Abstract
Membrane vesicles (MVs) are secreted from a wide range of microbial species and transfer their content to other cells. Although MVs play critical roles in bacterial communication, whether MVs selectively interact with bacterial cells in microbial communities is unclear. In this study, we investigated the specificity of the MV-cell interactions and evaluated the potential of MVs to target bacterial cells for delivery. MV association with bacterial cells was examined using a fluorescent membrane dye to label MVs. MVs derived from the enterobacterium Buttiauxella agrestis specifically interacted with cells of the parent strain but interacted less specifically with those of other genera tested in this study. Electron microscopic analyses showed that MVs were not only attached on B. agrestis cells but also fused to them. The interaction energy, which was characterized by hydrodynamic diameter and zeta potential based on the Derjaguin–Landau–Verwey–Overbeek (DLVO) theory, was significant low between MVs and cells in B. agrestis, compared to those between B. agrestis MVs and cells of other genera. Similar specific interaction was also occurred between B. agrestis MVs and cells of six other species belonging to Buttiauxella spp. B. agrestis harboring plasmid pBBR1MCS-1 secreted plasmid-containing MVs (p-MVs), and plasmid DNA in p-MVs was transferred to the same species. Moreover, antibiotic-associated MVs enabled effective killing of target species; the survival rate of B. agrestis was lower than those of Escherichia coli and Pseudomonas aeruginosa in the presence of gentamicin-associated MVs derived from B. agrestis. Altogether, we provide the evidence that MVs selectively interact with target bacterial cells and offer a new avenue for controlling specific bacterial species using bacterial MVs in microbial communities.
Highlights
Many bacteria and archaea produce small bilayered particles (20–200 nm) from their surfaces (Mashburn-Warren and Whiteley, 2006; Deatherage and Cookson, 2012)
We arbitrarily selected eleven bacterial strains, including C. glutamicum AJ2247, M. luteus JCM 1464, B. subtilis C1, F. johnsoniae JCM 8514, R. halotolerans JCM 17536, R. soli DS42, H. pseudoflava GA3, B. agrestis CUETM77-167, E. persicina HK204, P. aeruginosa PAO1, and P. alcaligenes JCM 20561, which are supposed to release membrane vesicles (MVs) in the culture at high levels compared to E. coli MG1655 (Supplementary Figure S1), for use in further analyses
The interaction of MVs derived from P. aeruginosa with bacterial cells has been studied well (Kadurugamuwa and Beveridge, 1996, 1997; Li et al, 1998; Tashiro et al, 2010) and showed different levels of association based on bacterial species in this study (Figure 1A)
Summary
Many bacteria and archaea produce small bilayered particles (20–200 nm) from their surfaces (Mashburn-Warren and Whiteley, 2006; Deatherage and Cookson, 2012). MVs have multifunctional roles, such as transferring nucleic acids or toxic compounds to other cells, promoting the formation and maintenance of biofilm, releasing unnecessary compounds from cells, providing resistance to antibiotics and phages and extending the membrane for extracellular electron transport (Tashiro et al, 2012; Biller et al, 2014; Pirbadian et al, 2014; Schwechheimer and Kuehn, 2015; Toyofuku et al, 2015; Roier et al, 2016). Substances such as virulence factors and genetic materials are highly concentrated in MVs and remain stable against environmental stresses. Elucidating the selectivity in MV interactions with bacterial cells is critical for an improved understanding of bacterial interactions in communities
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