Reproducible protocols for metagenomic analysis of human faecal phageomes View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2018-04-10

AUTHORS

Andrey N. Shkoporov, Feargal J. Ryan, Lorraine A. Draper, Amanda Forde, Stephen R. Stockdale, Karen M. Daly, Siobhan A. McDonnell, James A. Nolan, Thomas D.S. Sutton, Marion Dalmasso, Angela McCann, R. Paul Ross, Colin Hill

ABSTRACT

BACKGROUND: Recent studies have demonstrated that the human gut is populated by complex, highly individual and stable communities of viruses, the majority of which are bacteriophages. While disease-specific alterations in the gut phageome have been observed in IBD, AIDS and acute malnutrition, the human gut phageome remains poorly characterised. One important obstacle in metagenomic studies of the human gut phageome is a high level of discrepancy between results obtained by different research groups. This is often due to the use of different protocols for enriching virus-like particles, nucleic acid purification and sequencing. The goal of the present study is to develop a relatively simple, reproducible and cost-efficient protocol for the extraction of viral nucleic acids from human faecal samples, suitable for high-throughput studies. We also analyse the effect of certain potential confounding factors, such as storage conditions, repeated freeze-thaw cycles, and operator bias on the resultant phageome profile. Additionally, spiking of faecal samples with an exogenous phage standard was employed to quantitatively analyse phageomes following metagenomic sequencing. Comparative analysis of phageome profiles to bacteriome profiles was also performed following 16S rRNA amplicon sequencing. RESULTS: Faecal phageome profiles exhibit an overall greater individual specificity when compared to bacteriome profiles. The phageome and bacteriome both exhibited moderate change when stored at + 4 °C or room temperature. Phageome profiles were less impacted by multiple freeze-thaw cycles than bacteriome profiles, but there was a greater chance for operator effect in phageome processing. The successful spiking of faecal samples with exogenous bacteriophage demonstrated large variations in the total viral load between individual samples. CONCLUSIONS: The faecal phageome sequencing protocol developed in this study provides a valuable additional view of the human gut microbiota that is complementary to 16S amplicon sequencing and/or metagenomic sequencing of total faecal DNA. The protocol was optimised for several confounding factors that are encountered while processing faecal samples, to reduce discrepancies observed within and between research groups studying the human gut phageome. Rapid storage, limited freeze-thaw cycling and spiking of faecal samples with an exogenous phage standard are recommended for optimum results. More... »

PAGES

68

References to SciGraph publications

  • 2012-07-30. Storage conditions of intestinal microbiota matter in metagenomic analysis in BMC MICROBIOLOGY
  • 2015-01-22. Evaluation of methods to purify virus-like particles for metagenomic sequencing of intestinal viromes in BMC GENOMICS
  • 2014-07-24. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes in NATURE COMMUNICATIONS
  • 2017-03-03. Normalization and microbial differential abundance strategies depend upon data characteristics in MICROBIOME
  • 2017-01-23. Microbiota Transfer Therapy alters gut ecosystem and improves gastrointestinal and autism symptoms: an open-label study in MICROBIOME
  • 2014-12-05. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 in GENOME BIOLOGY
  • 2014-12-03. Temporal variability is a personalized feature of the human microbiome in GENOME BIOLOGY
  • 2011-04-20. Enterotypes of the human gut microbiome in NATURE
  • 2012-03-04. Fast gapped-read alignment with Bowtie 2 in NATURE METHODS
  • 2016-10-19. Tiny microbes, enormous impacts: what matters in gut microbiome studies? in GENOME BIOLOGY
  • 2015-11-17. Sample storage conditions significantly influence faecal microbiome profiles in SCIENTIFIC REPORTS
  • 2013-08-18. UPARSE: highly accurate OTU sequences from microbial amplicon reads in NATURE METHODS
  • 2010-03. A human gut microbial gene catalogue established by metagenomic sequencing in NATURE
  • 2016-06-21. Adjusting microbiome profiles for differences in microbial load by spike-in bacteria in MICROBIOME
  • 2015-10-08. SPINGO: a rapid species-classifier for microbial amplicon sequences in BMC BIOINFORMATICS
  • 2010-07. Viruses in the fecal microbiota of monozygotic twins and their mothers in NATURE
  • 2016-05-23. DADA2: High resolution sample inference from Illumina amplicon data in NATURE METHODS
  • 2016-12-02. Transmission of viruses via our microbiomes in MICROBIOME
  • 2015-09-14. Early life dynamics of the human gut virome and bacterial microbiome in infants in NATURE MEDICINE
  • 2015-11-17. Optimizing protocols for extraction of bacteriophages prior to metagenomic analyses of phage communities in the human gut in MICROBIOME
  • 2015-11-12. Modular approach to customise sample preparation procedures for viral metagenomics: a reproducible protocol for virome analysis in SCIENTIFIC REPORTS
  • 2012-03-13. The human microbiome: at the interface of health and disease in NATURE REVIEWS GENETICS
  • 2016-05-04. Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation in NATURE
  • 2013-06-09. Antibiotic Treatment Expands the Resistance Reservoir and Ecological Network of the Phage Metagenome in NATURE
  • 2016-06-21. Phages rarely encode antibiotic resistance genes: a cautionary tale for virome analyses in THE ISME JOURNAL: MULTIDISCIPLINARY JOURNAL OF MICROBIAL ECOLOGY
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    http://scigraph.springernature.com/pub.10.1186/s40168-018-0446-z

    DOI

    http://dx.doi.org/10.1186/s40168-018-0446-z

    DIMENSIONS

    https://app.dimensions.ai/details/publication/pub.1103148891

    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/29631623


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