Gram‐positive bacteria produce membrane vesicles: Proteomics‐based characterization of Staphylococcus aureus‐derived membrane vesicles

Abstract

Although archaea, Gram-negative bacteria, and mammalian cells constitutively secrete membrane vesicles (MVs) as a mechanism for cell-free intercellular communication, this cellular process has been overlooked in Gram-positive bacteria. Here, we found for the first time that Gram-positive bacteria naturally produce MVs into the extracellular milieu. Further characterizations showed that the density and size of Staphylococcus aureus-derived MVs are both similar to those of Gram-negative bacteria. With a proteomics approach, we identified with high confidence a total of 90 protein components of S. aureus-derived MVs. In the group of identified proteins, the highly enriched extracellular proteins suggested that a specific sorting mechanism for vesicular proteins exists. We also identified proteins that facilitate the transfer of proteins to other bacteria, as well to eliminate competing organisms, antibiotic resistance, pathological functions in systemic infections, and MV biogenesis. Taken together, these observations suggest that the secretion of MVs is an evolutionally conserved, universal process that occurs from simple organisms to complex multicellular organisms. This information will help us not only to elucidate the biogenesis and functions of MVs, but also to develop therapeutic tools for vaccines, diagnosis, and antibiotics effective against pathogenic strains of Gram-positive bacteria.

Origin of life: LUCA and extracellular membrane vesicles (EMVs)

“…It has been suggested that the vesicles produced by monoderm bacteria are like their diderm counterparts, involved in pathogenesis (Rivera et al 2010;Prados-Rosales et al 2011). Enzymes involved in peptidoglycan degradation, antibiotic degradation, virulence factors (anthrolysin, anthrax toxin components, coagulases, hemolysins and lipases) and immunologically-active compounds have been identified in these vesicles (Marsollier et al 2007;Lee et al 2009;Rivera et al 2010;Gurung et al 2011;Prados-Rosales et al 2011;Thay et al 2013;Brown et al 2014).…”

“…EMVs produced by these bacteria are derived from the cytoplasmic membrane and are 20-250 nm in diameter (Lee et al 2009;Schrempf et al 2011). It has been suggested that the vesicles produced by monoderm bacteria are like their diderm counterparts, involved in pathogenesis (Rivera et al 2010;Prados-Rosales et al 2011).…”

“…Planctomycetes form a distinct phylum of the domain bacteria and possess unusual features such as intracellular compartmentalization and proteinaceous cell walls (Lee et al 2009). Cells of the genus Gemmata also contain a membranebound nucleoid resembling the eukaryotic nucleus.…”

Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins

“…More recently, the release of membrane-derived vesicles by Grampositive Staphylococcus aureus, Mycobacterium ulcerans, and Bacillus spp. was reported (18)(19)(20)(21), suggesting that vesicle production is a widespread phenomenon among microbial species.…”

Pseudomonas Quinolone Signal Affects Membrane Vesicle Production in not only Gram-Negative but also Gram-Positive Bacteria

“…Until now, it had been thought that MV production occurred in only Gram-negative bacteria. However, a recent study reported that the Gram-positive bacterium Staphylococcus aureus naturally secretes MVs (20). Since the role and mechanism of MV production in Gram-positive bacteria remain unknown, further detailed analysis can be expected.…”