Extracellular heme recycling and sharing across species by novel mycomembrane vesicles of a Gram-positive bacterium

Abstract

Microbes spontaneously release membrane vesicles (MVs), which play roles in nutrient acquisition and microbial interactions. Iron is indispensable for microbes, but is a difficult nutrient to acquire. However, whether MVs are also responsible for efficient iron uptake and therefore involved in microbial interaction remains to be elucidated. Here, we used a Gram-positive strain, Dietzia sp. DQ12-45-1b, to analyze the function of its MVs in heme-iron recycling and sharing between species. We determined the structure and constituent of MVs and showed that DQ12-45-1b releases MVs originating from the mycomembrane. When comparing proteomes of MVs between iron-limiting and iron-rich conditions, we found that under iron-limiting conditions, heme-binding proteins are enriched. Next, we proved that MVs participate in extracellular heme capture and transport, especially in heme recycling from environmental hemoproteins. Finally, we found that the heme carried in MVs is utilized by multiple species, and we further verified that membrane fusion efficiency and species evolutionary distance determine heme delivery. Together, our findings strongly suggest that MVs act as a newly identified pathway for heme recycling, and represent a public good shared between phylogenetically closely related species.

T6SS secretes an LPS-binding effector to recruit OMVs for exploitative competition and horizontal gene transfer

“…In addition, membrane vesicles of Dietzia sp. DQ12-45-1b, a Gram-positive bacterium, participate in extracellular heme capture with heme-binding proteins, allowing the heme carried in MVs to be utilized by multiple related species [62]. Furthermore, iron deficit leads to increased OMV production in Haemophilus influenzae by downregulation of the Fur-regulated VacJ/Yrb ABC phospholipid transporter.…”

Mycolic acid-containing bacteria trigger distinct types of membrane vesicles through different routes

“…Previous studies ( Prados-Rosales et al., 2011 , 2014 ) show Mycobacterium MVs form inner membrane vesicles (IMVs), further questioning the mechanisms of how they can traverse the cell wall and the mycomembrane. In addition, despite the presence of the mycomembrane in the MCB cells, MVs derived from the mycomembrane are scarcely reported and their formation mechanisms are largely unknown ( Wang et al., 2020 ).…”

Biosynthesis of Tetrapyrrole Cofactors by Bacterial Community Inhabiting Porphyrine-Containing Shale Rock (Fore-Sudetic Monocline)

“…For example, living cells can discharge cobalamin into the soil or release it via cell lysis. Similarly in the case of heme, microorganisms secrete extracellular hemoproteins, e.g., extracellular peroxidases, which are then taken up by other microorganisms [47,48].…”