Peptidoglycan Remodeling and Conversion of an Inner Membrane into an Outer Membrane during Sporulation

SummaryTwo hallmarks of the Firmicute phylum, which includes the Bacilli and Clostridia classes, are their ability to form endospores and their “Gram-positive” single-membraned, thick-cell-wall envelope structure. Acetonema longum is part of a lesser-known family (the Veillonellaceae) of Clostridia that form endospores but that are surprisingly “Gram negative,” possessing both an inner and outer membrane and a thin cell wall. Here, we present macromolecular resolution, 3D electron cryotomographic images of vegetative, sporulating, and germinating A. longum cells showing that during the sporulation process, the inner membrane of the mother cell is inverted and transformed to become the outer membrane of the germinating cell. Peptidoglycan persists throughout, leading to a revised, “continuous” model of its role in the process. Coupled with genomic analyses, these results point to sporulation as a mechanism by which the bacterial outer membrane may have arisen and A. longum as a potential “missing link” between single- and double-membraned bacteria.

Graphical AbstractFigure optionsDownload full-size imageDownload high-quality image (491 K)Download as PowerPoint slideHighlights► A. longum is a Gram-negative (double-membraned) bacterium able to sporulate ► Two membranes derived from the inner membrane of the mother cell surround the spore ► During outgrowth A. longum converts an inner to an outer membrane ► Sporulation may provide insights into the biogenesis of a second membrane in bacteria