A new morphogenesis pathway in bacteria: unbalanced activity of cell wall synthesis machineries leads to coccus-to-rod transition and filamentation in ovococci

Abstract

SummaryBacteria display a variety of shapes, which have biological relevance. In most eubacteria, cell shape is maintained by the tough peptidoglycan (PG) layer of the cell wall, the sacculus. The organization of PG synthesis machineries, orchestrated by different cytoskeletal elements, determines the specific shapes of sacculi. In rod-shaped bacteria, the actin-like (MreB) and the tubuline-like (FtsZ) cytoskeletons control synthesis of the sidewall (elongation) and the crosswall (septation) respectively. Much less is known concerning cell morphogenesis in cocci, which lack MreB proteins. While spherical cocci exclusively display septal growth, ovococci additionally display peripheral growth, which is responsible of the slight longitudinal expansion that generates their ovoid shape. Here, we report that the ovococcus Lactococcus lactis has the ability to become rod-shaped. L. lactis IL1403 wild-type cells form long aseptate filaments during both biofilm and planktonic growth in a synthetic medium. Nascent PG insertion and the division protein FtsK localize in multiple peripheral rings regularly spaced along the filaments. We show that filamentation results from septation inhibition, and that penicillin-binding proteins PBP2x and PBP2b play a direct role in this process. We propose a model for filament formation in L. lactis, and discuss the possible biological role of such morphological differentiation.

The Requirement for Pneumococcal MreC and MreD Is Relieved by Inactivation of the Gene Encoding PBP1a

“…1). Our current working model is that the pneumococcal peripheral PG synthesis complex contains MreC, MreD, and PBP1a, along with several other proteins suggested by previous work in pneumococcus and other bacteria, including class B PBP2b Spn , RodA Spn , shuttle protein GpsB Spn , and another pneumococcal class A enzyme (see Introduction) (9,46,72). According to this model, the depletion of MreC, MreD, or both would decrease peripheral PG synthesis and lead to spherical cell formation ( Fig.…”

“…4; also see Fig. S3 and S4 in the supplemental material) (31,46). The marked reduction in width of ⌬pbp1a mutant cells (Fig.…”

“…4; also see Fig. S3 and S4 in the supplemental material), which binds to PG pentapeptides in regions of active PG biosynthesis (1,2,42,46,47).…”

“…Based on the composition of the complexes in rod-shaped cells, it has been hypothesized that specific sets of homologous cell division proteins mediate peripheral (MreC, MreD, RodA, and PBP2b) and septal (FtsZ, EzrA, PBP2x, FtsW, and DivIB/FtsL/DivIC) PG synthesis in ovococcus bacteria (72). A recent study correlating the effects of mutations or antibiotic treatments to changes in cell shapes supports the idea that the PBP2x and PBP2b class B transpeptidases are associated with septal and peripheral PG synthesis, respectively, in L. lactis (46) and provides some of the first direct evidence for a two-state model in ovococci. However, most other aspects of this model are largely untested, and it remains to be determined whether the two ovococcus PG synthesis machineries exist as two distinct complexes ( Fig.…”

Control of cell division in Streptococcus pneumoniae by the conserved Ser/Thr protein kinase StkP

“…Interestingly, S. pneumoniae MreC/D recently were shown to direct peripheral PG synthesis (59). Also, Lactococcus lactis, a phylogenetically close relative of S. pneumoniae, has been shown recently to undergo a coccus-to-rod transition as a result of unbalanced activity of the cell-synthesis machineries (60).…”