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Article

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

by
Ronald Biemann
1,*,†,
Enrico Buß
2,†,
Dirk Benndorf
2,3,4,*,
Theresa Lehmann
2,
Kay Schallert
2,
Sebastian Püttker
2,
Udo Reichl
2,4,
Berend Isermann
1,5,
Jochen G. Schneider
6,7,
Gunter Saake
8 and
Robert Heyer
2,8,*
1
Institute of Laboratory Medicine, Clinical Chemistry and Molecular Diagnostics, Leipzig University, Paul-List-Str. 13/15, 04103 Leipzig, Germany
2
Bioprocess Engineering, Otto von Guericke University, Universitätsplatz 2, 39106 Magdeburg, Germany
3
Microbiology, Anhalt University of Applied Sciences, Bernburger Straße 55, 06354 Köthen, Germany
4
Bioprocess Engineering, Max Planck Institute for Dynamics of Complex Technical Systems, Sandtorstraße 1, 39106 Magdeburg, Germany
5
Institute of Clinical Chemistry and Pathobiochemistry, Otto von Guericke University, Leipziger Straße 44, 39120 Magdeburg, Germany
6
Luxembourg Centre for Systems Biomedicine (LCSB), University of Luxembourg, 6, Avenue du Swing, L-4367 Belvaux, Luxembourg
7
Department of Internal Medicine II, Saarland University Medical Center, Kirrberger Str., 66424 Homburg Saar, Germany
8
Database and Software Engineering Group, Otto von Guericke University, Universitätsplatz 2, 39106 Magdeburg, Germany
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally.
Biomolecules 2021, 11(5), 726; https://doi.org/10.3390/biom11050726
Submission received: 1 April 2021 / Revised: 30 April 2021 / Accepted: 7 May 2021 / Published: 12 May 2021
(This article belongs to the Special Issue Host-Microbiome Interactions in Health and Disease)
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Abstract

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.
Keywords: metaproteomics; fecal samples; obesity; metabolic syndrome; gut inflammation; microbiome; weight loss metaproteomics; fecal samples; obesity; metabolic syndrome; gut inflammation; microbiome; weight loss

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MDPI and ACS Style

Biemann, R.; Buß, E.; Benndorf, D.; Lehmann, T.; Schallert, K.; Püttker, S.; Reichl, U.; Isermann, B.; Schneider, J.G.; Saake, G.; et al. Fecal Metaproteomics Reveals Reduced Gut Inflammation and Changed Microbial Metabolism Following Lifestyle-Induced Weight Loss. Biomolecules 2021, 11, 726. https://doi.org/10.3390/biom11050726

AMA Style

Biemann R, Buß E, Benndorf D, Lehmann T, Schallert K, Püttker S, Reichl U, Isermann B, Schneider JG, Saake G, et al. Fecal Metaproteomics Reveals Reduced Gut Inflammation and Changed Microbial Metabolism Following Lifestyle-Induced Weight Loss. Biomolecules. 2021; 11(5):726. https://doi.org/10.3390/biom11050726

Chicago/Turabian Style

Biemann, Ronald, Enrico Buß, Dirk Benndorf, Theresa Lehmann, Kay Schallert, Sebastian Püttker, Udo Reichl, Berend Isermann, Jochen G. Schneider, Gunter Saake, and et al. 2021. "Fecal Metaproteomics Reveals Reduced Gut Inflammation and Changed Microbial Metabolism Following Lifestyle-Induced Weight Loss" Biomolecules 11, no. 5: 726. https://doi.org/10.3390/biom11050726

APA Style

Biemann, R., Buß, E., Benndorf, D., Lehmann, T., Schallert, K., Püttker, S., Reichl, U., Isermann, B., Schneider, J. G., Saake, G., & Heyer, R. (2021). Fecal Metaproteomics Reveals Reduced Gut Inflammation and Changed Microbial Metabolism Following Lifestyle-Induced Weight Loss. Biomolecules, 11(5), 726. https://doi.org/10.3390/biom11050726

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