Fecal Metaproteomics Reveals Reduced Gut Inflammation and Changed Microbial Metabolism Following Lifestyle-Induced Weight Loss

Gut microbiota-mediated inflammation promotes obesity-associated low-grade inflammation, which represents a hallmark of metabolic syndrome. To investigate if lifestyle-induced weight loss (WL) may modulate the gut microbiome composition and its interaction with the host on a functional level, we ana...

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Main Authors: Ronald Biemann, Enrico Buß, Dirk Benndorf, Theresa Lehmann, Kay Schallert, Sebastian Püttker, Udo Reichl, Berend Isermann, Jochen G. Schneider, Gunter Saake, Robert Heyer
Format: Article
Language:English
Published: MDPI AG 2021-05-01
Series:Biomolecules
Subjects:
Online Access:https://www.mdpi.com/2218-273X/11/5/726
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author Ronald Biemann
Enrico Buß
Dirk Benndorf
Theresa Lehmann
Kay Schallert
Sebastian Püttker
Udo Reichl
Berend Isermann
Jochen G. Schneider
Gunter Saake
Robert Heyer
author_facet Ronald Biemann
Enrico Buß
Dirk Benndorf
Theresa Lehmann
Kay Schallert
Sebastian Püttker
Udo Reichl
Berend Isermann
Jochen G. Schneider
Gunter Saake
Robert Heyer
author_sort Ronald Biemann
collection DOAJ
description Gut microbiota-mediated inflammation promotes obesity-associated low-grade inflammation, which represents a hallmark of metabolic syndrome. To investigate if lifestyle-induced weight loss (WL) may modulate the gut microbiome composition and its interaction with the host on a functional level, we analyzed the fecal metaproteome of 33 individuals with metabolic syndrome in a longitudinal study before and after lifestyle-induced WL in a well-defined cohort. The 6-month WL intervention resulted in reduced BMI (−13.7%), improved insulin sensitivity (HOMA-IR, −46.1%), and reduced levels of circulating hsCRP (−39.9%), indicating metabolic syndrome reversal. The metaprotein spectra revealed a decrease of human proteins associated with gut inflammation. Taxonomic analysis revealed only minor changes in the bacterial composition with an increase of the families Desulfovibrionaceae, Leptospiraceae, Syntrophomonadaceae, Thermotogaceae and Verrucomicrobiaceae. Yet we detected an increased abundance of microbial metaprotein spectra that suggest an enhanced hydrolysis of complex carbohydrates. Hence, lifestyle-induced WL was associated with reduced gut inflammation and functional changes of human and microbial enzymes for carbohydrate hydrolysis while the taxonomic composition of the gut microbiome remained almost stable. The metaproteomics workflow has proven to be a suitable method for monitoring inflammatory changes in the fecal metaproteome.
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spelling doaj.art-dade76ade6da4dffa4198cb0f9ccc5a42023-11-21T19:21:32ZengMDPI AGBiomolecules2218-273X2021-05-0111572610.3390/biom11050726Fecal Metaproteomics Reveals Reduced Gut Inflammation and Changed Microbial Metabolism Following Lifestyle-Induced Weight LossRonald Biemann0Enrico Buß1Dirk Benndorf2Theresa Lehmann3Kay Schallert4Sebastian Püttker5Udo Reichl6Berend Isermann7Jochen G. Schneider8Gunter Saake9Robert Heyer10Institute of Laboratory Medicine, Clinical Chemistry and Molecular Diagnostics, Leipzig University, Paul-List-Str. 13/15, 04103 Leipzig, GermanyBioprocess Engineering, Otto von Guericke University, Universitätsplatz 2, 39106 Magdeburg, GermanyBioprocess Engineering, Otto von Guericke University, Universitätsplatz 2, 39106 Magdeburg, GermanyBioprocess Engineering, Otto von Guericke University, Universitätsplatz 2, 39106 Magdeburg, GermanyBioprocess Engineering, Otto von Guericke University, Universitätsplatz 2, 39106 Magdeburg, GermanyBioprocess Engineering, Otto von Guericke University, Universitätsplatz 2, 39106 Magdeburg, GermanyBioprocess Engineering, Otto von Guericke University, Universitätsplatz 2, 39106 Magdeburg, GermanyInstitute of Laboratory Medicine, Clinical Chemistry and Molecular Diagnostics, Leipzig University, Paul-List-Str. 13/15, 04103 Leipzig, GermanyLuxembourg Centre for Systems Biomedicine (LCSB), University of Luxembourg, 6, Avenue du Swing, L-4367 Belvaux, LuxembourgDatabase and Software Engineering Group, Otto von Guericke University, Universitätsplatz 2, 39106 Magdeburg, GermanyBioprocess Engineering, Otto von Guericke University, Universitätsplatz 2, 39106 Magdeburg, GermanyGut microbiota-mediated inflammation promotes obesity-associated low-grade inflammation, which represents a hallmark of metabolic syndrome. To investigate if lifestyle-induced weight loss (WL) may modulate the gut microbiome composition and its interaction with the host on a functional level, we analyzed the fecal metaproteome of 33 individuals with metabolic syndrome in a longitudinal study before and after lifestyle-induced WL in a well-defined cohort. The 6-month WL intervention resulted in reduced BMI (−13.7%), improved insulin sensitivity (HOMA-IR, −46.1%), and reduced levels of circulating hsCRP (−39.9%), indicating metabolic syndrome reversal. The metaprotein spectra revealed a decrease of human proteins associated with gut inflammation. Taxonomic analysis revealed only minor changes in the bacterial composition with an increase of the families Desulfovibrionaceae, Leptospiraceae, Syntrophomonadaceae, Thermotogaceae and Verrucomicrobiaceae. Yet we detected an increased abundance of microbial metaprotein spectra that suggest an enhanced hydrolysis of complex carbohydrates. Hence, lifestyle-induced WL was associated with reduced gut inflammation and functional changes of human and microbial enzymes for carbohydrate hydrolysis while the taxonomic composition of the gut microbiome remained almost stable. The metaproteomics workflow has proven to be a suitable method for monitoring inflammatory changes in the fecal metaproteome.https://www.mdpi.com/2218-273X/11/5/726metaproteomicsfecal samplesobesitymetabolic syndromegut inflammationmicrobiome
spellingShingle Ronald Biemann
Enrico Buß
Dirk Benndorf
Theresa Lehmann
Kay Schallert
Sebastian Püttker
Udo Reichl
Berend Isermann
Jochen G. Schneider
Gunter Saake
Robert Heyer
Fecal Metaproteomics Reveals Reduced Gut Inflammation and Changed Microbial Metabolism Following Lifestyle-Induced Weight Loss
Biomolecules
metaproteomics
fecal samples
obesity
metabolic syndrome
gut inflammation
microbiome
title Fecal Metaproteomics Reveals Reduced Gut Inflammation and Changed Microbial Metabolism Following Lifestyle-Induced Weight Loss
title_full Fecal Metaproteomics Reveals Reduced Gut Inflammation and Changed Microbial Metabolism Following Lifestyle-Induced Weight Loss
title_fullStr Fecal Metaproteomics Reveals Reduced Gut Inflammation and Changed Microbial Metabolism Following Lifestyle-Induced Weight Loss
title_full_unstemmed Fecal Metaproteomics Reveals Reduced Gut Inflammation and Changed Microbial Metabolism Following Lifestyle-Induced Weight Loss
title_short Fecal Metaproteomics Reveals Reduced Gut Inflammation and Changed Microbial Metabolism Following Lifestyle-Induced Weight Loss
title_sort fecal metaproteomics reveals reduced gut inflammation and changed microbial metabolism following lifestyle induced weight loss
topic metaproteomics
fecal samples
obesity
metabolic syndrome
gut inflammation
microbiome
url https://www.mdpi.com/2218-273X/11/5/726
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