Shotgun Metagenomics of 250 Adult Twins Reveals Genetic and Environmental Impacts on the Gut Microbiome
Open accessAbstract
The gut microbiota has been typically viewed as an environmental factor for human health. Twins are well suited for investigating the concordance of their gut microbiomes and decomposing genetic and environmental influences. However, existing twin studies utilizing metagenomic shotgun sequencing have included only a few samples. Here, we sequenced fecal samples from 250 adult twins in the TwinsUK registry and constructed a comprehensive gut microbial reference gene catalog. We demonstrate heritability of many microbial taxa and functional modules in the gut microbiome, including those associated with diseases. Moreover, we identified 8 million SNPs in the gut microbiome and observe a high similarity in microbiome SNPs between twins that slowly decreases after decades of living apart. The results shed new light on the genetic and environmental influences on the composition and function of the gut microbiome that could relate to risk of complex diseases.
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The gut microbiome is unique in each individual, even when considering identical twins.
“The gut microbiome is unique in each individual, even when considering identical twins20,35”
From Cross-cohort gut microbiome associations with immune checkpoint inhibitor response in advanced melanoma (2022) · cites this paper as [35]
Studies have found evidence for heritability of relative bacterial abundances or specific taxa.
“with studies finding evidence for heritability of relative bacterial abundances or specific taxa [15, 63–68]”
From Population structure of human gut bacteria in a diverse cohort from rural Tanzania and Botswana (2019) · cites this paper as [66]
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Labbé, A., Ganopolsky, J. G., Martoni, C., Prakash, S., & Jones, M. L. (2014) · PLoS ONE · doi:10.1371/journal.pone.0115175 · Cited by 144 · see citing works
Taras, D., Simmering, R., Collins, M. D., Lawson, P. A., & Blaut, M. (2002) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/00207713-52-2-423 · Cited by 143 · see citing works
Dietary Patterns and Heritability of Food Choice in a UK Female Twin Cohort
Teucher, B., Skinner, J. S., Skidmore, P. M. L., Cassidy, A., Fairweather‐Tait, S. J., Hooper, L., Roe, M. A., Foxall, R., Oyston, S. L., Cherkas, L. F., et al. (2007) · Twin Research and Human Genetics · doi:10.1375/twin.10.5.734 · Cited by 114 · see citing works
Self-citationAn integrated epigenomic analysis for type 2 diabetes susceptibility loci in monozygotic twins
Yuan, W., Xia, Y., Bell, C. G., Yet, İ., Ferreira, T. C., Ward, K. J., Gao, F., Loomis, A. K., Hyde, C. L., Wu, H., et al. (2014) · Nature Communications · doi:10.1038/ncomms6719 · Cited by 113 · see citing works
Self-citationResponsiveness of cardiometabolic-related microbiota to diet is influenced by host genetics
O’Connor, A., Quizon, P. M., Albright, J., Lin, F. T., & Bennett, B. J. (2014) · Mammalian Genome · doi:10.1007/s00335-014-9540-0 · Cited by 67 · see citing works
Probiotics and Other Key Determinants of Dietary Oxalate Absorption
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Early Microbial Markers of Celiac Disease
Viitasalo, L., Niemi, L., Ashorn, M. H., Ashorn, S., Braun, J. G., Huhtala, H., Collin, P., Mäki, M., Kaukinen, K., Kurppa, K., et al. (2014) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0000000000000089 · Cited by 29 · see citing works
Flagged first, then by citations
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Environment dominates over host genetics in shaping human gut microbiota
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Self-citationThe Human Gut Microbiome: From Association to Modulation
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Interplay between the human gut microbiome and host metabolism
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Self-citationEnvironmental factors shaping the gut microbiome in a Dutch population
Gacesa, R., Kurilshikov, A., Vich Vila, A., Sinha, T., Klaassen, M. A. Y., Bolte, L. A., Andreu-Sánchez, S., Chen, L., Collij, V., Hu, S., et al. (2022) · Nature · doi:10.1038/s41586-022-04567-7 · Cited by 735 · see citing works
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Accessible, curated metagenomic data through ExperimentHub
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Human genetic variation and the gut microbiome in disease
Hall, A. B., Tolonen, A. C., & Xavier, R. J. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2017.63 · Cited by 517 · see citing works
The person-to-person transmission landscape of the gut and oral microbiomes
Valles-Colomer, M., Blanco-Míguez, A., Manghi, P., Asnicar, F., Dubois, L., Golzato, D., Armanini, F., Cumbo, F., Huang, K. D., Manara, S., et al. (2023) · Nature · doi:10.1038/s41586-022-05620-1 · Cited by 449 · see citing works
Self-citationLee, K. A., Thomas, A. M., Bolte, L. A., Björk, J. R., de Ruijter, L. K., Armanini, F., Asnicar, F., Blanco-Miguez, A., Board, R., Calbet-Llopart, N., et al. (2022) · Nature Medicine · doi:10.1038/s41591-022-01695-5 · Cited by 464 · see citing works
Self-citationAdaptive Evolution within Gut Microbiomes of Healthy People
Zhao, S., Lieberman, T. D., Poyet, M., Kauffman, K. M., Gibbons, S. M., Groussin, M., Xavier, R. J., & Alm, E. J. (2019) · Cell Host & Microbe · doi:10.1016/j.chom.2019.03.007 · Cited by 434 · see citing works
Metagenome-wide association of gut microbiome features for schizophrenia
Zhu, F., Ju, Y., Wang, W., Wang, Q., Guo, R., Ma, Q., Sun, Q., Fan, Y., Xie, Y., Yang, Z., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15457-9 · Cited by 409 · see citing works
Self-citationBreast cancer in postmenopausal women is associated with an altered gut metagenome
Zhu, J., Liao, M., Yao, Z., Liang, W., Li, Q., Liu, J., Yang, H., Ji, Y., Wei, W., Tan, A., et al. (2018) · Microbiome · doi:10.1186/s40168-018-0515-3 · Cited by 377 · see citing works
Self-citationZhu, F., Guo, R., Wang, W., Ju, Y., Wang, Q., Ma, Q., Sun, Q., Fan, Y., Xie, Y., Yang, Z., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-019-0475-4 · Cited by 323 · see citing works
Self-citationThe Relationship Between the Human Genome and Microbiome Comes into View
Goodrich, J. K., Davenport, E. R., Clark, A. G., & Ley, R. E. (2017) · Annual Review of Genetics · doi:10.1146/annurev-genet-110711-155532 · Cited by 311 · see citing works
Heiss, C. N., & Olofsson, L. E. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12684 · Cited by 304 · see citing works
Host Genetics and Gut Microbiome: Challenges and Perspectives
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High-throughput, single-microbe genomics with strain resolution, applied to a human gut microbiome
Zheng, W., Zhao, S., Yin, Y., Zhang, H., Needham, D. M., Evans, E. D., Dai, C. L., Lu, P. J., Alm, E. J., & Weitz, D. A. (2022) · Science · doi:10.1126/science.abm1483 · Cited by 283 · see citing works
A faecal microbiota signature with high specificity for pancreatic cancer
Kartal, E., Schmidt, T. S. B., Molina-Montes, E., Rodríguez-Perales, S., Wirbel, J., Maistrenko, O. M., Akanni, W. A., Alashkar Alhamwe, B., Alves, R. J., Carrato, A., et al. (2022) · Gut · doi:10.1136/gutjnl-2021-324755 · Cited by 290 · see citing works
Gut microbiota changes in the extreme decades of human life: a focus on centenarians
Santoro, A., Ostan, R., Candela, M., Biagi, E., Brigidi, P., Capri, M., & Franceschi, C. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2674-y · Cited by 250 · see citing works
Codiversification of gut microbiota with humans
Suzuki, T. A., Fitzstevens, J. L., Schmidt, V. T., Enav, H., Huus, K. E., Mbong Ngwese, M., Grießhammer, A., Pfleiderer, A., Adegbite, B. R., Zinsou, J. F., et al. (2022) · Science · doi:10.1126/science.abm7759 · Cited by 210 · see citing works
Self-citationGut Dysbiosis and Muscle Aging: Searching for Novel Targets against Sarcopenia
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Compositional and functional features of the female premenopausal and postmenopausal gut microbiota
Zhao, H., Chen, J., Li, X., Sun, Q., Qin, P., & Wang, Q. (2019) · FEBS Letters · doi:10.1002/1873-3468.13527 · Cited by 138 · see citing works
Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy
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Microbiome-health interactions in older people
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Population structure of human gut bacteria in a diverse cohort from rural Tanzania and Botswana
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Metabolic independence drives gut microbial colonization and resilience in health and disease
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- Authors
- Xie, H., Guo, R., Zhong, H., Feng, Q., Lan, Z., Qin, B., Ward, K. J., Jackson, M. A., Xia, Y., Chen, X., Chen, B., Xia, H., Xu, C., Li, F., Xu, X., Al-Aama, J. Y., Yang, H., Wang, J., Kristiansen, K., Wang, J., Steves, C. J., Bell, J. T., Li, J., Spector, T. D., & Jia, H.
- Affiliations
- BGI Group (China) (CN)
- King's College London (GB)
- Corresponding author
- Li, Junhua
- Jia, Huijue
- ORCID
- Venue
- Cell Systems
- Publisher
- Elsevier BV
- Published
- 2016-12
- Volume
- 3
- Issue
- 6
- Pages
- 572-584.e3
- ISSN
- 2405-4712 (ISSN-L)
- PMC
- PMC6309625
- OpenAlex
- W2548330566
- Cited by
- 341
- References
- 87
- Citations by year
- 2026: 12 · 2025: 18 · 2024: 46 · 2023: 39 · 2022: 47 · 2021: 51 · 2020: 39 · 2019: 44 · 2018: 29 · 2017: 15
- FWCI
- 15.24
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell Systems (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Research Portal (King's College London) (submittedVersion)
- Funders
- Wellcome Trust (105022/Z/14/Z)
- NIH (RO1 DK093595, DP2 OD007444)
- Shenzhen Municipal Government of China (JSGG20140702161403250, DRC-SZ[2015]162, CXB201108250098A, JSGG20160229172752028, JCYJ20160229172757249)
- Fund for Science and Technology Development (FDCT) (077/2014/A2)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Keywords
- gut microbiota, twins, heritability, genetic factors, environmental influences, microbial taxa, functional modules, TwinsUK, fecal microbiota, complex diseases
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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