Outside-in: intracellular vesicles in giant sulfur bacteria contain peptidoglycan

Abstract

AbstractUntil recently, the cellular envelopes of bacteria were regarded as static and rigid relative to those of eukaryotes. While investigating peptidoglycan synthesis in populations of giant sulfur bacteria, Candidatus Thiomargarita spp., we observed internal vesicle-like features (VLFs). VLFs, as imaged following the active incorporation of D-amino acids, appear to begin as invaginations and delaminations of the cellular envelope. Staining with wheat germ agglutinin confirmed the presence of peptidoglycan in VLFs, while polymyxin B revealed that the outer membrane is present in some VLFs. Transmission electron microscopy revealed a complex network of interconnected VLFs. Genomes of Ca. Thiomargarita nelsonii lack a canonical divisome, while possessing homologs to genes such as actin, membrane scaffolding proteins, and dynamins that are associated with phagocytosis in eukaryotes. The physiological role of VLFs remains unclear, but the presence of sulfur globules in some suggests compartmentalization of metabolism and energy production. This is the first report of peptidoglycan and outer membrane bound intracellular vesicles within prokaryotic cells. These findings transform the canonical view of the inflexible bacterial cell envelope and further narrow the divide between prokaryotes and eukaryotes.