A cryptic plasmid is among the most numerous genetic elements in the human gut

Fogarty, Emily C.; Schechter, Matthew S.; Lolans, Karen; Sheahan, Madeline L.; Veseli, Iva; Moore, Ryan M.; Kiefl, Evan; Moody, Thomas; Rice, Phoebe A.; Yu, Michael K.; Mimee, Mark; Chang, Eugene B.; Ruscheweyh, Hans-Joachim; Sunagawa, Shinichi; Mclellan, Sandra L.; Willis, Amy D.; Comstock, Laurie E.; Eren, A. Murat

doi:10.1016/j.cell.2024.01.039

Cited by 19 publications

(9 citation statements)

References 146 publications

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“…The transfer frequency in plate-grown co-cultured bacteria was approximately 10 -8 transformants/recipient (Fig 5E). This frequency is one to two orders of magnitude lower than other well-studied mobile genetic elements in Bacteroides 57–59 . As expected by the low level of transcription of the conjugation genes during in vitro biofilm growth, no transfer was detected in biofilms grown in liquid medium.…”

Section: Resultsmentioning

confidence: 66%

“…While most MGEs are highly variable, subject to frequent recombination, and geographically clustered 15,17 , a few “fitness optimal” combinations are conserved. To our knowledge, only one other 2.7-kb plasmid is as highly prevalent as pMMCAT, but this very small cryptic plasmid appears to be parasitic on its host cell 57 . Our data show that pMMCAT confers a significant fitness advantage to the strains that acquire it, potentially explaining its rapid fixation in human populations.…”

Section: Discussionmentioning

confidence: 88%

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A pervasive large conjugative plasmid mediates multispecies biofilm formation in the intestinal microbiota increasing resilience to perturbations

García-Bayona,

Said,

Coyne

et al. 2024

Preprint

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Although horizontal gene transfer is pervasive in the intestinal microbiota, we understand only superficially the roles of most exchanged genes and how the mobile repertoire affects community dynamics. Similarly, little is known about the mechanisms underlying the ability of a community to recover after a perturbation. Here, we identified and functionally characterized a large conjugative plasmid that is one of the most frequently transferred elements among Bacteroidales species and is ubiquitous in diverse human populations. This plasmid encodes both an extracellular polysaccharide and fimbriae, which promote the formation of multispecies biofilms in the mammalian gut. We use a hybridization-based approach to visualize biofilms in clarified whole colon tissue with unprecedented 3D spatial resolution. These biofilms increase bacterial survival to common stressors encountered in the gut, increasing strain resiliency, and providing a rationale for the plasmid's recent spread and high worldwide prevalence.

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Section: Resultsmentioning

confidence: 66%

Section: Discussionmentioning

confidence: 88%

A pervasive large conjugative plasmid mediates multispecies biofilm formation in the intestinal microbiota increasing resilience to perturbations

García-Bayona,

Said,

Coyne

et al. 2024

Preprint

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“…8 kb that was recently described as one of the most abundant genetic elements of the human gut microbiome. 73 We found pBI143 in strains of 16 of the 21 ecosystems and 40 of the 127 clonal lineages, including 14 species. In addition, we found another small plasmid of ∼5 kbp that was present in strains of seven communities.…”

Section: Resultsmentioning

confidence: 70%

Comprehensive analyses of a large human gut Bacteroidales culture collection reveal species and strain level diversity and evolution

Zhang,

Cole,

Coyne

et al. 2024

Preprint

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Species of the Bacteroidales order are among the most abundant and stable bacterial members of the human gut microbiome with diverse impacts on human health. While Bacteroidales strains and species are genomically and functionally diverse, order-wide comparative analyses are lacking. We cultured and sequenced the genomes of 408 Bacteroidales isolates from healthy human donors representing nine genera and 35 species and performed comparative genomic, gene-specific, mobile gene, and metabolomic analyses. Families, genera, and species could be grouped based on many distinctive features. However, we also show extensive DNA transfer between diverse families, allowing for shared traits and strain evolution. Inter- and intra-specific diversity is also apparent in the metabolomic profiling studies. This highly characterized and diverse Bacteroidales culture collection with strain-resolved genomic and metabolomic analyses can serve as a resource to facilitate informed selection of strains for microbiome reconstitution.

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“…A recent paper described the discovery of a “cryptic” plasmid named pBI143, which was discovered by shotgun metagenomics of the human gut microbiome . This plasmid is highly enriched in the human microbiome, is ∼14 times more enriched than Carjivirus , is reportedly ubiquitous in industrialized gut microbiomes, and has reported sewage concentrations of >10 8 GC/100 mL . The role of this plasmid in the microbiome is unclear, and it may be a “genetic parasite” .…”

Section: Introductionmentioning

confidence: 99%

“…This plasmid is highly enriched in the human microbiome, is ∼14 times more enriched than Carjivirus , is reportedly ubiquitous in industrialized gut microbiomes, and has reported sewage concentrations of >10 8 GC/100 mL . The role of this plasmid in the microbiome is unclear, and it may be a “genetic parasite” . Initial screening of pBI143 suggested that it is correlated with fecal contamination in environmental waters but at a concentration higher than those of other molecular fecal indicators .…”

Section: Introductionmentioning

confidence: 99%

Assessing the Relative Concentration Efficiency and Spatial–Temporal Distribution of Plasmid pBI143 in Raw Wastewater

Oceguera Johnson,

Shaffer,

North

et al. 2024

Environ. Sci. Technol. Lett.

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Plasmid pBI143 has recently been identified as being highly abundant in the human gut microbiome, suggesting potential as a fecal water quality indicator and normalization marker in wastewater-based surveillance. We evaluated the relative concentration efficiency and spatial−temporal distribution in raw wastewater to inform its development as a marker. The results showed significantly higher (p < 0.01) enrichment in raw wastewater solids (mean of 9.2 × 10 7 GC/mL) than in liquid fractions [mean of 2.3 × 10 6 genome copies (GC)/mL]. The relative concentration efficiencies were 28% for nanotrap particles, 23% for Amicon ultrafiltration, 3.6% for pH drop and filtration, 4% for skim milk flocculation, and 0.04% for poly(ethylene glycol) precipitation compared to direct wastewater extraction. DNase pretreatment reduced pBI143 levels by 90.3%, indicating that it is mainly extracellular in raw wastewater. Over 21 days, pBI143 levels remained stable and were consistently a mean of 1.3 log 10 higher than other fecal indicators (Carjivirus, PMMoV, and HF183). In raw wastewater from eight states (n = 16), pBI143 concentrations averaged 2.2 × 10 6 GC/mL (95% confidence interval of 1.7−2.7 × 10 6 ) and pBI143 was detected in all samples. The findings support pBI143's potential as a fecal indicator and normalization marker, though further validation is needed to confirm its specificity to humans.

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A cryptic plasmid is among the most numerous genetic elements in the human gut

Cited by 19 publications

References 146 publications

A pervasive large conjugative plasmid mediates multispecies biofilm formation in the intestinal microbiota increasing resilience to perturbations

A pervasive large conjugative plasmid mediates multispecies biofilm formation in the intestinal microbiota increasing resilience to perturbations

Comprehensive analyses of a large human gut Bacteroidales culture collection reveal species and strain level diversity and evolution

Assessing the Relative Concentration Efficiency and Spatial–Temporal Distribution of Plasmid pBI143 in Raw Wastewater

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