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

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 micro...

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Published in:The ISME Journal 2021-02, Vol.15 (2), p.605-617
Main Authors: Wang, Meng, Nie, Yong, Wu, Xiao-Lei
Format: Article
Language:English
Subjects:
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Biological Transport
Cell Membrane - metabolism
Cell Wall - metabolism
Constraining
Extracellular vesicles
Gram-Positive Bacteria
Heme
Iron
Iron constituents
Membrane fusion
Membrane vesicles
Membranes
Microorganisms
Nutrient release
Nutrients
Phylogeny
Recycling
Species
Vesicles
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Wu, Xiao-Lei
description 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.
doi_str_mv 10.1038/s41396-020-00800-1
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subjects Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Biological Transport
Cell Membrane - metabolism
Cell Wall - metabolism
Constraining
Extracellular vesicles
Gram-Positive Bacteria
Heme
Iron
Iron constituents
Membrane fusion
Membrane vesicles
Membranes
Microorganisms
Nutrient release
Nutrients
Phylogeny
Recycling
Species
Vesicles
title Extracellular heme recycling and sharing across species by novel mycomembrane vesicles of a Gram-positive bacterium
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