Comprehensive insights from composition to functional microbe-based biodiversity of the infant human gut microbiota
Abstract During infancy, gut microbiota development is a crucial process involved in the establishment of microbe–host interactions which may persist throughout adulthood, and which are believed to influence host health. To fully understand the complexities of such interactions, it is essential to a...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-05-01
|
| Series: | npj Biofilms and Microbiomes |
| Online Access: | https://doi.org/10.1038/s41522-023-00392-6 |
| _version_ | 1827948292832493568 |
|---|---|
| author | Gabriele Andrea Lugli Leonardo Mancabelli Christian Milani Federico Fontana Chiara Tarracchini Giulia Alessandri Douwe van Sinderen Francesca Turroni Marco Ventura |
| author_facet | Gabriele Andrea Lugli Leonardo Mancabelli Christian Milani Federico Fontana Chiara Tarracchini Giulia Alessandri Douwe van Sinderen Francesca Turroni Marco Ventura |
| author_sort | Gabriele Andrea Lugli |
| collection | DOAJ |
| description | Abstract During infancy, gut microbiota development is a crucial process involved in the establishment of microbe–host interactions which may persist throughout adulthood, and which are believed to influence host health. To fully understand the complexities of such interactions, it is essential to assess gut microbiota diversity of newborns and its associated microbial dynamics and relationships pertaining to health and disease. To explore microbial biodiversity during the first 3 years of human life, 10,935 shotgun metagenomic datasets were taxonomically and functionally classified. Microbial species distribution between infants revealed the presence of eight major Infant Community State Types (ICSTs), being dominated by 17 bacterial taxa, whose distribution was shown to correspond to the geographical origin and infant health status. In total, 2390 chromosomal sequences of the predominant taxa were reconstructed from metagenomic data and used in combination with 44,987 publicly available genomes to trace the distribution of microbial Population Subspecies (PS) within the different infant groups, revealing patterns of multistrain coexistence among ICSTs. Finally, implementation of a metagenomic- and metatranscriptomic-based metabolic profiling highlighted different enzymatic expression patterns of the gut microbiota that allowed us to acquire insights into mechanistic aspects of health-gut microbiota interplay in newborns. Comparison between metagenomic and metatranscriptomic data highlights how a complex environment like the human gut must be investigated by employing both sequencing methodologies and possibly supplemented with metabolomics approaches. While metagenomic analyses are very useful for microbial classification aimed at unveiling key players driving microbiota balances, using these data to explain functionalities of the microbiota is not always warranted. |
| first_indexed | 2024-04-09T12:52:01Z |
| format | Article |
| id | doaj.art-c38aa33a467142929e6ff997207f7ad6 |
| institution | Directory Open Access Journal |
| issn | 2055-5008 |
| language | English |
| last_indexed | 2024-04-09T12:52:01Z |
| publishDate | 2023-05-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | npj Biofilms and Microbiomes |
| spelling | doaj.art-c38aa33a467142929e6ff997207f7ad62023-05-14T11:10:18ZengNature Portfolionpj Biofilms and Microbiomes2055-50082023-05-019111310.1038/s41522-023-00392-6Comprehensive insights from composition to functional microbe-based biodiversity of the infant human gut microbiotaGabriele Andrea Lugli0Leonardo Mancabelli1Christian Milani2Federico Fontana3Chiara Tarracchini4Giulia Alessandri5Douwe van Sinderen6Francesca Turroni7Marco Ventura8Laboratory of Probiogenomics, Department of Chemistry, Life Sciences, and Environmental Sustainability, University of ParmaDepartment of Medicine and Surgery, University of ParmaLaboratory of Probiogenomics, Department of Chemistry, Life Sciences, and Environmental Sustainability, University of ParmaLaboratory of Probiogenomics, Department of Chemistry, Life Sciences, and Environmental Sustainability, University of ParmaLaboratory of Probiogenomics, Department of Chemistry, Life Sciences, and Environmental Sustainability, University of ParmaLaboratory of Probiogenomics, Department of Chemistry, Life Sciences, and Environmental Sustainability, University of ParmaAPC Microbiome Institute and School of Microbiology, Bioscience Institute, National University of IrelandLaboratory of Probiogenomics, Department of Chemistry, Life Sciences, and Environmental Sustainability, University of ParmaLaboratory of Probiogenomics, Department of Chemistry, Life Sciences, and Environmental Sustainability, University of ParmaAbstract During infancy, gut microbiota development is a crucial process involved in the establishment of microbe–host interactions which may persist throughout adulthood, and which are believed to influence host health. To fully understand the complexities of such interactions, it is essential to assess gut microbiota diversity of newborns and its associated microbial dynamics and relationships pertaining to health and disease. To explore microbial biodiversity during the first 3 years of human life, 10,935 shotgun metagenomic datasets were taxonomically and functionally classified. Microbial species distribution between infants revealed the presence of eight major Infant Community State Types (ICSTs), being dominated by 17 bacterial taxa, whose distribution was shown to correspond to the geographical origin and infant health status. In total, 2390 chromosomal sequences of the predominant taxa were reconstructed from metagenomic data and used in combination with 44,987 publicly available genomes to trace the distribution of microbial Population Subspecies (PS) within the different infant groups, revealing patterns of multistrain coexistence among ICSTs. Finally, implementation of a metagenomic- and metatranscriptomic-based metabolic profiling highlighted different enzymatic expression patterns of the gut microbiota that allowed us to acquire insights into mechanistic aspects of health-gut microbiota interplay in newborns. Comparison between metagenomic and metatranscriptomic data highlights how a complex environment like the human gut must be investigated by employing both sequencing methodologies and possibly supplemented with metabolomics approaches. While metagenomic analyses are very useful for microbial classification aimed at unveiling key players driving microbiota balances, using these data to explain functionalities of the microbiota is not always warranted.https://doi.org/10.1038/s41522-023-00392-6 |
| spellingShingle | Gabriele Andrea Lugli Leonardo Mancabelli Christian Milani Federico Fontana Chiara Tarracchini Giulia Alessandri Douwe van Sinderen Francesca Turroni Marco Ventura Comprehensive insights from composition to functional microbe-based biodiversity of the infant human gut microbiota npj Biofilms and Microbiomes |
| title | Comprehensive insights from composition to functional microbe-based biodiversity of the infant human gut microbiota |
| title_full | Comprehensive insights from composition to functional microbe-based biodiversity of the infant human gut microbiota |
| title_fullStr | Comprehensive insights from composition to functional microbe-based biodiversity of the infant human gut microbiota |
| title_full_unstemmed | Comprehensive insights from composition to functional microbe-based biodiversity of the infant human gut microbiota |
| title_short | Comprehensive insights from composition to functional microbe-based biodiversity of the infant human gut microbiota |
| title_sort | comprehensive insights from composition to functional microbe based biodiversity of the infant human gut microbiota |
| url | https://doi.org/10.1038/s41522-023-00392-6 |
| work_keys_str_mv | AT gabrieleandrealugli comprehensiveinsightsfromcompositiontofunctionalmicrobebasedbiodiversityoftheinfanthumangutmicrobiota AT leonardomancabelli comprehensiveinsightsfromcompositiontofunctionalmicrobebasedbiodiversityoftheinfanthumangutmicrobiota AT christianmilani comprehensiveinsightsfromcompositiontofunctionalmicrobebasedbiodiversityoftheinfanthumangutmicrobiota AT federicofontana comprehensiveinsightsfromcompositiontofunctionalmicrobebasedbiodiversityoftheinfanthumangutmicrobiota AT chiaratarracchini comprehensiveinsightsfromcompositiontofunctionalmicrobebasedbiodiversityoftheinfanthumangutmicrobiota AT giuliaalessandri comprehensiveinsightsfromcompositiontofunctionalmicrobebasedbiodiversityoftheinfanthumangutmicrobiota AT douwevansinderen comprehensiveinsightsfromcompositiontofunctionalmicrobebasedbiodiversityoftheinfanthumangutmicrobiota AT francescaturroni comprehensiveinsightsfromcompositiontofunctionalmicrobebasedbiodiversityoftheinfanthumangutmicrobiota AT marcoventura comprehensiveinsightsfromcompositiontofunctionalmicrobebasedbiodiversityoftheinfanthumangutmicrobiota |