Characterization of the human DNA gut virome across populations with different subsistence strategies and geographical origin

Rampelli, Simone; Turroni, Silvia; Schnorr, Stephanie L.; Soverini, Matteo; Quercia, Sara; Barone, Monica; Castagnetti, Andréa; Biagi, Elena; Gallinella, Giorgio; Brigidi, Patrizia; Candela, Marco

doi:10.1111/1462-2920.13938

Cited by 38 publications

(31 citation statements)

References 47 publications

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“…Using de novo assembly and discovery approaches, we identi ed a huge number of viruses from the subjects' fecal samples, including approximately 55,000 non-redundant complete and partial DNA viral genomes and 569 non-redundant RNA viruses, particularly the number of DNA vOTUs increased over 8fold compared with the isolated viral sequences in RefSeq database. The majority of viruses were unclassi ed even at the family level, in agreement with previous observations of extensive novelty of viral world in multiple environments as well as in human gut [43][44][45].…”

Section: Discussionsupporting

confidence: 91%

Characterization of the Gut DNA and RNA Viromes in A Cohort of Chinese Residents and Visiting Pakistanis

Yan

Wang

Chen

et al. 2020

Preprint

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Background: Trillions of viruses inhabit the gastrointestinal tract. Some of them have been well-studied on their roles in infection and human health, but the majority remain unsurveyed. It has been established that the composition of the gut virome is highly variable based on the changes of diet, physical state, and environmental factors. However, the effect of host genetic factors, e.g. ethnic origin, on the gut virome is rarely investigated. Results: Here, we characterized and compared the gut virome in a cohort of local Chinese residents and visiting Pakistani individuals, each group containing 24 healthy adults and 6 children. Using metagenomic shotgun sequencing and assembly of fecal samples, a huge number of viral operational taxonomic units (vOTUs) were identified for profiling the DNA and RNA viromes. National background contributed a primary variation to individuals’ gut virome. Compared with the Chinese adults, the Pakistan adults showed higher macrodiversity and different compositional and functional structures in their DNA virome and lower diversity and altered composition in their RNA virome. The virome variations of Pakistan children were inherited from the that of the adults but also tended to share similar characteristics with the Chinese cohort. We also analyzed and compared the bacterial microbiome between two cohorts and further revealed numerous connections between virus and bacterial host. Statistically, the gut DNA and RNA viromes were covariant to some extent (p<0.001), and they both influenced the holistic bacterial composition and vice versa.Conclusions: we systematically described the baseline gut virome in a well-characterized cohort of Chinese and visiting Pakistanis and demonstrated that the national background contributed a primary variation to gut virome. The mechanisms underlying the difference between two cohorts remain unclear, but the ethnic factor must be proposed and considered in designing future studies of the virome.

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Section: Discussionsupporting

confidence: 91%

Characterization of the Gut DNA and RNA Viromes in A Cohort of Chinese Residents and Visiting Pakistanis

Yan

Wang

Chen

et al. 2020

Preprint

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“…The faecal virome diversity of Central India rural inhabitants was greater than their urban counterparts ( Figure 6B). A similar observation is described by Rampelli et al (2017), whereby two hunter-gatherer communities also had a higher faecal viral diversity compared to two Western society cohorts [39]. There were several limitations to this study.…”

Section: Discussionsupporting

confidence: 57%

Metagenomics Reveals Impact of Urbanisation in Central India on the Human Gut Microbiome and its Antimicrobial Resistance Profiles

Monaghan¹,

Sloan²,

Stockdale³

et al. 2019

Preprint

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Background The impact of the rapid urbanisation of low- and middle-income countries on the human gut microbiome remains grossly understudied. Whilst the effect of urbanisation on the bacterial populations of the human gut microbiome have been documented, little is known about the influence of diet and antibiotics on the bacteriome, its virome, and antibiotic resistome. Here, we use shotgun metagenomics to comprehensively characterise the bacterial and viral fractions of the human gut microbiome, and their encoded functions, from two divergent Central Indian populations (rural agriculturalists from Melghat and an urban population in Nagpur). Additionally, we investigate cohorts with and without diarrhoea, and the potential burden of Clostridioides difficile, associated with widespread unregulated use of antibiotics in India. Results We observed distinct rural-urban differences in the gut microbiome, including viral diversity and composition, with geography exhibiting a greater influence than diarrhoeal status. Urban microbiomes were enriched in metabolic pathways responsible for degradation of drugs and organic compounds, which were predicted to relate to replacement of rural-enriched Prevotella spp. and fermentative Clostridiales with Enterobacteriaceae and Bacteroides spp. By linking phages present in the microbiome to their bacterial hosts through CRISPR spacers, a shift from Prevotella- and Eubacterium-infecting phages to Bacteroides- and Parabacteroides-infecting phages was observed in rural and urban populations, respectively. Additionally, the auxiliary metabolic potential of rural-associated phage populations was enriched for carbon and amino acid energy harvesting potential, compared to urban-associated phages. A core set of antimicrobial resistance genes was identified in both populations, particularly those conferring resistance to macrolides, tetracyclines and 1stgeneration cephalosporins, with the majority also showing evidence of resistance to fluoroquinolones, aminoglycosides and sulphonamides. In a subgroup of urban subjects with diarrhoea and high antibiotic exposure, most of whom tested positive for C. difficile toxin, evidence of resistance to fosfomycin, glycopeptides, daptomycin, 3rd generation cephalosporins and carbapenems was widespread. Conclusions We report distinct differences in antimicrobial resistance gene profiles as well as a marked variation in the burden of C. difficile disease between rural and urban populations. The key drivers of variation in urban and rural Indian microbiomes are geography, diet, industrial and healthcare exposures.

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“…Moreover, a specific-host virome profile has been suggested, but this profile can be modified by endogenous and exogenous factors [ 7 ]. In particular, factors such as age, drugs, diet and infections could have effects on the virome composition, as has been observed in chickens, pigs and humans [ 8 – 10 ]. However, the structure of the fecal virome in wild ducks has not been researched.…”

Section: Introductionmentioning

confidence: 99%

Fecal virome composition of migratory wild duck species

et al. 2018

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The fecal virome comprises a complex diversity of eukaryotic viruses, phages and viruses that infect the host. However, little is known about the intestinal community of viruses that is present in wild waterfowl, and the structure of this community in wild ducks has not yet been studied. The fecal virome compositions of six species of wild dabbling ducks and one species of wild diving duck were thus analyzed. Fecal samples were collected directly from the rectums of 60 ducks donated by hunters. DNA and RNA virus particles were purified and sequenced using the MiSeq Illumina platform. The reads obtained from the sequencing were analyzed and compared with sequences in the GenBank database. Viral-related sequences from the Herpesviridae, Alloherpesviridae, Adenoviridae, Retroviridae and Myoviridae viral families showed the highest overall abundances in the samples. The virome analysis identified viruses that had not been found in wild duck feces and revealed distinct virome profiles between different species and between samples of the same species. This study increases our understanding of viruses in wild ducks as possible viral reservoirs and provides a basis for further studying and monitoring the transmission of viruses from wild animals to humans and disease outbreaks in domestic animals.

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Characterization of the human DNA gut virome across populations with different subsistence strategies and geographical origin

Cited by 38 publications

References 47 publications

Characterization of the Gut DNA and RNA Viromes in A Cohort of Chinese Residents and Visiting Pakistanis

Characterization of the Gut DNA and RNA Viromes in A Cohort of Chinese Residents and Visiting Pakistanis

Metagenomics Reveals Impact of Urbanisation in Central India on the Human Gut Microbiome and its Antimicrobial Resistance Profiles

Fecal virome composition of migratory wild duck species

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