Metaproteomic assessment of gut microbial and host functional perturbations in Helicobacter pylori-infected patients subjected to an antimicrobial protocol

ABSTRACTThe impact of therapeutic interventions on the human gut microbiota (GM) is a clinical issue of paramount interest given the strong interconnection between microbial dynamics and human health. Orally administered antibiotics are known to reduce GM biomass and modify GM taxonomic profile. How...

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Main Authors: Marcello Abbondio, Alessandro Tanca, Laura De Diego, Rosangela Sau, Stefano Bibbò, Giovanni Mario Pes, Maria Pina Dore, Sergio Uzzau
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:Gut Microbes
Subjects:
Online Access:https://www.tandfonline.com/doi/10.1080/19490976.2023.2291170
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author Marcello Abbondio
Alessandro Tanca
Laura De Diego
Rosangela Sau
Stefano Bibbò
Giovanni Mario Pes
Maria Pina Dore
Sergio Uzzau
author_facet Marcello Abbondio
Alessandro Tanca
Laura De Diego
Rosangela Sau
Stefano Bibbò
Giovanni Mario Pes
Maria Pina Dore
Sergio Uzzau
author_sort Marcello Abbondio
collection DOAJ
description ABSTRACTThe impact of therapeutic interventions on the human gut microbiota (GM) is a clinical issue of paramount interest given the strong interconnection between microbial dynamics and human health. Orally administered antibiotics are known to reduce GM biomass and modify GM taxonomic profile. However, the impact of antimicrobial therapies on GM functions and biochemical pathways has scarcely been studied. Here, we characterized the fecal metaproteome of 10 Helicobacter pylori-infected patients before (T0) and after 10 days (T1) of a successful quadruple therapy (bismuth, tetracycline, metronidazole, and rabeprazole) and 30 days after therapy cessation (T2), to investigate how GM and host functions change during the eradication and healing processes. At T1, the abundance ratio between microbial and host proteins was reversed compared with that at T0 and T2. Several pathobionts (including Klebsiella, Proteus, Enterococcus, Muribaculum, and Enterocloster) were increased at T1. Therapy reshaped the relative contributions of the functions required to produce acetate, propionate, and butyrate. Proteins related to the uptake and processing of complex glycans were increased. Microbial cross-feeding with sialic acid, fucose, and rhamnose was enhanced, whereas hydrogen sulfide production was reduced. Finally, microbial proteins involved in antibiotic resistance and inflammation were more abundant after therapy. Moreover, a reduction in host proteins with known roles in inflammation and H. pylori-mediated carcinogenesis was observed. In conclusion, our results support the use of metaproteomics to monitor drug-induced remodeling of GM and host functions, opening the way for investigating new antimicrobial therapies aimed at preserving gut environmental homeostasis.
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spelling doaj.art-d8ca4f2e9d7847f6a48a989d365b38db2024-02-08T12:02:08ZengTaylor & Francis GroupGut Microbes1949-09761949-09842023-12-0115210.1080/19490976.2023.2291170Metaproteomic assessment of gut microbial and host functional perturbations in Helicobacter pylori-infected patients subjected to an antimicrobial protocolMarcello Abbondio0Alessandro Tanca1Laura De Diego2Rosangela Sau3Stefano Bibbò4Giovanni Mario Pes5Maria Pina Dore6Sergio Uzzau7Department of Biomedical Sciences, University of Sassari, Sassari, ItalyDepartment of Biomedical Sciences, University of Sassari, Sassari, ItalyDepartment of Biomedical Sciences, University of Sassari, Sassari, ItalyDepartment of Biomedical Sciences, University of Sassari, Sassari, ItalyDepartment of Medicine, Surgery and Pharmacy, University of Sassari, Sassari, ItalyDepartment of Medicine, Surgery and Pharmacy, University of Sassari, Sassari, ItalyDepartment of Medicine, Surgery and Pharmacy, University of Sassari, Sassari, ItalyDepartment of Biomedical Sciences, University of Sassari, Sassari, ItalyABSTRACTThe impact of therapeutic interventions on the human gut microbiota (GM) is a clinical issue of paramount interest given the strong interconnection between microbial dynamics and human health. Orally administered antibiotics are known to reduce GM biomass and modify GM taxonomic profile. However, the impact of antimicrobial therapies on GM functions and biochemical pathways has scarcely been studied. Here, we characterized the fecal metaproteome of 10 Helicobacter pylori-infected patients before (T0) and after 10 days (T1) of a successful quadruple therapy (bismuth, tetracycline, metronidazole, and rabeprazole) and 30 days after therapy cessation (T2), to investigate how GM and host functions change during the eradication and healing processes. At T1, the abundance ratio between microbial and host proteins was reversed compared with that at T0 and T2. Several pathobionts (including Klebsiella, Proteus, Enterococcus, Muribaculum, and Enterocloster) were increased at T1. Therapy reshaped the relative contributions of the functions required to produce acetate, propionate, and butyrate. Proteins related to the uptake and processing of complex glycans were increased. Microbial cross-feeding with sialic acid, fucose, and rhamnose was enhanced, whereas hydrogen sulfide production was reduced. Finally, microbial proteins involved in antibiotic resistance and inflammation were more abundant after therapy. Moreover, a reduction in host proteins with known roles in inflammation and H. pylori-mediated carcinogenesis was observed. In conclusion, our results support the use of metaproteomics to monitor drug-induced remodeling of GM and host functions, opening the way for investigating new antimicrobial therapies aimed at preserving gut environmental homeostasis.https://www.tandfonline.com/doi/10.1080/19490976.2023.2291170Antibioticsfecal samplegut microbiotahuman metaproteomeinfectionmicrobial functions
spellingShingle Marcello Abbondio
Alessandro Tanca
Laura De Diego
Rosangela Sau
Stefano Bibbò
Giovanni Mario Pes
Maria Pina Dore
Sergio Uzzau
Metaproteomic assessment of gut microbial and host functional perturbations in Helicobacter pylori-infected patients subjected to an antimicrobial protocol
Gut Microbes
Antibiotics
fecal sample
gut microbiota
human metaproteome
infection
microbial functions
title Metaproteomic assessment of gut microbial and host functional perturbations in Helicobacter pylori-infected patients subjected to an antimicrobial protocol
title_full Metaproteomic assessment of gut microbial and host functional perturbations in Helicobacter pylori-infected patients subjected to an antimicrobial protocol
title_fullStr Metaproteomic assessment of gut microbial and host functional perturbations in Helicobacter pylori-infected patients subjected to an antimicrobial protocol
title_full_unstemmed Metaproteomic assessment of gut microbial and host functional perturbations in Helicobacter pylori-infected patients subjected to an antimicrobial protocol
title_short Metaproteomic assessment of gut microbial and host functional perturbations in Helicobacter pylori-infected patients subjected to an antimicrobial protocol
title_sort metaproteomic assessment of gut microbial and host functional perturbations in helicobacter pylori infected patients subjected to an antimicrobial protocol
topic Antibiotics
fecal sample
gut microbiota
human metaproteome
infection
microbial functions
url https://www.tandfonline.com/doi/10.1080/19490976.2023.2291170
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