Microviridae Goes Temperate: Microvirus-Related Proviruses Reside in the Genomes of Bacteroidetes

Krupovìč, Mart; Forterre, Patrick

doi:10.1371/journal.pone.0019893

Cited by 113 publications

(134 citation statements)

References 57 publications

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“…All four predicted proteins encoded by this phage with a 6.2-kb genome (Fig. 1E) exhibit significant similarity to the Alpavirinae, a recently described subfamily identified from Bacteroidetes prophages, that belongs to the Microviridae (previously considered to be exclusively lytic) (11,12). The changes in relative abundance of ϕHSC02 best correlated with a change (reduction) in the abundance of Bacteroides ovatus.…”

Section: Nonsimultaneous Detection Of Viruses and Community Rearrangementioning

confidence: 74%

Gnotobiotic mouse model of phage–bacterial host dynamics in the human gut

Reyes

McNulty

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

300

269

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Bacterial viruses (phages) are the most abundant biological group on Earth and are more genetically diverse than their bacterial prey/ hosts. To characterize their role as agents shaping gut microbial community structure, adult germ-free mice were colonized with a consortium of 15 sequenced human bacterial symbionts, 13 of which harbored one or more predicted prophages. One member, Bacteroides cellulosilyticus WH2, was represented by a library of isogenic transposon mutants that covered 90% of its genes. Once assembled, the community was subjected to a staged phage attack with a pool of live or heat-killed virus-like particles (VLPs) purified from the fecal microbiota of five healthy humans. Shotgun sequencing of DNA from the input pooled VLP preparation plus shotgun sequencing of gut microbiota samples and purified fecal VLPs from the gnotobiotic mice revealed a reproducible nonsimultaneous pattern of attack extending over a 25-d period that involved five phages, none described previously. This system allowed us to (i) correlate increases in specific phages present in the pooled VLPs with reductions in the representation of particular bacterial taxa, (ii) provide evidence that phage resistance occurred because of ecological or epigenetic factors, (iii) track the origin of each of the five phages among the five human donors plus the extent of their genome variation between and within recipient mice, and (iv) establish the dramatic in vivo fitness advantage that a locus within a B. cellulosilyticus prophage confers upon its host. Together, these results provide a defined community-wide view of phage-bacterial host dynamics in the gut.T he human gut is home to tens of trillions of microbial cells representing all three domains of life, although most are bacteria. These organisms collaborate and compete for functional niches and physical locations (habitats). Together, they form a continuously functioning microbial metabolic "organ." The microbial diversity, interpersonal variation, and dynamism of the human gut microbiota make the task of identifying the factors that define community configurations extremely challenging.In some ecosystems, phages maintain high bacterial strain level diversity through lysis of their host strains (constant diversity dynamics model; refs 1, 2). The resulting emptied niche is filled with either an evolved resistant bacterial strain or a taxonomically closely related bacterial species. These dynamics have been observed in open marine environments (1). In contrast, a recent study of 37 healthy adults indicated that a person's fecal microbiota was remarkably stable, with 60% of bacterial strains retained over the course of 5 y (3). Stability followed a power law dynamic that when extrapolated suggests that most strains in an individual's gut community are retained for decades (3). In a metagenomic analysis of virus-like particles (VLPs) purified from the fecal microbiota of healthy adult monozygotic twins and their mothers, sampled over the course of a year, viral community structure exh...

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Section: Nonsimultaneous Detection Of Viruses and Community Rearrangementioning

confidence: 74%

Gnotobiotic mouse model of phage–bacterial host dynamics in the human gut

Reyes

McNulty

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

300

269

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“…3 (32), but functional parallels emerged as follows. First, the largest gene (gp 2) is a DNA replication protein (Dataset S1), as in the ssDNA model phage ϕX174 [the A protein (33)].…”

Section: Resultsmentioning

confidence: 99%

Twelve previously unknown phage genera are ubiquitous in global oceans

Holmfeldt

Solonenko

Shah

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

171

173

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Viruses are fundamental to ecosystems ranging from oceans to humans, yet our ability to study them is bottlenecked by the lack of ecologically relevant isolates, resulting in "unknowns" dominating culture-independent surveys. Here we present genomes from 31 phages infecting multiple strains of the aquatic bacterium Cellulophaga baltica (Bacteroidetes) to provide data for an underrepresented and environmentally abundant bacterial lineage. Comparative genomics delineated 12 phage groups that (i) each represent a new genus, and (ii) represent one novel and four wellknown viral families. This diversity contrasts the few well-studied marine phage systems, but parallels the diversity of phages infecting human-associated bacteria. Although all 12 Cellulophaga phages represent new genera, the podoviruses and icosahedral, nontailed ssDNA phages were exceptional, with genomes up to twice as large as those previously observed for each phage type. Structural novelty was also substantial, requiring experimental phage proteomics to identify 83% of the structural proteins. The presence of uncommon nucleotide metabolism genes in four genera likely underscores the importance of scavenging nutrient-rich molecules as previously seen for phages in marine environments. Metagenomic recruitment analyses suggest that these particular Cellulophaga phages are rare and may represent a first glimpse into the phage side of the rare biosphere. However, these analyses also revealed that these phage genera are widespread, occurring in 94% of 137 investigated metagenomes. Together, this diverse and novel collection of phages identifies a small but ubiquitous fraction of unknown marine viral diversity and provides numerous environmentally relevant phage-host systems for experimental hypothesis testing. model systems | phage genomics | phage taxonomy | queuosine biosynthesis | prophage

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“…As a result, nine contigs were assembled from viromes derived from atmospheric 32 and aquatic 26,33,34 samples. As ssDNA viruses are known to integrate into the genomes of their hosts 35,36 , we also searched for the presence of CHIVs in the eukaryotic genome databases. The latter approach yielded four additional contigs matching our criteria.…”

Section: Resultsmentioning

confidence: 99%

Chimeric viruses blur the borders between the major groups of eukaryotic single-stranded DNA viruses

et al. 2013

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Metagenomic studies have uncovered an astonishing diversity of ssDNA viruses encoding replication proteins (Reps) related to those of eukaryotic Circoviridae, Geminiviridae or Nanoviridae; however, exact evolutionary relationships among these viruses remain obscure. Recently, a unique chimeric virus (CHIV) genome, which has apparently emerged via recombination between ssRNA and ssDNA viruses, has been discovered. Here we report on the assembly of 13 new CHIV genomes recovered from various environments. Our results indicate a single event of capsid protein (CP) gene capture from an RNA virus in the history of this virus group. The domestication of the CP gene was followed by an unprecedented recurrent replacement of the Rep genes in CHIVs with distant counterparts from diverse ssDNA viruses. We suggest that parasitic and symbiotic interactions between unicellular eukaryotes were central for the emergence of CHIVs and that such turbulent evolution was primarily dictated by incongruence between the CP and Rep proteins.

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Microviridae Goes Temperate: Microvirus-Related Proviruses Reside in the Genomes of Bacteroidetes

Cited by 113 publications

References 57 publications

Gnotobiotic mouse model of phage–bacterial host dynamics in the human gut

Gnotobiotic mouse model of phage–bacterial host dynamics in the human gut

Twelve previously unknown phage genera are ubiquitous in global oceans

Chimeric viruses blur the borders between the major groups of eukaryotic single-stranded DNA viruses

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