Centenarians have a diverse gut virome with the potential to modulate metabolism and promote healthy lifespan

Johansen, Joachim; Atarashi, Koji; Arai, Yasumichi; Hirose, Nobuyoshi; Sørensen, Søren J.; Vatanen, Tommi; Knip, Mikael; Honda, Kenya; Xavier, Ramnik J.; Rasmussen, Simon; Plichta, Damian R.

doi:10.1038/s41564-023-01370-6

Cited by 34 publications

(23 citation statements)

References 61 publications

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“…Similarities of these genes between T.nexilis_strain B1 and R.gnavus_strain suggested that these genes are encoded on MGEs. Moreover, four sulphur related genes included in strain B1, B2, and B3 (but not in strain A1, A2, and A3) were similar to those of phage genomes, which is consistent with the previous finding showing that many microbial genes related to sulphur metabolism are encoded on prophages 42 . Considering that several sulphate-reducing bacteria have resistance to oxidative stress 43 , this feature may affect the survival of strain B in an oxidative environment.…”

Section: Discussionsupporting

confidence: 91%

Horizontal gene transfer shapes pathogenic bacteria in multiple sclerosis

Yamamura,

Takewaki,

Kiguchi

et al. 2023

Preprint

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Multiple sclerosis (MS) is an autoimmune demyelinating disease influenced by environmental factors. Except during relapses, baseline neurological status is generally stable in the early stage, whereas progressive deterioration may occur silently. The progressive disease form (secondary progressive MS; SPMS) characterised by both neuroinflammation and neurodegeneration differs significantly from the non-progressive form in microbiome profiles1 2 3. After confirming an increased abundance of gut bacterium “Tyzzerella nexilis” in SPMS, the role of T.nexilis in progressive MS was studied. The strain-level analysis based on long-read metagenomics identified a distinct cluster of T.nexilis highly enriched in SPMS. T.nexilis strains in this novel cluster were characterised by an incredible number of mobile genetic elements (MGEs) and the absence of defence systems against MGEs. Mono-colonisation with this MGEs-enriched T.nexilis strain made germ-free mice more susceptible to induction of experimental autoimmune encephalomyelitis. The pathogenicity of this strain was mediated by TLR5 stimulation by flagella encoded on MGEs. Moreover, this T.nexilis strain was thought to have potentials of causing neurodegeneration, because of its ability to produce reduced sulphur compounds encoded on MGEs. Such a horizontal gene transfer, causing functional diversity beyond existing bacterial taxonomy, may have causal implications in chronic disorders influenced by gut microbiome.

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Section: Discussionsupporting

confidence: 91%

Horizontal gene transfer shapes pathogenic bacteria in multiple sclerosis

Yamamura,

Takewaki,

Kiguchi

et al. 2023

Preprint

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“…The design of the DRiDO study is described in depth in Di Francesco et al Briefly, 937 female DO mice began one of five dietary interventions at six months of age (Fig. 1a, see Methods): ad libitum food consumption (AL, control group), fasting one day per week (1D), fasting two consecutive days per week (2D), consuming 20% fewer calories every day (20), or consuming 40% fewer calories every day (40). Mice were extensively phenotyped over their lifespans (Extended Data Table 1).…”

Section: Longitudinal Metagenomic Sequencing Of Diversity Outbred Micementioning

confidence: 99%

“…First, how does the microbiome age? Numerous studies in mice [15][16][17] and humans [18][19][20][21] have reported ageassociated microbiome changes, but these changes are inconsistent across cohorts 22 . Two community features frequently reported to increase with age are ɑ-diversity 18,[22][23][24] and uniqueness 25,26 .…”

Section: Introductionmentioning

confidence: 99%

Interactions between the gut microbiome, dietary restriction, and aging in genetically diverse mice

Litichevskiy,

Considine,

Gill

et al. 2023

Preprint

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SummaryThe intestinal microbiome changes with age, but the causes and consequences of microbiome aging remain unclear. Furthermore, the gut microbiome has been proposed to mediate the benefit of lifespan- extending interventions such as dietary restriction, but this hypothesis warrants further exploration. Here, by analyzing 2997 metagenomes collected longitudinally from 913 deeply phenotyped, genetically diverse mice, we provide new insights into the interplay between the microbiome, aging, dietary restriction, host genetics, and a wide range of health parameters. First, we find that microbiome uniqueness increases with age across datasets and species. Moreover, age-associated changes are better explained by cumulative exposure to stochastic events (neutral theory) than by the influence of an aging host (selection theory). Second, we unexpectedly find that the majority of microbiome features are significantly heritable and that the amount of variation explained by host genetics is as large as that of aging and dietary restriction. Third, we find that the intensity of dietary restriction parallels the extent of microbiome changes and that dietary restriction does not rejuvenate the microbiome. Lastly, we find that the microbiome is significantly associated with multiple health parameters — including body composition, immune parameters, and frailty — but not with lifespan. In summary, this large and multifaceted study sheds light on the factors influencing the microbiome and aspects of host physiology modulated by the microbiome.

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“…Whether a mild phage infects a host via a lysogenic or lytic cycle depends on the environment; stressors such as DNA damage or nutritional deficiencies can induce prophages to enter the lytic cycle, with phages favoring the lysogenic cycle in the intestinal tracts of healthy young adults, whereas, in the intestinal tracts of centenarians, concomitant inflammatory stimuli and nutritional deficiencies may induce phages to switch more frequently to the lytic cycle [ 17 ]. Host abundance also influences the mode of infection; when bacteria are more abundant, phages prefer to infect bacteria via the lytic cycle.…”

Section: Introductionmentioning

confidence: 99%

Developmental Dynamics of the Gut Virome in Tibetan Pigs at High Altitude: A Metagenomic Perspective across Age Groups

Luo,

Guan,

et al. 2024

Viruses

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Tibetan pig is a geographically isolated pig breed that inhabits high-altitude areas of the Qinghai–Tibetan plateau. At present, there is limited research on viral diseases in Tibetan pigs. This study provides a novel metagenomic exploration of the gut virome in Tibetan pigs (altitude ≈ 3000 m) across three critical developmental stages, including lactation, nursery, and fattening. The composition of viral communities in the Tibetan pig intestine, with a dominant presence of Microviridae phages observed across all stages of development, in combination with the previous literature, suggest that it may be associated with geographical locations with high altitude. Functional annotation of viral operational taxonomic units (vOTUs) highlights that, among the constantly increasing vOTUs groups, the adaptability of viruses to environmental stressors such as salt and heat indicates an evolutionary response to high-altitude conditions. It shows that the lactation group has more abundant viral auxiliary metabolic genes (vAMGs) than the nursery and fattening groups. During the nursery and fattening stages, this leaves only DNMT1 at a high level. which may be a contributing factor in promoting gut health. The study found that viruses preferentially adopt lytic lifestyles at all three developmental stages. These findings not only elucidate the dynamic interplay between the gut virome and host development, offering novel insights into the virome ecology of Tibetan pigs and their adaptation to high-altitude environments, but also provide a theoretical basis for further studies on pig production and epidemic prevention under extreme environmental conditions.

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Centenarians have a diverse gut virome with the potential to modulate metabolism and promote healthy lifespan

Cited by 34 publications

References 61 publications

Horizontal gene transfer shapes pathogenic bacteria in multiple sclerosis

Horizontal gene transfer shapes pathogenic bacteria in multiple sclerosis

Interactions between the gut microbiome, dietary restriction, and aging in genetically diverse mice

Developmental Dynamics of the Gut Virome in Tibetan Pigs at High Altitude: A Metagenomic Perspective across Age Groups

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