Characterization and Spatial Mapping of the Human Gut Metasecretome

ABSTRACT Bacterially secreted proteins play an important role in microbial physiology and ecology in many environments, including the mammalian gut. While gut microbes have been extensively studied over the past decades, little is known about the proteins that they secrete into the gastrointestinal...

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Main Authors: Florencia Velez-Cortes, Harris Wang
Format: Article
Language:English
Published: American Society for Microbiology 2022-12-01
Series:mSystems
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/msystems.00717-22
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author Florencia Velez-Cortes
Harris Wang
author_facet Florencia Velez-Cortes
Harris Wang
author_sort Florencia Velez-Cortes
collection DOAJ
description ABSTRACT Bacterially secreted proteins play an important role in microbial physiology and ecology in many environments, including the mammalian gut. While gut microbes have been extensively studied over the past decades, little is known about the proteins that they secrete into the gastrointestinal tract. In this study, we developed and applied a computational pipeline to a comprehensive catalog of human-associated metagenome-assembled genomes in order to predict and analyze the bacterial metasecretome of the human gut, i.e., the collection of proteins secreted out of the cytoplasm by human gut bacteria. We identified the presence of large and diverse families of secreted carbohydrate-active enzymes and assessed their phylogenetic distributions across different taxonomic groups, which revealed an enrichment in Bacteroidetes and Verrucomicrobia. By mapping secreted proteins to available metagenomic data from endoscopic sampling of the human gastrointestinal tract, we specifically pinpointed regions in the upper and lower intestinal tract along the lumen and mucosa where specific glycosidases are secreted by resident microbes. The metasecretome analyzed in this study constitutes the most comprehensive list of secreted proteins produced by human gut bacteria reported to date and serves as a useful resource for the microbiome research community. IMPORTANCE Bacterially secreted proteins are necessary for the proper functioning of bacterial cells and communities. Secreted proteins provide bacterial cells with the ability to harvest resources from the exterior, import these resources into the cell, and signal to other bacteria. In the human gut microbiome, these actions impact host health and allow the maintenance of a healthy gut bacterial community. We utilized computational tools to identify the major components of human gut bacterially secreted proteins and determined their spatial distribution in the gastrointestinal tract. Our analysis of human gut bacterial secreted proteins will allow a better understanding of the impact of gut bacteria on human health and represents a step toward identifying new protein functions with interesting applications in biomedicine and industry.
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spelling doaj.art-40db41fec465486b99ccd9e8fb28a0042022-12-22T04:23:55ZengAmerican Society for MicrobiologymSystems2379-50772022-12-017610.1128/msystems.00717-22Characterization and Spatial Mapping of the Human Gut MetasecretomeFlorencia Velez-Cortes0Harris Wang1Department of Systems Biology, Columbia University, New York, New York, USADepartment of Systems Biology, Columbia University, New York, New York, USAABSTRACT Bacterially secreted proteins play an important role in microbial physiology and ecology in many environments, including the mammalian gut. While gut microbes have been extensively studied over the past decades, little is known about the proteins that they secrete into the gastrointestinal tract. In this study, we developed and applied a computational pipeline to a comprehensive catalog of human-associated metagenome-assembled genomes in order to predict and analyze the bacterial metasecretome of the human gut, i.e., the collection of proteins secreted out of the cytoplasm by human gut bacteria. We identified the presence of large and diverse families of secreted carbohydrate-active enzymes and assessed their phylogenetic distributions across different taxonomic groups, which revealed an enrichment in Bacteroidetes and Verrucomicrobia. By mapping secreted proteins to available metagenomic data from endoscopic sampling of the human gastrointestinal tract, we specifically pinpointed regions in the upper and lower intestinal tract along the lumen and mucosa where specific glycosidases are secreted by resident microbes. The metasecretome analyzed in this study constitutes the most comprehensive list of secreted proteins produced by human gut bacteria reported to date and serves as a useful resource for the microbiome research community. IMPORTANCE Bacterially secreted proteins are necessary for the proper functioning of bacterial cells and communities. Secreted proteins provide bacterial cells with the ability to harvest resources from the exterior, import these resources into the cell, and signal to other bacteria. In the human gut microbiome, these actions impact host health and allow the maintenance of a healthy gut bacterial community. We utilized computational tools to identify the major components of human gut bacterially secreted proteins and determined their spatial distribution in the gastrointestinal tract. Our analysis of human gut bacterial secreted proteins will allow a better understanding of the impact of gut bacteria on human health and represents a step toward identifying new protein functions with interesting applications in biomedicine and industry.https://journals.asm.org/doi/10.1128/msystems.00717-22gut microbiomehuman microbiomemetagenomics
spellingShingle Florencia Velez-Cortes
Harris Wang
Characterization and Spatial Mapping of the Human Gut Metasecretome
mSystems
gut microbiome
human microbiome
metagenomics
title Characterization and Spatial Mapping of the Human Gut Metasecretome
title_full Characterization and Spatial Mapping of the Human Gut Metasecretome
title_fullStr Characterization and Spatial Mapping of the Human Gut Metasecretome
title_full_unstemmed Characterization and Spatial Mapping of the Human Gut Metasecretome
title_short Characterization and Spatial Mapping of the Human Gut Metasecretome
title_sort characterization and spatial mapping of the human gut metasecretome
topic gut microbiome
human microbiome
metagenomics
url https://journals.asm.org/doi/10.1128/msystems.00717-22
work_keys_str_mv AT florenciavelezcortes characterizationandspatialmappingofthehumangutmetasecretome
AT harriswang characterizationandspatialmappingofthehumangutmetasecretome