan growth. In Anabaena mutants bearing inactivated mreB, mreC, or mreD genes, which showed conspicuous alterations in the filament morphology, consecutive septal bands of peptidoglycan growth were frequently not parallel to each other and were irregularly spaced along the filament, reproducing the disposition of the Z-ring. Both lateral and septal growth was impaired in strains down-expressing Z-ring components, and MreB and MreD appeared to directly interact with some divisome components. We propose that, in Anabaena, association with the divisome is a way for localization of MreB, MreC, and MreD at the cell poles, where they regulate lateral, midcell, and septal peptidoglycan growth with the latter being involved in localization and maintenance of the intercellular septal-junction protein structures that mediate cell-cell communication along the filament. IMPORTANCE Peptidoglycan surrounds the bacterial cell, being essential for the determination of the bacterium-specific morphology and survival. Peptidoglycan growth has been thoroughly investigated in some model rod-shaped bacteria, and more recently some representatives with disparate morphologies became into focus, revealing that patterns of peptidoglycan growth are much more diverse than previously anticipated. Anabaena forms filaments of communicated cells exhibiting features of multicellular organisms, such as the production of morphogens and coupled circadian oscillations. Here, we showed that Anabaena presented a distinct pattern of peptidoglycan growth characterized by continuous incorporation of material at the polar intercellular regions, contributing to assembling and maintaining the protein complexes that expand the septal peptidoglycan mediating intercellular molecular exchange in the filament.

Automated summary

Peptidoglycan growth in bacteria is essential for their morphology and survival. Recent studies have revealed that the patterns of peptidoglycan growth are more diverse than previously thought. Anabaena, a filamentous bacterium, exhibits features of multicellular organisms and has a unique pattern of continuous peptidoglycan incorporation at the intercellular regions. This pattern contributes to the assembly and maintenance of protein complexes involved in intercellular molecular exchange.