Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation

Browne, Hilary P.; Forster, Samuel C.; Anonye, Blessing O.; Kumar, Nitin; Neville, B. Anne; Stares, Mark D.; Goulding, David; Lawley, Trevor D.

doi:10.1038/nature17645

Cited by 1,299Gut microbiota and healthMicrobial Community Ecology and PhysiologyGenomics and Phylogenetic Studies

Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation

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Browne, Hilary P., Forster, Samuel C., Anonye, Blessing O., Kumar, Nitin, Neville, B. Anne, Stares, Mark D., Goulding, David, Lawley, Trevor D.·2016·Nature

DOI 10.1038/nature17645PMC PMC4890681

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Abstract

Our intestinal microbiota harbours a diverse bacterial community required for our health, sustenance and wellbeing. Intestinal colonization begins at birth and climaxes with the acquisition of two dominant groups of strict anaerobic bacteria belonging to the Firmicutes and Bacteroidetes phyla. Culture-independent, genomic approaches have transformed our understanding of the role of the human microbiome in health and many diseases. However, owing to the prevailing perception that our indigenous bacteria are largely recalcitrant to culture, many of their functions and phenotypes remain unknown. Here we describe a novel workflow based on targeted phenotypic culturing linked to large-scale whole-genome sequencing, phylogenetic analysis and computational modelling that demonstrates that a substantial proportion of the intestinal bacteria are culturable. Applying this approach to healthy individuals, we isolated 137 bacterial species from characterized and candidate novel families, genera and species that were archived as pure cultures. Whole-genome and metagenomic sequencing, combined with computational and phenotypic analysis, suggests that at least 50-60% of the bacterial genera from the intestinal microbiota of a healthy individual produce resilient spores, specialized for host-to-host transmission. Our approach unlocks the human intestinal microbiota for phenotypic analysis and reveals how a marked proportion of oxygen-sensitive intestinal bacteria can be transmitted between individuals, affecting microbiota heritability.

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Many more species continue to be cultured as laboratory-based efforts have become more high-throughput.
“Many more species continue to be cultured as laboratory-based efforts have become more high-throughput 43,44 .”
From Human microbiome myths and misconceptions (2023) · cites this paper as [44]

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Authors: Browne, H. P., Forster, S. C., Anonye, B. O., Kumar, N., Neville, B. A., Stares, M. D., Goulding, D., & Lawley, T. D.
Affiliations: Wellcome Sanger Institute (GB)
Corresponding author: Lawley, Trevor D.
ORCID: Browne, Hilary P.
Forster, Samuel C.
Anonye, Blessing O.
Kumar, Nitin
Stares, Mark D.
Goulding, David
Lawley, Trevor D.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2016-05-04
Volume: 533
Issue: 7604
Pages: 543-546
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature17645
PMC: PMC4890681
OpenAlex: W2345813655
Cited by: 1,299
References: 41
Citations by year: 2026: 60 · 2025: 90 · 2024: 119 · 2023: 102 · 2022: 131 · 2021: 164 · 2020: 170 · 2019: 180 · 2018: 119 · 2017: 120 · 2016: 41 · 2015: 1
FWCI: 79.72
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Nature (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
CLOK (University of Central Lancashire) (acceptedVersion)
Monash University Research Portal (Monash University) (submittedVersion, other-oa)
RePEc: Research Papers in Economics (submittedVersion)
Funders: Wellcome Trust (098051)
State Government of Victoria
Medical Research Council (098051, PF451, MR/K000551/1)
National Health and Medical Research Council (1091097)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords: uncultured bacteria, human gut microbiome, bacterial sporulation, spore-forming bacteria, host-to-host transmission, novel bacterial taxa, Firmicutes, Bacteroidetes, anaerobic bacteria, metagenomics, whole genome sequencing
MeSH terms: Gastrointestinal Microbiome, Anaerobiosis, Bacteria, Feces, Health, Humans, Oxygen, Phenotype, Phylogeny, Species Specificity, Spores, Bacterial, Bacterial Typing Techniques, Genome, Bacterial, Sequence Analysis, DNA, Cell Culture Techniques, Metagenome, Metagenomics

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Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation

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