Global phylogeography and ancient evolution of the widespread human gut virus crAssphage

Edwards, Robert A.; Vega, Alejandro A.; Norman, Holly M.; Ohaeri, Maria; Levi, Kyle; Dinsdale, Elizabeth A.; Cinek, Ondřej; Aziz, Ramy K.; McNair, Katelyn; Barr, Jeremy J.; Bibby, Kyle; Brouns, Stan J. J.; Cazares, Adrián; Jonge, Patrick A. de; Desnues, Christelle; Díaz‐Muñoz, Samuel L.; Fineran, Peter C.; Kurilshikov, Alexander; Lavigne, Rob; Mazankova, Karla; McCarthy, David Thomas; Nóbrega, Franklin L.; Reyes, Alejandro; Tapia, German; Trefault, Nicole; Tyakht, Alexander V.; Vinuesa, Pablo; Wagemans, Jeroen; Zhernakova, Alexandra; Aarestrup, Frank Møller; Ahmadov, Gunduz; Alassaf, Abeer; Antón, Josefa; Asangba, Abigail E.; Billings, E; Cantu, Adrian; Carlton, Jane M.; Cazares, Daniel; Cho, Gyu-Sung; Condeff, Tess; Cortés, Pilar; Cranfield, Mike; Cuevas, Daniel A.; Iglesia, Rodrigo De la; Decewicz, Przemysław; Doane, Michael P.; Dominy, Nathaniel J.; Dziewit, Łukasz; Elwasila, Bashir Mukhtar; Eren, A. Murat; Franz, Charles M. A. P.; Fu, Jingyuan; García-Aljaro, Cristina; Ghedin, Elodie; Gulino, Kristen M.; Haggerty, John M.; Head, Steven R.; Hendriksen, René S.; Hill, Colin; Hyöty, Heikki; Ilina, Elena; Irwin, Mitchell T.; Jeffries, Thomas C.; Torroella, Juan Jofre; Junge, Randall E.; Kelley, Scott T.; Kowalewski, Martín M.; Kumaresan, Deepak; Leigh, Steven R.; Lisitsyna, Eugenia S.; Llagostera, Montserrat; Maritz, Julia M.; Marr, Linsey C.; McCann, A.; Mirzaei, Mohammadali Khan; Molshanski-Mor, Shahar; Monteiro, Sílvia; Moreira-Grez, Ben; Morris, Megan M.; Mugisha, Lawrence; Muniesa, Maite; Neve, Horst; Nguyen, Nam; Nigro, Olivia D.; Nilsson, Anders S.; O’Connell, Taylor; Odeh, Rasha; Oliver, Andrew; Piuri, Mariana; Prussin, Aaron J.; Qimron, Udi; Zhe-xue, Quan; Rainetová, Petra; Rojas, Adán Andrés Ramírez; Raya, Raúl R.; Rice, Gillian A.O.; Rossi, Alessandro; Santos, Ricardo; Shimashita, John; Stachler, Elyse; Stene, Lars C.; Strain, Ronan; Stumpf, Rebecca M.; Torres, Pedro J.; Twaddle, Alan; Ibekwe, RC; Villagra, Nicolás A.; Wandro, Stephen; White, Bryan A.; Whitely, Andy; Whiteson, Katrine; Wijmenga, Cisca; Zambrano, María Mercedes; Zschach, Henrike; Dutilh, Bas E.

doi:10.1101/527796

Cited by 31 publications

(51 citation statements)

References 71 publications

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“…Interestingly, a subset of infants have a crAss-like phage but their mothers do not. This could be due to waxing/waning amounts of crAss-like phages in mothers, as has been described in adults 14 . If this is the case, the crAsslike phage may have been present in the mother at a level lower than our limit of detection and thus may have been transmitted to the baby.…”

Section: Resultsmentioning

confidence: 69%

“…The in silico discovery of p-crAssphage and recent publication of hundreds of crAss-like phage genomes has highlighted the diversity and global prevalence of these phages in human gut microbiomes. CrAss-like phages have even been found in non-human primates 14 We first characterized p-crAssphage and found no samples collected from infants within 24h of birth met our 1x coverage threshold. P-crAssphage becomes increasingly prevalent as infants age, but does not reach the levels found in mothers by one year of life.…”

Section: Discussionmentioning

confidence: 94%

“…Although p-crAssphage is highly abundant in the adult gut microbiome 5,14 and has been detected in infant gut microbiomes, it is unclear when or how it is acquired. Consistent with previous studies describing low relative abundance or absence of p-crAssphage in the infant gut microbiome 7,22 , we found 0 out of 22 infants have ≥ 1,000 p-crAssphage reads in samples collected within 24 hours of birth (Table S1).…”

Section: Resultsmentioning

confidence: 99%

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Acquisition, transmission and strain diversity of human gut-colonizing crAss-like phages

Siranosian

Tamburini

Sherlock

et al. 2018

Preprint

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CrAss-like phages are double-stranded DNA viruses that are prevalent in human gut microbiomes. Here, we analyze gut metagenomic data from mother-infant pairs and patients undergoing fecal microbiota transplantation to evaluate the patterns of acquisition, transmission and strain diversity of crAss-like phages. We find that crAss-like phages are rarely detected at birth but are increasingly prevalent in the infant microbiome after one month of life. We observe nearly identical genomes in 50% of cases where the same crAss-like clade is detected in both the mother and the infant, suggesting vertical transmission. In cases of putative transmission of prototypical crAssphage (p-crAssphage), we find that a subset of strains present in the mother are detected in the infant, and that strain diversity in infants increases with time. Strain diversity in the p-crAssphage population in mothers is generally low, with a median of 50 variable sites in the 97kb genome. Putative tail fiber proteins are enriched for nonsynonymous strain variation compared to other genes, suggesting a potential evolutionary benefit to maintaining strain diversity in specific genes. Finally, we show that p-crAssphage can be acquired through fecal microbiota transplantation. These results enhance our understanding of the acquisition, individual-level strain diversity, and transmission of crAss-like phages, which have emerged as some of the most successful human-associated microbes.

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Section: Resultsmentioning

confidence: 69%

Section: Discussionmentioning

confidence: 94%

Section: Resultsmentioning

confidence: 99%

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Acquisition, transmission and strain diversity of human gut-colonizing crAss-like phages

Siranosian

Tamburini

Sherlock

et al. 2018

Preprint

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“…2D; Data S11). This suggests that phylogeographic patterns observed for human-associated crAssphages between cities and across continents (7) hold for at least a subset of baboon-associated phages in groups that range within kilometers of each another. Microorganism transmission through social interactions within groups thus not only shapes baboon bacteria community composition (12), but phage community structure and evolution as well.…”

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confidence: 95%

Primate phageomes are structured by superhost phylogeny and environment

Gogarten

Rühlemann

Archie

et al. 2020

Preprint

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The evolutionary origins of human-associated bacteriophage communities are poorly understood.To address this question, we examined fecal phageomes of 23 wild non-human primate taxa, including multiple representatives of all the major primate radiations, and find relatives of the majority of human-associated phages. Primate taxa have distinct phageome compositions that exhibit a clear phylosymbiotic signal, and phage-superhost co-divergence is detected for 44 individual phages. Within species, neighboring social groups harbor evolutionarily and compositionally distinct phageomes, structured by superhost social behavior. However, captive non-human primate phageomes are more similar to humans than their wild counterparts, revealing replacement of wild-associated phages with human-associated ones. Together, our results suggest that potentially labile primate-phage associations persisted across millions of years of evolution, potentially facilitated by transmission between groupmates. One Sentence Summary:Relatives of human-associated phages in wild primates reveal ancient but dynamic superhostphage associations shaped by social transmission. Main Text:Mammals harbor diverse communities of microorganisms, the majority of which are bacteria in the gastrointestinal tract. Gut bacterial communities in turn host diverse bacteriophage communities that influence their structure, function, colonization patterns, and ultimately superhost health (the superhost is the host for bacteria that in turn host the bacteriophages; 1).

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“…The first isolated member of this group, ΦCrAss001, shows podovirus-like morphology and infects the bacterium, Bacteroides intestinalis [12]. In addition to the human gut, crAss-like phages are found in nonhuman primate and termite guts, terrestrial and groundwater sources, and oceanic environments [11, 13–15]. Across metagenomic studies, crAssphage sensu stricto is nearly exclusively associated with the human gut microbiome [8, 11] and has been proposed as a potential biomarker for fecal contamination [16–20].…”

Section: Introductionmentioning

confidence: 99%

Biogeographic study of human gut-associated crAssphage suggests impacts from industrialization and recent expansion

Honap

Sankaranarayanan

Schnorr

et al. 2018

Preprint

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31CrAssphage (cross-assembly phage) is a bacteriophage that was first discovered in 32 human gut metagenomic data. CrAssphage belongs to a diverse family of crAss-like 33 bacteriophages thought to infect gut commensal bacteria belonging to Bacteroides species. 34However, not much is known about the biogeography of crAssphage and whether certain strains 35 are associated with specific human populations. In this study, we screened publicly available 36 human gut metagenomic data from 3,341 samples for the presence of crAssphage sensu stricto 37 (NC_024711.1). We found that crAssphage prevalence is low in traditional, hunter-gatherer 38 populations, such as the Hadza from Tanzania and Matses from Peru, as compared to 39 industrialized, urban populations. Statistical comparisons showed no association of crAssphage 40 prevalence with variables such as age, sex, body mass index, and health status of individuals. 41Phylogenetic analyses show that crAssphage strains reconstructed from the same individual over 42 multiple time-points, cluster together. CrAssphage strains from individuals from the same study 43 population do not always cluster together. Some evidence of clustering is seen at the level of 44 broadly defined geographic regions, however, the relative positions of these clusters within the 45 crAssphage phylogeny are not well-supported. We hypothesize that this lack of strong 46 biogeographic structuring is suggestive of a recent expansion event within crAssphage. Using a 47Bayesian dating approach, we estimate this expansion has occurred within the past 200 years. 48Overall, we determine that crAssphage presence is associated with an industrialized lifestyle. 49The absence of strong biogeographic structuring within global crAssphage strains is likely due to 50 a recent population expansion within this bacteriophage. 51 52

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Global phylogeography and ancient evolution of the widespread human gut virus crAssphage

Cited by 31 publications

References 71 publications

Acquisition, transmission and strain diversity of human gut-colonizing crAss-like phages

Acquisition, transmission and strain diversity of human gut-colonizing crAss-like phages

Primate phageomes are structured by superhost phylogeny and environment

Biogeographic study of human gut-associated crAssphage suggests impacts from industrialization and recent expansion

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