Donor-delivered cell wall hydrolases facilitate nanotube penetration into recipient bacteria

Amit K Baidya,Ilan Rosenshine,Sigal Ben-Yehuda

doi:10.1038/s41467-020-15605-1

Amit K Baidya, Ilan Rosenshine + Show 1 more

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https://doi.org/10.1038/s41467-020-15605-1

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Journal: Nature Communications	Publication Date: Apr 22, 2020
Citations: 19	License type: open-access

Affiliation: Hebrew University of Jerusalem

Abstract

Bacteria can produce membranous nanotubes that mediate contact-dependent exchange of molecules among bacterial cells. However, it is unclear how nanotubes cross the cell wall to emerge from the donor or to penetrate into the recipient cell. Here, we report that Bacillus subtilis utilizes cell wall remodeling enzymes, the LytC amidase and its enhancer LytB, for efficient nanotube extrusion and penetration. Nanotube production is reduced in a lytBC mutant, and the few nanotubes formed appear deficient in penetrating into target cells. Donor-derived LytB molecules localize along nanotubes and on the surface of nanotube-connected neighbouring cells, primarily at sites of nanotube penetration. Furthermore, LytB from donor B. subtilis can activate LytC of recipient bacteria from diverse species, facilitating cell wall hydrolysis to establish nanotube connection. Our data provide a mechanistic view of how intercellular connecting devices can be formed among neighbouring bacteria.

Highlights

Bacteria can produce membranous nanotubes that mediate contact-dependent exchange of molecules among bacterial cells
As LytB and LytC hydrolases were found to be associated with the nanotube biochemical fraction[5], we reasoned that they might facilitate the passage of nanotubes through the thick cell wall (CW) material, enabling their reach to the cell exterior
The few nanotubes that eventually extruded from the ΔlytBC mutant cells, appeared as they failed to penetrate into the nearby recipient bacterium, exhibiting unusual “continual” nanotubes, extending over the surface of their neighboring cell (Fig. 1b, d; Supplementary Fig. 1C)

Summary

Introduction

Bacteria can produce membranous nanotubes that mediate contact-dependent exchange of molecules among bacterial cells. It is unclear how nanotubes cross the cell wall to emerge from the donor or to penetrate into the recipient cell. Nanotubes were found to serve as conduits for intercellular exchange of metabolites, cytoplasmic proteins and even plasmids, hinting at their potential significance in shaping natural bacterial communities[3,4,5,6] Utilizing these intercellular bridges, Bs could deliver the WapA tRNase toxin to, and acquire nutrients from, the opponent species B. megaterium (Bm)[6]. These hydrolases participate in key cellular processes including cell division and assembly of complex structures, such as secretion systems, flagella, and pili[21,23,24]

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