Cargando…

Analysis of global human gut metagenomes shows that metabolic resilience potential for short-chain fatty acid production is strongly influenced by lifestyle

High taxonomic diversity in non-industrial human gut microbiomes is often interpreted as beneficial; however, it is unclear if taxonomic diversity engenders ecological resilience (i.e. community stability and metabolic continuity). We estimate resilience through genus and species-level richness, phy...

Descripción completa

Detalles Bibliográficos
Autores principales: Jacobson, David K., Honap, Tanvi P., Ozga, Andrew T., Meda, Nicolas, Kagoné, Thérèse S., Carabin, Hélène, Spicer, Paul, Tito, Raul Y., Obregon-Tito, Alexandra J., Reyes, Luis Marin, Troncoso-Corzo, Luzmila, Guija-Poma, Emilio, Sankaranarayanan, Krithivasan, Lewis, Cecil M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7813856/
https://www.ncbi.nlm.nih.gov/pubmed/33462272
http://dx.doi.org/10.1038/s41598-021-81257-w
_version_ 1783637944041472000
author Jacobson, David K.
Honap, Tanvi P.
Ozga, Andrew T.
Meda, Nicolas
Kagoné, Thérèse S.
Carabin, Hélène
Spicer, Paul
Tito, Raul Y.
Obregon-Tito, Alexandra J.
Reyes, Luis Marin
Troncoso-Corzo, Luzmila
Guija-Poma, Emilio
Sankaranarayanan, Krithivasan
Lewis, Cecil M.
author_facet Jacobson, David K.
Honap, Tanvi P.
Ozga, Andrew T.
Meda, Nicolas
Kagoné, Thérèse S.
Carabin, Hélène
Spicer, Paul
Tito, Raul Y.
Obregon-Tito, Alexandra J.
Reyes, Luis Marin
Troncoso-Corzo, Luzmila
Guija-Poma, Emilio
Sankaranarayanan, Krithivasan
Lewis, Cecil M.
author_sort Jacobson, David K.
collection PubMed
description High taxonomic diversity in non-industrial human gut microbiomes is often interpreted as beneficial; however, it is unclear if taxonomic diversity engenders ecological resilience (i.e. community stability and metabolic continuity). We estimate resilience through genus and species-level richness, phylogenetic diversity, and evenness in short-chain fatty acid (SCFA) production among a global gut metagenome panel of 12 populations (n = 451) representing industrial and non-industrial lifestyles, including novel metagenomic data from Burkina Faso (n = 90). We observe significantly higher genus-level resilience in non-industrial populations, while SCFA production in industrial populations is driven by a few phylogenetically closely related species (belonging to Bacteroides and Clostridium), meaning industrial microbiomes have low resilience potential. Additionally, database bias obfuscates resilience estimates, as we were 2–5 times more likely to identify SCFA-encoding species in industrial microbiomes compared to non-industrial. Overall, we find high phylogenetic diversity, richness, and evenness of bacteria encoding SCFAs in non-industrial gut microbiomes, signaling high potential for resilience in SCFA production, despite database biases that limit metagenomic analysis of non-industrial populations.
format Online
Article
Text
id pubmed-7813856
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-78138562021-01-21 Analysis of global human gut metagenomes shows that metabolic resilience potential for short-chain fatty acid production is strongly influenced by lifestyle Jacobson, David K. Honap, Tanvi P. Ozga, Andrew T. Meda, Nicolas Kagoné, Thérèse S. Carabin, Hélène Spicer, Paul Tito, Raul Y. Obregon-Tito, Alexandra J. Reyes, Luis Marin Troncoso-Corzo, Luzmila Guija-Poma, Emilio Sankaranarayanan, Krithivasan Lewis, Cecil M. Sci Rep Article High taxonomic diversity in non-industrial human gut microbiomes is often interpreted as beneficial; however, it is unclear if taxonomic diversity engenders ecological resilience (i.e. community stability and metabolic continuity). We estimate resilience through genus and species-level richness, phylogenetic diversity, and evenness in short-chain fatty acid (SCFA) production among a global gut metagenome panel of 12 populations (n = 451) representing industrial and non-industrial lifestyles, including novel metagenomic data from Burkina Faso (n = 90). We observe significantly higher genus-level resilience in non-industrial populations, while SCFA production in industrial populations is driven by a few phylogenetically closely related species (belonging to Bacteroides and Clostridium), meaning industrial microbiomes have low resilience potential. Additionally, database bias obfuscates resilience estimates, as we were 2–5 times more likely to identify SCFA-encoding species in industrial microbiomes compared to non-industrial. Overall, we find high phylogenetic diversity, richness, and evenness of bacteria encoding SCFAs in non-industrial gut microbiomes, signaling high potential for resilience in SCFA production, despite database biases that limit metagenomic analysis of non-industrial populations. Nature Publishing Group UK 2021-01-18 /pmc/articles/PMC7813856/ /pubmed/33462272 http://dx.doi.org/10.1038/s41598-021-81257-w Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Jacobson, David K.
Honap, Tanvi P.
Ozga, Andrew T.
Meda, Nicolas
Kagoné, Thérèse S.
Carabin, Hélène
Spicer, Paul
Tito, Raul Y.
Obregon-Tito, Alexandra J.
Reyes, Luis Marin
Troncoso-Corzo, Luzmila
Guija-Poma, Emilio
Sankaranarayanan, Krithivasan
Lewis, Cecil M.
Analysis of global human gut metagenomes shows that metabolic resilience potential for short-chain fatty acid production is strongly influenced by lifestyle
title Analysis of global human gut metagenomes shows that metabolic resilience potential for short-chain fatty acid production is strongly influenced by lifestyle
title_full Analysis of global human gut metagenomes shows that metabolic resilience potential for short-chain fatty acid production is strongly influenced by lifestyle
title_fullStr Analysis of global human gut metagenomes shows that metabolic resilience potential for short-chain fatty acid production is strongly influenced by lifestyle
title_full_unstemmed Analysis of global human gut metagenomes shows that metabolic resilience potential for short-chain fatty acid production is strongly influenced by lifestyle
title_short Analysis of global human gut metagenomes shows that metabolic resilience potential for short-chain fatty acid production is strongly influenced by lifestyle
title_sort analysis of global human gut metagenomes shows that metabolic resilience potential for short-chain fatty acid production is strongly influenced by lifestyle
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7813856/
https://www.ncbi.nlm.nih.gov/pubmed/33462272
http://dx.doi.org/10.1038/s41598-021-81257-w
work_keys_str_mv AT jacobsondavidk analysisofglobalhumangutmetagenomesshowsthatmetabolicresiliencepotentialforshortchainfattyacidproductionisstronglyinfluencedbylifestyle
AT honaptanvip analysisofglobalhumangutmetagenomesshowsthatmetabolicresiliencepotentialforshortchainfattyacidproductionisstronglyinfluencedbylifestyle
AT ozgaandrewt analysisofglobalhumangutmetagenomesshowsthatmetabolicresiliencepotentialforshortchainfattyacidproductionisstronglyinfluencedbylifestyle
AT medanicolas analysisofglobalhumangutmetagenomesshowsthatmetabolicresiliencepotentialforshortchainfattyacidproductionisstronglyinfluencedbylifestyle
AT kagonethereses analysisofglobalhumangutmetagenomesshowsthatmetabolicresiliencepotentialforshortchainfattyacidproductionisstronglyinfluencedbylifestyle
AT carabinhelene analysisofglobalhumangutmetagenomesshowsthatmetabolicresiliencepotentialforshortchainfattyacidproductionisstronglyinfluencedbylifestyle
AT spicerpaul analysisofglobalhumangutmetagenomesshowsthatmetabolicresiliencepotentialforshortchainfattyacidproductionisstronglyinfluencedbylifestyle
AT titorauly analysisofglobalhumangutmetagenomesshowsthatmetabolicresiliencepotentialforshortchainfattyacidproductionisstronglyinfluencedbylifestyle
AT obregontitoalexandraj analysisofglobalhumangutmetagenomesshowsthatmetabolicresiliencepotentialforshortchainfattyacidproductionisstronglyinfluencedbylifestyle
AT reyesluismarin analysisofglobalhumangutmetagenomesshowsthatmetabolicresiliencepotentialforshortchainfattyacidproductionisstronglyinfluencedbylifestyle
AT troncosocorzoluzmila analysisofglobalhumangutmetagenomesshowsthatmetabolicresiliencepotentialforshortchainfattyacidproductionisstronglyinfluencedbylifestyle
AT guijapomaemilio analysisofglobalhumangutmetagenomesshowsthatmetabolicresiliencepotentialforshortchainfattyacidproductionisstronglyinfluencedbylifestyle
AT sankaranarayanankrithivasan analysisofglobalhumangutmetagenomesshowsthatmetabolicresiliencepotentialforshortchainfattyacidproductionisstronglyinfluencedbylifestyle
AT lewiscecilm analysisofglobalhumangutmetagenomesshowsthatmetabolicresiliencepotentialforshortchainfattyacidproductionisstronglyinfluencedbylifestyle