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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Taylor & Francis Group
2023-12-01
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Series: | Gut Microbes |
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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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institution | Directory Open Access Journal |
issn | 1949-0976 1949-0984 |
language | English |
last_indexed | 2024-03-08T04:41:20Z |
publishDate | 2023-12-01 |
publisher | Taylor & Francis Group |
record_format | Article |
series | Gut Microbes |
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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