Cargando…

A Salvaging Strategy Enables Stable Metabolite Provisioning among Free-Living Bacteria

All organisms rely on complex metabolites such as amino acids, nucleotides, and cofactors for essential metabolic processes. Some microbes synthesize these fundamental ingredients of life de novo, while others rely on uptake to fulfill their metabolic needs. Although certain metabolic processes are...

Descripción completa

Detalles Bibliográficos
Autores principales: Gude, Sebastian, Pherribo, Gordon J., Taga, Michiko E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9426567/
https://www.ncbi.nlm.nih.gov/pubmed/35924847
http://dx.doi.org/10.1128/msystems.00288-22
_version_ 1784778710826614784
author Gude, Sebastian
Pherribo, Gordon J.
Taga, Michiko E.
author_facet Gude, Sebastian
Pherribo, Gordon J.
Taga, Michiko E.
author_sort Gude, Sebastian
collection PubMed
description All organisms rely on complex metabolites such as amino acids, nucleotides, and cofactors for essential metabolic processes. Some microbes synthesize these fundamental ingredients of life de novo, while others rely on uptake to fulfill their metabolic needs. Although certain metabolic processes are inherently “leaky,” the mechanisms enabling stable metabolite provisioning among microbes in the absence of a host remain largely unclear. In particular, how can metabolite provisioning among free-living bacteria be maintained under the evolutionary pressure to economize resources? Salvaging, the process of “recycling and reusing,” can be a metabolically efficient route to obtain access to required resources. Here, we show experimentally how precursor salvaging in engineered Escherichia coli populations can lead to stable, long-term metabolite provisioning. We find that salvaged cobamides (vitamin B(12) and related enzyme cofactors) are readily made available to nonproducing population members, yet salvagers are strongly protected from overexploitation. We also describe a previously unnoted benefit of precursor salvaging, namely, the removal of the nonfunctional, proliferation-inhibiting precursor. As long as compatible precursors are present, any microbe possessing the terminal steps of a biosynthetic process can, in principle, forgo de novo biosynthesis in favor of salvaging. Consequently, precursor salvaging likely represents a potent, yet overlooked, alternative to de novo biosynthesis for the acquisition and provisioning of metabolites in free-living bacterial populations. IMPORTANCE Recycling gives new life to old things. Bacteria have the ability to recycle and reuse complex molecules they encounter in their environment to fulfill their basic metabolic needs in a resource-efficient way. By studying the salvaging (recycling and reusing) of vitamin B(12) precursors, we found that metabolite salvaging can benefit others and provide stability to a bacterial community at the same time. Salvagers of vitamin B(12) precursors freely share the result of their labor yet cannot be outcompeted by freeloaders, likely because salvagers retain preferential access to the salvaging products. Thus, salvaging may represent an effective, yet overlooked, mechanism of acquiring and provisioning nutrients in microbial populations.
format Online
Article
Text
id pubmed-9426567
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher American Society for Microbiology
record_format MEDLINE/PubMed
spelling pubmed-94265672022-08-31 A Salvaging Strategy Enables Stable Metabolite Provisioning among Free-Living Bacteria Gude, Sebastian Pherribo, Gordon J. Taga, Michiko E. mSystems Research Article All organisms rely on complex metabolites such as amino acids, nucleotides, and cofactors for essential metabolic processes. Some microbes synthesize these fundamental ingredients of life de novo, while others rely on uptake to fulfill their metabolic needs. Although certain metabolic processes are inherently “leaky,” the mechanisms enabling stable metabolite provisioning among microbes in the absence of a host remain largely unclear. In particular, how can metabolite provisioning among free-living bacteria be maintained under the evolutionary pressure to economize resources? Salvaging, the process of “recycling and reusing,” can be a metabolically efficient route to obtain access to required resources. Here, we show experimentally how precursor salvaging in engineered Escherichia coli populations can lead to stable, long-term metabolite provisioning. We find that salvaged cobamides (vitamin B(12) and related enzyme cofactors) are readily made available to nonproducing population members, yet salvagers are strongly protected from overexploitation. We also describe a previously unnoted benefit of precursor salvaging, namely, the removal of the nonfunctional, proliferation-inhibiting precursor. As long as compatible precursors are present, any microbe possessing the terminal steps of a biosynthetic process can, in principle, forgo de novo biosynthesis in favor of salvaging. Consequently, precursor salvaging likely represents a potent, yet overlooked, alternative to de novo biosynthesis for the acquisition and provisioning of metabolites in free-living bacterial populations. IMPORTANCE Recycling gives new life to old things. Bacteria have the ability to recycle and reuse complex molecules they encounter in their environment to fulfill their basic metabolic needs in a resource-efficient way. By studying the salvaging (recycling and reusing) of vitamin B(12) precursors, we found that metabolite salvaging can benefit others and provide stability to a bacterial community at the same time. Salvagers of vitamin B(12) precursors freely share the result of their labor yet cannot be outcompeted by freeloaders, likely because salvagers retain preferential access to the salvaging products. Thus, salvaging may represent an effective, yet overlooked, mechanism of acquiring and provisioning nutrients in microbial populations. American Society for Microbiology 2022-08-04 /pmc/articles/PMC9426567/ /pubmed/35924847 http://dx.doi.org/10.1128/msystems.00288-22 Text en Copyright © 2022 Gude et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Gude, Sebastian
Pherribo, Gordon J.
Taga, Michiko E.
A Salvaging Strategy Enables Stable Metabolite Provisioning among Free-Living Bacteria
title A Salvaging Strategy Enables Stable Metabolite Provisioning among Free-Living Bacteria
title_full A Salvaging Strategy Enables Stable Metabolite Provisioning among Free-Living Bacteria
title_fullStr A Salvaging Strategy Enables Stable Metabolite Provisioning among Free-Living Bacteria
title_full_unstemmed A Salvaging Strategy Enables Stable Metabolite Provisioning among Free-Living Bacteria
title_short A Salvaging Strategy Enables Stable Metabolite Provisioning among Free-Living Bacteria
title_sort salvaging strategy enables stable metabolite provisioning among free-living bacteria
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9426567/
https://www.ncbi.nlm.nih.gov/pubmed/35924847
http://dx.doi.org/10.1128/msystems.00288-22
work_keys_str_mv AT gudesebastian asalvagingstrategyenablesstablemetaboliteprovisioningamongfreelivingbacteria
AT pherribogordonj asalvagingstrategyenablesstablemetaboliteprovisioningamongfreelivingbacteria
AT tagamichikoe asalvagingstrategyenablesstablemetaboliteprovisioningamongfreelivingbacteria
AT gudesebastian salvagingstrategyenablesstablemetaboliteprovisioningamongfreelivingbacteria
AT pherribogordonj salvagingstrategyenablesstablemetaboliteprovisioningamongfreelivingbacteria
AT tagamichikoe salvagingstrategyenablesstablemetaboliteprovisioningamongfreelivingbacteria