Viruses in the faecal microbiota of monozygotic twins and their mothers

Abstract

Viral diversity and life cycles are poorly understood in the human gut and other body habitats. Phages and their encoded functions may provide informative signatures of a human microbiota and of microbial community responses to various disturbances, and may indicate whether community health or dysfunction is manifest after apparent recovery from a disease or therapeutic intervention. Here we report sequencing of the viromes (metagenomes) of virus-like particles isolated from faecal samples collected from healthy adult female monozygotic twins and their mothers at three time points over a one-year period. We compared these data sets with data sets of sequenced bacterial 16S ribosomal RNA genes and total-faecal-community DNA. Co-twins and their mothers share a significantly greater degree of similarity in their faecal bacterial communities than do unrelated individuals. In contrast, viromes are unique to individuals regardless of their degree of genetic relatedness. Despite remarkable interpersonal variations in viromes and their encoded functions, intrapersonal diversity is very low, with >95% of virotypes retained over the period surveyed, and with viromes dominated by a few temperate phages that exhibit remarkable genetic stability. These results indicate that a predatory viral–microbial dynamic, manifest in a number of other characterized environmental ecosystems, is notably absent in the very distal intestine.

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Figure 1: Classification of viruses present in VLP preparations generated from faecal samples collected from four families of monozygotic twins and their mothers.
Figure 2: Sample-by-sample view of the proportional representation of KEGG second-level pathways in sequenced VLP-associated viromes and gut microbiomes.
Figure 3: Gnotobiotic mice reveal in vivo activation of the transcriptome of an M. formatexigens prophage.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Gene Expression Omnibus

Data deposits

Virome data sets reported here are accessible in the NCBI Short Read Archive under accession number SRA012183. 16S rRNA data sets are available in GenBank under accession number SRA020605. RNA-Seq data have been deposited in the Gene Expression Omnibus as series GSE21906 (see Methods for further details).

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Acknowledgements

We thank S. Wagoner and J. Manchester for technical assistance, J. Faith for help developing Phage_omics and, together with F. Rey, for microbial RNA-Seq data sets, P. Turnbaugh for assistance with faecal metagenomic studies, and B. Rodriguez-Mueller and D. Willner for valuable discussions. This work was supported in part by grants from the NIH (American Recovery and Reinvestment Act supplemental funding of DK78669), the Crohn’s and Colitis Foundation of America and the Dr. Miriam and Sheldon G. Adelson Medical Research Foundation. A.R. is the recipient of an International Fulbright Science and Technology Program award.

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A.R. and J.I.G. designed the experiments; A.C.H. recruited the patients; A.R., M.H. and N.H. generated the data; A.R., F.E.A., F.R. and J.I.G. interpreted the results; and A.R., F.R. and J.I.G. wrote the paper.

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Correspondence to Jeffrey I. Gordon.

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The authors declare no competing financial interests.

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Reyes, A., Haynes, M., Hanson, N. et al. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466, 334–338 (2010). https://doi.org/10.1038/nature09199

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