Infant gut bacteriophage strain persistence during the first three years of life

Bacteriophages are key components of gut microbiomes, yet the phage colonization process in the infant gut remains uncertain. Here, we established a large phage sequence database and used strain-resolved analyses to investigate phage succession in infants throughout the first three years of life. Analysis of 819 fecal metagenomes collected from 28 full-term and 24 preterm infants and their mothers revealed that early-life phageome richness increased over time and reached adult-like complexity by age three. Approximately 9% of early phage colonizers, mostly maternally transmitted and infecting Bacteroides, persisted for three years and were more prevalent in full-term than in preterm infants. Although rare, phages with stop codon reassignment were more likely to persist than non-recoded phages and generally displayed an increase in in-frame re-assigned stop codons over three years. Overall, maternal seeding, stop codon reassignment, host CRISPR-Cas locus prevalence, and diverse phage populations contribute to stable viral colonization.

[1]  A. Bernheim,et al.  The highly diverse antiphage defence systems of bacteria , 2023, Nature Reviews Microbiology.

[2]  J. Banfield,et al.  COBRA improves the quality of viral genomes assembled from metagenomes , 2023, bioRxiv.

[3]  A. Bhatt,et al.  Phage-inclusive profiling of human gut microbiomes with Phanta. , 2023, Nature biotechnology.

[4]  Shiraz A. Shah,et al.  Expanding known viral diversity in the healthy infant gut , 2023, Nature Microbiology.

[5]  N. Kyrpides,et al.  You can move, but you can’t hide: identification of mobile genetic elements with geNomad , 2023, bioRxiv.

[6]  M. Rupnik,et al.  Broad host range may be a key to long-term persistence of bacteriophages infecting intestinal Bacteroidaceae species , 2022, Scientific Reports.

[7]  Adair L. Borges,et al.  Experimental validation that human microbiome phages use alternative genetic coding , 2022, Nature Communications.

[8]  Donovan H. Parks,et al.  GTDB-Tk v2: memory friendly classification with the genome taxonomy database , 2022, bioRxiv.

[9]  Junhua Li,et al.  Advances and challenges in cataloging the human gut virome. , 2022, Cell host & microbe.

[10]  C. Hill,et al.  Mutualistic interplay between bacteriophages and bacteria in the human gut , 2022, Nature Reviews Microbiology.

[11]  O. Cooper,et al.  Bacteriophages evolve enhanced persistence to a mucosal surface , 2022, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Adair L. Borges,et al.  Widespread stop-codon recoding in bacteriophages may regulate translation of lytic genes , 2022, Nature Microbiology.

[13]  William A. Walters,et al.  Longitudinal comparison of the developing gut virome in infants and their mothers , 2022, bioRxiv.

[14]  F. Bäckhed,et al.  The developing infant gut microbiome: A strain-level view. , 2022, Cell host & microbe.

[15]  N. Neff,et al.  Robust Variation in Infant Gut Microbiome Assembly Across a Spectrum of Lifestyles , 2022, bioRxiv.

[16]  J. Raes,et al.  The virota and its transkingdom interactions in the healthy infant gut , 2022, Proceedings of the National Academy of Sciences of the United States of America.

[17]  J. Banfield,et al.  Using strain-resolved analysis to identify contamination in metagenomics data , 2022, bioRxiv.

[18]  Nandita R. Garud,et al.  Ecological Stability Emerges at the Level of Strains in the Human Gut Microbiome , 2021, bioRxiv.

[19]  Nandita R. Garud,et al.  Rapid evolution and strain turnover in the infant gut microbiome , 2021, bioRxiv.

[20]  J. Banfield,et al.  Infant gut strain persistence is associated with maternal origin, phylogeny, and traits including surface adhesion and iron acquisition , 2021, Cell reports. Medicine.

[21]  Michael Shamash,et al.  Phages in the infant gut: a framework for virome development during early life , 2021, The ISME Journal.

[22]  Natalia N. Ivanova,et al.  Metagenomic compendium of 189,680 DNA viruses from the human gut microbiome , 2021, Nature Microbiology.

[23]  Michael J. Tisza,et al.  A catalog of tens of thousands of viruses from human metagenomes reveals hidden associations with chronic diseases , 2021, Proceedings of the National Academy of Sciences.

[24]  A. Khosravi,et al.  Bacteriophages and the Immune System. , 2021, Annual review of virology.

[25]  H. Drost,et al.  Sensitive protein alignments at tree-of-life scale using DIAMOND , 2021, Nature Methods.

[26]  F. Bushman,et al.  The human virome: assembly, composition and host interactions , 2021, Nature Reviews Microbiology.

[27]  Shiraz A. Shah,et al.  Streamlining CRISPR spacer-based bacterial host predictions to decipher the viral dark matter , 2021, Nucleic acids research.

[28]  M. Touchon,et al.  Bacteria have numerous distinctive groups of phage–plasmids with conserved phage and variable plasmid gene repertoires , 2021, Nucleic acids research.

[29]  J. Banfield,et al.  inStrain profiles population microdiversity from metagenomic data and sensitively detects shared microbial strains , 2021, Nature Biotechnology.

[30]  N. Kyrpides,et al.  CheckV assesses the quality and completeness of metagenome-assembled viral genomes , 2020, Nature Biotechnology.

[31]  C. Hill,et al.  Long-term persistence of crAss-like phage crAss001 is associated with phase variation in Bacteroides intestinalis , 2020, bioRxiv.

[32]  C. Gray,et al.  crAssphage genomes identified in fecal samples of an adult and infants with evidence of positive genomic selective pressure within tail protein genes. , 2020, Virus research.

[33]  Ayal B. Gussow,et al.  Thousands of previously unknown phages discovered in whole-community human gut metagenomes , 2020, Microbiome.

[34]  E. Elinav,et al.  Phages and their potential to modulate the microbiome and immunity , 2020, Cellular & Molecular Immunology.

[35]  R. Finn,et al.  Massive expansion of human gut bacteriophage diversity , 2020, Cell.

[36]  M. Sullivan,et al.  The Gut Virome Database Reveals Age-Dependent Patterns of Virome Diversity in the Human Gut , 2020, Cell Host & Microbe.

[37]  Z. Taranu,et al.  Challenges of Studying the Human Virome - Relevant Emerging Technologies. , 2020, Trends in microbiology.

[38]  R. Sorek,et al.  Abortive Infection: Bacterial Suicide as an Antiviral Immune Strategy. , 2020, Annual review of virology.

[39]  Ryan D. Crawford,et al.  Phase-variable capsular polysaccharides and lipoproteins modify bacteriophage susceptibility in Bacteroides thetaiotaomicron , 2020, Nature Microbiology.

[40]  F. Bushman,et al.  The stepwise assembly of the neonatal virome is modulated by breastfeeding , 2020, Nature.

[41]  Eugene V. Koonin,et al.  Seeker: Alignment-free identification of bacteriophage genomes by deep learning , 2020, bioRxiv.

[42]  S. Hallam,et al.  Ecology and molecular targets of hypermutation in the global microbiome , 2020, Nature Communications.

[43]  Karthik Anantharaman,et al.  VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences , 2020, Microbiome.

[44]  S. Moineau,et al.  Phage diversity, genomics and phylogeny , 2020, Nature Reviews Microbiology.

[45]  B. Warner,et al.  Discordant transmission of bacteria and viruses from mothers to babies at birth , 2019, Microbiome.

[46]  Narmada Thanki,et al.  CDD/SPARCLE: the conserved domain database in 2020 , 2019, Nucleic Acids Res..

[47]  Donovan H Parks,et al.  GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database , 2019, Bioinform..

[48]  K. Seed,et al.  Dominant Vibrio cholerae phage exhibits lysis inhibition sensitive to disruption by a defensive phage satellite , 2019, bioRxiv.

[49]  J. Hinton,et al.  A window into lysogeny: revealing temperate phage biology with transcriptomics , 2019, bioRxiv.

[50]  Cindy J. Castelle,et al.  The distinction of CPR bacteria from other bacteria based on protein family content , 2019, Nature Communications.

[51]  Steven D. Townsend,et al.  Temporal development of the infant gut microbiome , 2019, Open Biology.

[52]  T. Sutton,et al.  The human gut virome is highly diverse, stable and individual-specific , 2019, bioRxiv.

[53]  Christine L. Sun,et al.  Clades of huge phages from across Earth’s ecosystems , 2019, bioRxiv.

[54]  J. Banfield,et al.  Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms , 2019, Microbiome.

[55]  J. Banfield,et al.  Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms , 2019, Microbiome.

[56]  C. Hill,et al.  Bacteriophages of the Human Gut: The "Known Unknown" of the Microbiome. , 2019, Cell host & microbe.

[57]  Feng Li,et al.  MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies , 2019, PeerJ.

[58]  A. Manges,et al.  The Human Microbiome and Child Growth - First 1000 Days and Beyond. , 2019, Trends in microbiology.

[59]  M. Vaneechoutte,et al.  Interactions between Bacteriophage, Bacteria, and the Mammalian Immune System , 2018, Viruses.

[60]  Natalia N. Ivanova,et al.  Minimum Information about an Uncultivated Virus Genome (MIUViG) , 2018, Nature Biotechnology.

[61]  G. Sherlock,et al.  Acquisition, transmission and strain diversity of human gut-colonizing crAss-like phages , 2018, Nature Communications.

[62]  R. Edwards,et al.  A diversity-generating retroelement encoded by a globally ubiquitous Bacteroides phage , 2018, Microbiome.

[63]  S. Lynch,et al.  The gut microbiome: Relationships with disease and opportunities for therapy , 2018, The Journal of experimental medicine.

[64]  R. Gibbs,et al.  Temporal development of the gut microbiome in early childhood from the TEDDY study , 2018, Nature.

[65]  Oskar Hallatschek,et al.  Evolutionary dynamics of bacteria in the gut microbiome within and across hosts , 2018, bioRxiv.

[66]  L. Debarbieux,et al.  “I will survive”: A tale of bacteriophage-bacteria coevolution in the gut , 2018, Gut microbes.

[67]  Alexander J Probst,et al.  Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy , 2017, Nature Microbiology.

[68]  H. Ochman,et al.  Biological species in the viral world , 2018, Proceedings of the National Academy of Sciences.

[69]  R. Sorek,et al.  Contemporary Phage Biology: From Classic Models to New Insights , 2018, Cell.

[70]  H. Neve,et al.  Rates of Mutation and Recombination in Siphoviridae Phage Genome Evolution over Three Decades , 2018, Molecular biology and evolution.

[71]  Varun Khanna,et al.  The Gut Microbiota Facilitates Drifts in the Genetic Diversity and Infectivity of Bacterial Viruses. , 2017, Cell host & microbe.

[72]  Jeff F. Miller,et al.  Diversity-generating retroelements: natural variation, classification and evolution inferred from a large-scale genomic survey , 2017, Nucleic acids research.

[73]  W. D. de Vos,et al.  The First Microbial Colonizers of the Human Gut: Composition, Activities, and Health Implications of the Infant Gut Microbiota , 2017, Microbiology and Molecular Biology Reviews.

[74]  P. Scanlan Bacteria-Bacteriophage Coevolution in the Human Gut: Implications for Microbial Diversity and Functionality. , 2017, Trends in microbiology.

[75]  J. Banfield,et al.  dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication , 2017, The ISME Journal.

[76]  M. Mirzaei,et al.  Ménage à trois in the human gut: interactions between host, bacteria and phages , 2017, Nature Reviews Microbiology.

[77]  S. Abedon,et al.  Lysogeny in nature: mechanisms, impact and ecology of temperate phages , 2017, The ISME Journal.

[78]  Johannes Söding,et al.  MMseqs software suite for fast and deep clustering and searching of large protein sequence sets , 2016, Bioinform..

[79]  Blake A. Simmons,et al.  MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets , 2016, Bioinform..

[80]  M. Drab,et al.  Mammalian Host-Versus-Phage immune response determines phage fate in vivo , 2015, Scientific Reports.

[81]  R. Feiner,et al.  A new perspective on lysogeny: prophages as active regulatory switches of bacteria , 2015, Nature Reviews Microbiology.

[82]  Yanjiao Zhou,et al.  Early life dynamics of the human gut virome and bacterial microbiome in infants , 2015, Nature Medicine.

[83]  V. Tremaroli,et al.  Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life. , 2015, Cell host & microbe.

[84]  Tommi Vatanen,et al.  The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes. , 2015, Cell host & microbe.

[85]  M. Dominguez-Bello,et al.  The infant microbiome development: mom matters. , 2015, Trends in molecular medicine.

[86]  Anders F. Andersson,et al.  Binning metagenomic contigs by coverage and composition , 2014, Nature Methods.

[87]  Frederic D Bushman,et al.  Rapid evolution of the human gut virome , 2013, Proceedings of the National Academy of Sciences.

[88]  P. Salamon,et al.  Bacteriophage adhering to mucus provide a non–host-derived immunity , 2013, Proceedings of the National Academy of Sciences.

[89]  Brian C. Thomas,et al.  Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization , 2013, Genome research.

[90]  Alison S. Waller,et al.  Genomic variation landscape of the human gut microbiome , 2012, Nature.

[91]  R. Knight,et al.  Diversity, stability and resilience of the human gut microbiota , 2012, Nature.

[92]  J. Kelsen,et al.  The gut microbiota, environment and diseases of modern society , 2012, Gut microbes.

[93]  Siu-Ming Yiu,et al.  IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth , 2012, Bioinform..

[94]  J. Clemente,et al.  Human gut microbiome viewed across age and geography , 2012, Nature.

[95]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[96]  A. Biegert,et al.  HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment , 2011, Nature Methods.

[97]  Sean R. Eddy,et al.  Accelerated Profile HMM Searches , 2011, PLoS Comput. Biol..

[98]  Miriam L. Land,et al.  Trace: Tennessee Research and Creative Exchange Prodigal: Prokaryotic Gene Recognition and Translation Initiation Site Identification Recommended Citation Prodigal: Prokaryotic Gene Recognition and Translation Initiation Site Identification , 2022 .

[99]  Anders F. Andersson,et al.  Virus Population Dynamics and Acquired Virus Resistance in Natural Microbial Communities , 2008, Science.

[100]  R. Barrangou,et al.  CRISPR Provides Acquired Resistance Against Viruses in Prokaryotes , 2007, Science.

[101]  Robert C. Edgar,et al.  PILER-CR: Fast and accurate identification of CRISPR repeats , 2007, BMC Bioinformatics.

[102]  T. Klaenhammer,et al.  Abortive Phage Resistance Mechanism AbiZ Speeds the Lysis Clock To Cause Premature Lysis of Phage-Infected Lactococcus lactis , 2006, Journal of bacteriology.

[103]  R. Simons,et al.  Tropism switching in Bordetella bacteriophage defines a family of diversity-generating retroelements , 2004, Nature.

[104]  R. Simons,et al.  Reverse Transcriptase-Mediated Tropism Switching in Bordetella Bacteriophage , 2002, Science.

[105]  Patricia P. Chan,et al.  tRNAscan-SE: Searching for tRNA Genes in Genomic Sequences. , 2019, Methods in molecular biology.

[106]  E. Dempsey,et al.  Maternal Vertical Transmission Affecting Early-life Microbiota Development. , 2019, Trends in microbiology.

[107]  J. Clemente,et al.  The Long-Term Stability of the Human Gut Microbiota , 2013 .