Comprehensive analysis of mobile genetic elements in the gut microbiome reveals phylum-level niche-adaptive gene pools

Mobile genetic elements (MGEs) drive extensive horizontal transfer in the gut microbiome. This transfer could benefit human health by conferring new metabolic capabilities to commensal microbes, or it could threaten human health by spreading antibiotic resistance genes to pathogens. Despite their biological importance and medical relevance, MGEs from the gut microbiome have not been systematically characterized. Here, we present a comprehensive analysis of chromosomal MGEs in the gut microbiome using a method called Split Read Insertion Detection (SRID) that enables the identification of the exact mobilizable unit of MGEs. Leveraging the SRID method, we curated a database of 5600 putative MGEs encompassing seven MGE classes called ImmeDB (Intestinal microbiome mobile element database) (https://immedb.mit.edu/). We observed that many MGEs carry genes that confer an adaptive advantage to the gut environment including gene families involved in antibiotic resistance, bile salt detoxification, mucus degradation, capsular polysaccharide biosynthesis, polysaccharide utilization, and sporulation. We find that antibiotic resistance genes are more likely to be spread by conjugation via integrative conjugative elements or integrative mobilizable elements than transduction via prophages. Additionally, we observed that horizontal transfer of MGEs is extensive within phyla but rare across phyla. Taken together, our findings support a phylum level niche-adaptive gene pools in the gut microbiome. ImmeDB will be a valuable resource for future fundamental and translational studies on the gut microbiome and MGE communities.

[1]  R. Colwell,et al.  SYN‐004 (ribaxamase), an oral beta‐lactamase, mitigates antibiotic‐mediated dysbiosis in a porcine gut microbiome model , 2017, Journal of applied microbiology.

[2]  E. Pamer,et al.  Cooperating Commensals Restore Colonization Resistance to Vancomycin-Resistant Enterococcus faecium. , 2017, Cell host & microbe.

[3]  K. Pollard,et al.  An integrated metagenomics pipeline for strain profiling reveals novel patterns of bacterial transmission and biogeography , 2016, Genome research.

[4]  A. K. Singh,et al.  Mobile genes in the human microbiome are structured from global to individual scales , 2016, Nature.

[5]  M. Sullivan,et al.  Phages rarely encode antibiotic resistance genes: a cautionary tale for virome analyses , 2016, The ISME Journal.

[6]  Nitin Kumar,et al.  Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation , 2016, Nature.

[7]  David S. Wishart,et al.  PHASTER: a better, faster version of the PHAST phage search tool , 2016, Nucleic Acids Res..

[8]  O. Kuipers,et al.  A mobile genetic element profoundly increases heat resistance of bacterial spores , 2016, The ISME Journal.

[9]  Bernhard Y. Renard,et al.  Detecting Horizontal Gene Transfer by Mapping Sequencing Reads Across Species Boundaries , 2016, bioRxiv.

[10]  A. Grossman,et al.  Integrative and Conjugative Elements (ICEs): What They Do and How They Work. , 2015, Annual review of genetics.

[11]  M. Touchon,et al.  Identification of protein secretion systems in bacterial genomes , 2015, Scientific Reports.

[12]  Brian D. Ondov,et al.  Mash: fast genome and metagenome distance estimation using MinHash , 2015, Genome Biology.

[13]  Bernard Henrissat,et al.  Genetic determinants of in vivo fitness and diet responsiveness in multiple human gut Bacteroides , 2015, Science.

[14]  Duy Tin Truong,et al.  MetaPhlAn2 for enhanced metagenomic taxonomic profiling , 2015, Nature Methods.

[15]  Jens V. Stein,et al.  The outer mucus layer hosts a distinct intestinal microbial niche , 2015, Nature Communications.

[16]  Anna-Sophie Fiston-Lavier,et al.  A call for benchmarking transposable element annotation methods , 2015, Mobile DNA.

[17]  Rob Knight,et al.  ConStrains identifies microbial strains in metagenomic datasets , 2015, Nature Biotechnology.

[18]  Jinling Huang,et al.  Horizontal gene transfer: building the web of life , 2015, Nature Reviews Genetics.

[19]  Timothy K Lu,et al.  Programming a Human Commensal Bacterium, Bacteroides thetaiotaomicron, to Sense and Respond to Stimuli in the Murine Gut Microbiota. , 2015, Cell systems.

[20]  Michael A. Fischbach,et al.  A biosynthetic pathway for a prominent class of microbiota-derived bile acids , 2015, Nature chemical biology.

[21]  O. Kohany,et al.  Repbase Update, a database of repetitive elements in eukaryotic genomes , 2015, Mobile DNA.

[22]  Jie Zhang,et al.  Current progress of targetron technology: Development, improvement and application in metabolic engineering , 2015, Biotechnology journal.

[23]  Christophe Dessimoz,et al.  Inferring Horizontal Gene Transfer , 2015, PLoS Comput. Biol..

[24]  S. Lonardi,et al.  CLARK: fast and accurate classification of metagenomic and genomic sequences using discriminative k-mers , 2015, BMC Genomics.

[25]  L. Tailford,et al.  Mucin glycan foraging in the human gut microbiome , 2015, Front. Genet..

[26]  Elhanan Borenstein,et al.  Extensive Strain-Level Copy-Number Variation across Human Gut Microbiome Species , 2015, Cell.

[27]  F. Bushman,et al.  Correlation between intraluminal oxygen gradient and radial partitioning of intestinal microbiota. , 2014, Gastroenterology.

[28]  Chongle Pan,et al.  Sigma: Strain-level inference of genomes from metagenomic analysis for biosurveillance , 2014, Bioinform..

[29]  Molly K. Gibson,et al.  Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology , 2014, The ISME Journal.

[30]  N. Leblond-Bourget,et al.  Conjugative and mobilizable genomic islands in bacteria: evolution and diversity. , 2014, FEMS microbiology reviews.

[31]  Jennifer R. Huddleston Horizontal gene transfer in the human gastrointestinal tract: potential spread of antibiotic resistance genes , 2014 .

[32]  T. Besser,et al.  Modeling the Infection Dynamics of Bacteriophages in Enteric Escherichia coli: Estimating the Contribution of Transduction to Antimicrobial Gene Spread , 2014, Applied and Environmental Microbiology.

[33]  E. Rocha,et al.  Key components of the eight classes of type IV secretion systems involved in bacterial conjugation or protein secretion , 2014, Nucleic acids research.

[34]  Derrick E. Wood,et al.  Kraken: ultrafast metagenomic sequence classification using exact alignments , 2014, Genome Biology.

[35]  P. Siguier,et al.  Bacterial insertion sequences: their genomic impact and diversity , 2014, FEMS microbiology reviews.

[36]  Matthew Fraser,et al.  InterProScan 5: genome-scale protein function classification , 2014, Bioinform..

[37]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[38]  Adam Godzik,et al.  Polysaccharides utilization in human gut bacterium Bacteroides thetaiotaomicron: comparative genomics reconstruction of metabolic and regulatory networks , 2013, BMC Genomics.

[39]  E. Birney,et al.  Pfam: the protein families database , 2013, Nucleic Acids Res..

[40]  Pedro M. Coutinho,et al.  The carbohydrate-active enzymes database (CAZy) in 2013 , 2013, Nucleic Acids Res..

[41]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[42]  E. Rocha,et al.  Evolution of Conjugation and Type IV Secretion Systems , 2012, Molecular biology and evolution.

[43]  Katherine H. Huang,et al.  Structure, Function and Diversity of the Healthy Human Microbiome , 2012, Nature.

[44]  Guangchuang Yu,et al.  clusterProfiler: an R package for comparing biological themes among gene clusters. , 2012, Omics : a journal of integrative biology.

[45]  M. Mergeay,et al.  Towards a more accurate annotation of tyrosine-based site-specific recombinases in bacterial genomes , 2012, Mobile DNA.

[46]  E. Martens,et al.  How glycan metabolism shapes the human gut microbiota , 2012, Nature Reviews Microbiology.

[47]  Liam J. Revell,et al.  phytools: an R package for phylogenetic comparative biology (and other things) , 2012 .

[48]  Otto X. Cordero,et al.  Ecology drives a global network of gene exchange connecting the human microbiome , 2011, Nature.

[49]  Mart Krupovic,et al.  Genomics of Bacterial and Archaeal Viruses: Dynamics within the Prokaryotic Virosphere , 2011, Microbiology and Molecular Reviews.

[50]  Zhen Xu,et al.  ICEberg: a web-based resource for integrative and conjugative elements found in Bacteria , 2011, Nucleic Acids Res..

[51]  A. Lambowitz,et al.  Group II introns: mobile ribozymes that invade DNA. , 2011, Cold Spring Harbor perspectives in biology.

[52]  L. Comstock,et al.  Longitudinal Analysis of the Prevalence, Maintenance, and IgA Response to Species of the Order Bacteroidales in the Human Gut , 2011, Infection and Immunity.

[53]  E. Boyd,et al.  Dichotomy in the evolution of pathogenicity island and bacteriophage encoded integrases from pathogenic Escherichia coli strains. , 2011, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[54]  E. Rocha,et al.  Horizontal Transfer, Not Duplication, Drives the Expansion of Protein Families in Prokaryotes , 2011, PLoS genetics.

[55]  A. Roberts,et al.  Oral biofilms: a reservoir of transferable, bacterial, antimicrobial resistance , 2010, Expert review of anti-infective therapy.

[56]  Stephen D. Bentley,et al.  Twenty-eight divergent polysaccharide loci specifying within- and amongst-strain capsule diversity in three strains of Bacteroides fragilis , 2010, Microbiology.

[57]  Sean R. Eddy,et al.  Hidden Markov model speed heuristic and iterative HMM search procedure , 2010, BMC Bioinformatics.

[58]  Matthew K. Waldor,et al.  Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow , 2010, Nature Reviews Microbiology.

[59]  George M Church,et al.  The human microbiome harbors a diverse reservoir of antibiotic resistance genes , 2010, Virulence.

[60]  Gunnar C. Hansson,et al.  The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host–microbial interactions , 2010, Proceedings of the National Academy of Sciences.

[61]  G. Michel,et al.  Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota , 2010, Nature.

[62]  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 .

[63]  Gipsi Lima-Mendez,et al.  ACLAME: A CLAssification of Mobile genetic Elements, update 2010 , 2009, Nucleic Acids Res..

[64]  Toni Gabaldón,et al.  trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses , 2009, Bioinform..

[65]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[66]  A. Velcich,et al.  The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria , 2008, Proceedings of the National Academy of Sciences.

[67]  Colin Hill,et al.  Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome , 2008, Proceedings of the National Academy of Sciences.

[68]  L. Paoletti,et al.  Role of glycan synthesis in colonization of the mammalian gut by the bacterial symbiont Bacteroides fragilis , 2008, Proceedings of the National Academy of Sciences.

[69]  R. Wilson,et al.  Evolution of Symbiotic Bacteria in the Distal Human Intestine , 2007, PLoS biology.

[70]  D. Fouts Phage_Finder: Automated identification and classification of prophage regions in complete bacterial genome sequences , 2006, Nucleic acids research.

[71]  A. Salyers,et al.  A Bacteroides Conjugative Transposon, CTnERL, Can Transfer a Portion of Itself by Conjugation without Excising from the Chromosome , 2006, Journal of bacteriology.

[72]  Patricia Siguier,et al.  ISfinder: the reference centre for bacterial insertion sequences , 2005, Nucleic Acids Res..

[73]  C. Hill,et al.  The interaction between bacteria and bile. , 2005, FEMS microbiology reviews.

[74]  T. Speed,et al.  GOstat: find statistically overrepresented Gene Ontologies within a group of genes. , 2004, Bioinformatics.

[75]  S. Salzberg,et al.  Versatile and open software for comparing large genomes , 2004, Genome Biology.

[76]  H. Harmsen,et al.  Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov. , 2002, International journal of systematic and evolutionary microbiology.

[77]  A. Salyers,et al.  Characterization of the 13-KilobaseermF Region of the BacteroidesConjugative Transposon CTnDOT , 2001, Applied and Environmental Microbiology.

[78]  J. Hacker,et al.  Ecological fitness, genomic islands and bacterial pathogenicity , 2001, EMBO reports.

[79]  H. Vlamakis,et al.  Evidence for Extensive Resistance Gene Transfer amongBacteroides spp. and among Bacteroides and Other Genera in the Human Colon , 2001, Applied and Environmental Microbiology.

[80]  P. Glaser,et al.  Characterization of transposon Tn1549, conferring VanB-type resistance in Enterococcus spp. , 2000, Microbiology.

[81]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[82]  D. Kasper,et al.  Analysis of a Capsular Polysaccharide Biosynthesis Locus of Bacteroides fragilis , 1999, Infection and Immunity.

[83]  Timothy K Lu,et al.  Programming a Human Commensal Bacterium, Bacteroides thetaiotaomicron, to Sense and Respond to Stimuli in the Murine Gut Microbiota. , 2016, Cell systems.

[84]  Sam P. Brown,et al.  What traits are carried on mobile genetic elements, and why? , 2011, Heredity.

[85]  Sylvia S. Mader Evolution and diversity , 1993 .