Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Examining horizontal gene transfer in microbial communities

Abstract

Bacteria acquire novel DNA through horizontal gene transfer (HGT), a process that enables an organism to rapidly adapt to changing environmental conditions, provides a competitive edge and potentially alters its relationship with its host. Although the HGT process is routinely exploited in laboratories, there is a surprising disconnect between what we know from laboratory experiments and what we know from natural environments, such as the human gut microbiome. Owing to a suite of newly available computational algorithms and experimental approaches, we have a broader understanding of the genes that are being transferred and are starting to understand the ecology of HGT in natural microbial communities. This Review focuses on these new technologies, the questions they can address and their limitations. As these methods are applied more broadly, we are beginning to recognize the full extent of HGT possible within a microbiome and the punctuated dynamics of HGT, specifically in response to external stimuli. Furthermore, we are better characterizing the complex selective pressures on mobile genetic elements and the mechanisms by which they interact with the bacterial host genome.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: General routes of horizontal gene transfer within natural communities.
Fig. 2: Metagenomic assessment of the mobilome.
Fig. 3: Reporter constructs for examining recipients of horizontal gene transfer and movement of mobile genetic elements.
Fig. 4: Hi-C applications to identify bacterial host associations of mobile genetic elements.
Fig. 5: PCR-based methods for examining single mobile genes and their genomic contexts.
Fig. 6: Disentangling the processes of horizontal gene transfer and natural selection.

References

  1. 1.

    Hehemann, J.-H. et al. Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464, 908–912 (2010).

    CAS  PubMed  Google Scholar 

  2. 2.

    Summers, A. O. et al. Mercury released from dental ‘silver’ fillings provokes an increase in mercury- and antibiotic-resistant bacteria in oral and intestinal floras of primates. Antimicrob. Agents Chemother. 37, 825–834 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Hemme, C. L. et al. Lateral gene transfer in a heavy metal-contaminated-groundwater microbial community. mBio 7, e02234-15 (2016).

    PubMed  PubMed Central  Google Scholar 

  4. 4.

    Böhm, M.-E., Huptas, C., Krey, V. M. & Scherer, S. Massive horizontal gene transfer, strictly vertical inheritance and ancient duplications differentially shape the evolution of Bacillus cereus enterotoxin operons hbl, cytK and nhe. BMC Evol. Biol. 15, 246 (2015).

    PubMed  PubMed Central  Google Scholar 

  5. 5.

    Ikuma, K. & Gunsch, C. K. Genetic bioaugmentation as an effective method for in situ bioremediation: functionality of catabolic plasmids following conjugal transfers. Bioengineered 3, 236–241 (2012).

    PubMed  PubMed Central  Google Scholar 

  6. 6.

    Nagpal, S., Haque, M. M. & Mande, S. S. Vikodak — a modular framework for inferring functional potential of microbial communities from 16S metagenomic datasets. PLoS ONE 11, e0148347 (2016).

    PubMed  PubMed Central  Google Scholar 

  7. 7.

    Langille, M. G. I. et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31, 814–821 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Loper, J. E. et al. Comparative genomics of plant-associated Pseudomonas spp.: insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genet. 8, e1002784 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Rasko, D. A. et al. The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J. Bacteriol. 190, 6881–6893 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Waldor, M. K. & Mekalanos, J. J. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272, 1910–1914 (1996).

    CAS  PubMed  Google Scholar 

  11. 11.

    Putze, J. et al. Genetic structure and distribution of the colibactin genomic island among members of the family Enterobacteriaceae. Infect. Immun. 77, 4696–4703 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Fischer, S. et al. Indication of horizontal DNA gene transfer by extracellular vesicles. PLoS ONE 11, e0163665 (2016).

    PubMed  PubMed Central  Google Scholar 

  13. 13.

    McDaniel, L. D. et al. High frequency of horizontal gene transfer in the oceans. Science 330, 50 (2010).

    CAS  PubMed  Google Scholar 

  14. 14.

    Aune, T. E. V. & Aachmann, F. L. Methodologies to increase the transformation efficiencies and the range of bacteria that can be transformed. Appl. Microbiol. Biotechnol. 85, 1301–1313 (2010).

    CAS  PubMed  Google Scholar 

  15. 15.

    Sørensen, S. J., Bailey, M., Hansen, L. H., Kroer, N. & Wuertz, S. Studying plasmid horizontal transfer in situ: a critical review. Nat. Rev. Microbiol. 3, 700–710 (2005).

    PubMed  Google Scholar 

  16. 16.

    Hausner, M. & Wuertz, S. High rates of conjugation in bacterial biofilms as determined by quantitative in situ analysis. Appl. Environ. Microbiol. 65, 3710–3713 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Keen, N. T., Tamaki, S., Kobayashi, D. & Trollinger, D. Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria. Gene 70, 191–197 (1988).

    CAS  PubMed  Google Scholar 

  18. 18.

    Eisen, J. A. Horizontal gene transfer among microbial genomes: new insights from complete genome analysis. Curr. Opin. Genet. Dev. 10, 606–611 (2000).

    CAS  PubMed  Google Scholar 

  19. 19.

    Koonin, E. V., Makarova, K. S. & Aravind, L. Horizontal gene transfer in prokaryotes: quantification and classification. Annu. Rev. Microbiol. 55, 709–742 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Bertelli, C., Tilley, K. E. & Brinkman, F. S. L. Microbial genomic island discovery, visualization and analysis. Brief. Bioinform. 20, 1685–1698 (2019).

    CAS  PubMed  Google Scholar 

  21. 21.

    Gao, F. & Zhang, C.-T. GC-Profile: a web-based tool for visualizing and analyzing the variation of GC content in genomic sequences. Nucleic Acids Res. 34, W686–W691 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Baran, R. H. & Ko, H. Detecting horizontally transferred and essential genes based on dinucleotide relative abundance. DNA Res. Int. J. Rapid Publ. Rep. Genes. Genomes 15, 267–276 (2008).

    CAS  Google Scholar 

  23. 23.

    Pal, C., Bengtsson-Palme, J., Kristiansson, E. & Larsson, D. G. J. Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential. BMC Genomics 16, 964 (2015).

    PubMed  PubMed Central  Google Scholar 

  24. 24.

    Di Venanzio, G. et al. Urinary tract colonization is enhanced by a plasmid that regulates uropathogenic Acinetobacter baumannii chromosomal genes. Nat. Commun. 10, 2763 (2019).

    PubMed  PubMed Central  Google Scholar 

  25. 25.

    Landsberger, M. et al. Anti-CRISPR phages cooperate to overcome CRISPR-Cas immunity. Cell 174, 908–916.e12 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Brito, I. L. et al. Mobile genes in the human microbiome are structured from global to individual scales. Nature 535, 435–439 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Ling, A. & Cordaux, R. Insertion sequence inversions mediated by ectopic recombination between terminal inverted repeats. PLoS ONE 5, e15654 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Pop, M. Genome assembly reborn: recent computational challenges. Brief. Bioinform. 10, 354–366 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Zeevi, D. et al. Structural variation in the gut microbiome associates with host health. Nature 568, 43–48 (2019). Structural variants within bacterial genomes, largely due to integrated MGEs, found within the gut microbiota are associated with host phenotypes.

    CAS  PubMed  Google Scholar 

  30. 30.

    Kingsford, C., Schatz, M. C. & Pop, M. Assembly complexity of prokaryotic genomes using short reads. BMC Bioinforma. 11, 21 (2010).

    Google Scholar 

  31. 31.

    Leplae, R., Lima-Mendez, G. & Toussaint, A. ACLAME: a classification of mobile genetic elements, update 2010. Nucleic Acids Res. 38, D57–D61 (2010).

    CAS  PubMed  Google Scholar 

  32. 32.

    Jiang, X., Hall, A. B., Xavier, R. J. & Alm, E. J. Comprehensive analysis of chromosomal mobile genetic elements in the gut microbiome reveals phylum-level niche-adaptive gene pools. PLoS ONE 14, e0223680 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Carattoli, A. et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob. Agents Chemother. 58, 3895–3903 (2014).

    PubMed  PubMed Central  Google Scholar 

  34. 34.

    Roux, S., Enault, F., Hurwitz, B. L. & Sullivan, M. B. VirSorter: mining viral signal from microbial genomic data. PeerJ 3, e985 (2015).

    PubMed  PubMed Central  Google Scholar 

  35. 35.

    Wagner, A., Lewis, C. & Bichsel, M. A survey of bacterial insertion sequences using IScan. Nucleic Acids Res. 35, 5284–5293 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Rozov, R. et al. Recycler: an algorithm for detecting plasmids from de novo assembly graphs. Bioinformatics 33, 475–482 (2017).

    CAS  PubMed  Google Scholar 

  37. 37.

    Krawczyk, P. S., Lipinski, L. & Dziembowski, A. PlasFlow: predicting plasmid sequences in metagenomic data using genome signatures. Nucleic Acids Res. 46, e35 (2018).

    PubMed  PubMed Central  Google Scholar 

  38. 38.

    Arredondo-Alonso, S., Willems, R. J., van Schaik, W. & Schürch, A. C. On the (im)possibility of reconstructing plasmids from whole-genome short-read sequencing data. Microb. Genomics 3, e000128 (2017).

    Google Scholar 

  39. 39.

    Jørgensen, T. S., Xu, Z., Hansen, M. A., Sørensen, S. J. & Hansen, L. H. Hundreds of circular novel plasmids and DNA elements identified in a rat cecum metamobilome. PLoS ONE 9, e87924 (2014).

    PubMed  PubMed Central  Google Scholar 

  40. 40.

    Li, J. et al. An integrated catalog of reference genes in the human gut microbiome. Nat. Biotechnol. 32, 834–841 (2014).

    CAS  PubMed  Google Scholar 

  41. 41.

    Gregory, A. C. et al. Marine DNA viral macro- and microdiversity from pole to pole. Cell 177, 1109–1123.e14 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Bin Jang, H. et al. Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks. Nat. Biotechnol. 37, 632–639 (2019).

    Google Scholar 

  43. 43.

    Song, W., Wemheuer, B., Zhang, S., Steensen, K. & Thomas, T. MetaCHIP: community-level horizontal gene transfer identification through the combination of best-match and phylogenetic approaches. Microbiome 7, 36 (2019).

    PubMed  PubMed Central  Google Scholar 

  44. 44.

    Franzosa, E. A. et al. Identifying personal microbiomes using metagenomic codes. Proc. Natl Acad. Sci. USA 112, E2930–E2938 (2015).

    CAS  PubMed  Google Scholar 

  45. 45.

    Brito, I. L. et al. Transmission of human-associated microbiota along family and social networks. Nat. Microbiol. 4, 964–971 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Seiler, E., Trappe, K. & Renard, B. Y. Where did you come from, where did you go: refining metagenomic analysis tools for horizontal gene transfer characterisation. PLOS Comput. Biol. 15, e1007208 (2019).

    PubMed  PubMed Central  Google Scholar 

  47. 47.

    Sieber, C. M. K. et al. Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy. Nat. Microbiol. 3, 836–843 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Wu, Y.-W., Simmons, B. A. & Singer, S. W. MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics 32, 605–607 (2016).

    CAS  PubMed  Google Scholar 

  49. 49.

    Alneberg, J. et al. Binning metagenomic contigs by coverage and composition. Nat. Methods 11, 1144–1146 (2014).

    CAS  PubMed  Google Scholar 

  50. 50.

    Sharon, I. et al. Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization. Genome Res. 23, 111–120 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Brooks, B. et al. Microbes in the neonatal intensive care unit resemble those found in the gut of premature infants. Microbiome 2, 1 (2014).

    PubMed  PubMed Central  Google Scholar 

  52. 52.

    Cleary, B. et al. Detection of low-abundance bacterial strains in metagenomic datasets by eigengenome partitioning. Nat. Biotechnol. 33, 1053–1060 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Lim, E. S. et al. Early life dynamics of the human gut virome and bacterial microbiome in infants. Nat. Med. 21, 1228–1234 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Duerkop, B. A. et al. Murine colitis reveals a disease-associated bacteriophage community. Nat. Microbiol. 3, 1023–1031 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. 55.

    Norman, J. M. et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160, 447–460 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Reyes, A. et al. Gut DNA viromes of Malawian twins discordant for severe acute malnutrition. Proc. Natl Acad. Sci. USA 112, 11941–11946 (2015).

    CAS  PubMed  Google Scholar 

  57. 57.

    Thurber, R. V., Haynes, M., Breitbart, M., Wegley, L. & Rohwer, F. Laboratory procedures to generate viral metagenomes. Nat. Protoc. 4, 470–483 (2009).

    CAS  PubMed  Google Scholar 

  58. 58.

    Roux, S. et al. Minimum information about an uncultivated virus genome (MIUViG). Nat. Biotechnol. 37, 29–37 (2019). This article provides a coherent outline for evaluating metagenomic assembled phage genomes.

    CAS  PubMed  Google Scholar 

  59. 59.

    d’Humières, C. et al. A simple, reproducible and cost-effective procedure to analyse gut phageome: from phage isolation to bioinformatic approach. Sci. Rep. 9, 11331 (2019).

    PubMed  PubMed Central  Google Scholar 

  60. 60.

    Castro-Mejía, J. L. et al. Optimizing protocols for extraction of bacteriophages prior to metagenomic analyses of phage communities in the human gut. Microbiome 3, 64 (2015).

    PubMed  PubMed Central  Google Scholar 

  61. 61.

    Kleiner, M., Hooper, L. V. & Duerkop, B. A. Evaluation of methods to purify virus-like particles for metagenomic sequencing of intestinal viromes. BMC Genomics 16, 7 (2015).

    PubMed  PubMed Central  Google Scholar 

  62. 62.

    Schulz, F. et al. Giant viruses with an expanded complement of translation system components. Science 356, 82–85 (2017).

    CAS  PubMed  Google Scholar 

  63. 63.

    Dutilh, B. E. et al. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat. Commun. 5, 4498 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. 64.

    Devoto, A. E. et al. Megaphages infect Prevotella and variants are widespread in gut microbiomes. Nat. Microbiol. 4, 693–700 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  65. 65.

    Tamminen, M., Virta, M., Fani, R. & Fondi, M. Large-scale analysis of plasmid relationships through gene-sharing networks. Mol. Biol. Evol. 29, 1225–1240 (2012).

    CAS  PubMed  Google Scholar 

  66. 66.

    Brown Kav, A. et al. Insights into the bovine rumen plasmidome. Proc. Natl Acad. Sci. USA 109, 5452–5457 (2012).

    PubMed  Google Scholar 

  67. 67.

    Li, A.-D., Li, L.-G. & Zhang, T. Exploring antibiotic resistance genes and metal resistance genes in plasmid metagenomes from wastewater treatment plants. Front. Microbiol. 6, 1025 (2015).

    PubMed  PubMed Central  Google Scholar 

  68. 68.

    Jones, B. V. & Marchesi, J. R. Transposon-aided capture (TRACA) of plasmids resident in the human gut mobile metagenome. Nat. Methods 4, 55–61 (2007).

    CAS  PubMed  Google Scholar 

  69. 69.

    Delaney, S., Murphy, R. & Walsh, F. A comparison of methods for the extraction of plasmids capable of conferring antibiotic resistance in a human pathogen from complex broiler cecal samples. Front. Microbiol. 9, 1731 (2018).

    PubMed  PubMed Central  Google Scholar 

  70. 70.

    Hidalgo-Cantabrana, C., Sanozky-Dawes, R. & Barrangou, R. Insights into the human virome using CRISPR spacers from microbiomes. Viruses 10, 479 (2018).

    PubMed Central  Google Scholar 

  71. 71.

    Paez-Espino, D. et al. Uncovering Earth’s virome. Nature 536, 425–430 (2016).

    CAS  PubMed  Google Scholar 

  72. 72.

    Andersson, A. F. & Banfield, J. F. Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320, 1047–1050 (2008).

    CAS  PubMed  Google Scholar 

  73. 73.

    Stern, A., Mick, E., Tirosh, I., Sagy, O. & Sorek, R. CRISPR targeting reveals a reservoir of common phages associated with the human gut microbiome. Genome Res. 22, 1985–1994 (2012). This article shows an examination of CRISPR spacers across a population can be used to identify prevalent and individual-specific MGEs.

    CAS  PubMed  PubMed Central  Google Scholar 

  74. 74.

    Minot, S. et al. Rapid evolution of the human gut virome. Proc. Natl Acad. Sci. USA 110, 12450–12455 (2013).

    CAS  PubMed  Google Scholar 

  75. 75.

    Pärnänen, K. et al. Evaluating the mobility potential of antibiotic resistance genes in environmental resistomes without metagenomics. Sci. Rep. 6, 35790 (2016).

    PubMed  PubMed Central  Google Scholar 

  76. 76.

    Shintani, M., Sanchez, Z. K. & Kimbara, K. Genomics of microbial plasmids: classification and identification based on replication and transfer systems and host taxonomy. Front. Microbiol. 6, 242 (2015).

    PubMed  PubMed Central  Google Scholar 

  77. 77.

    Kuleshov, V. et al. Synthetic long-read sequencing reveals intraspecies diversity in the human microbiome. Nat. Biotechnol. 34, 64–69 (2016).

    CAS  PubMed  Google Scholar 

  78. 78.

    Zlitni, S. et al. Strain-resolved microbiome sequencing reveals mobile elements that drive bacterial competition on a clinical timescale. Genome Med. 12, 50 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. 79.

    Suzuki, Y. et al. Long-read metagenomic exploration of extrachromosomal mobile genetic elements in the human gut. Microbiome 7, 119 (2019).

    PubMed  PubMed Central  Google Scholar 

  80. 80.

    Amarasinghe, S. L. et al. Opportunities and challenges in long-read sequencing data analysis. Genome Biol. 21, 30 (2020).

    PubMed  PubMed Central  Google Scholar 

  81. 81.

    Moss, E. L., Maghini, D. G. & Bhatt, A. S. Complete, closed bacterial genomes from microbiomes using nanopore sequencing. Nat. Biotechnol. 38, 701–707 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. 82.

    Beaulaurier, J., Schadt, E. E. & Fang, G. Deciphering bacterial epigenomes using modern sequencing technologies. Nat. Rev. Genet. 20, 157–172 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. 83.

    Rand, A. C. et al. Mapping DNA methylation with high throughput nanopore sequencing. Nat. Methods 14, 411–413 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. 84.

    Somerville, V. et al. Long-read based de novo assembly of low-complexity metagenome samples results in finished genomes and reveals insights into strain diversity and an active phage system. BMC Microbiol. 19, 143 (2019).

    PubMed  PubMed Central  Google Scholar 

  85. 85.

    Cohen, N. R. et al. A role for the bacterial GATC methylome in antibiotic stress survival. Nat. Genet. 48, 581–586 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. 86.

    Leonard, M. T. et al. The methylome of the gut microbiome: disparate Dam methylation patterns in intestinal Bacteroides dorei. Front. Microbiol. 5, 361 (2014).

    PubMed  PubMed Central  Google Scholar 

  87. 87.

    Smillie, C. S. et al. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480, 241–244 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. 88.

    Zhao, S. et al. Adaptive evolution within gut microbiomes of healthy people. Cell Host Microbe 25, 656–667.e8 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. 89.

    Bonham, K. S., Wolfe, B. E. & Dutton, R. J. Extensive horizontal gene transfer in cheese-associated bacteria. eLife 6, e22144 (2017).

    PubMed  PubMed Central  Google Scholar 

  90. 90.

    Forster, S. C. et al. A human gut bacterial genome and culture collection for improved metagenomic analyses. Nat. Biotechnol. 37, 186–192 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. 91.

    Poyet, M. et al. A library of human gut bacterial isolates paired with longitudinal multiomics data enables mechanistic microbiome research. Nat. Med. 25, 1442–1452 (2019).

    CAS  PubMed  Google Scholar 

  92. 92.

    De Gelder, L., Ponciano, J. M., Joyce, P. & Top, E. M. Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship. Microbiol. Read. Engl. 153, 452–463 (2007).

    Google Scholar 

  93. 93.

    del Campo, I. et al. Determination of conjugation rates on solid surfaces. Plasmid 67, 174–182 (2012).

    PubMed  Google Scholar 

  94. 94.

    Arevalo, P., VanInsberghe, D., Elsherbini, J., Gore, J. & Polz, M. F. A reverse ecology approach based on a biological definition of microbial populations. Cell 178, 820–834.e14 (2019).

    CAS  PubMed  Google Scholar 

  95. 95.

    Durrant, M. G., Li, M. M., Siranosian, B. & Bhatt, A. S. A Bioinformatic analysis of integrative mobile genetic elements highlights their role in bacterial adaptation. Cell Host Microbe 27, 140–153 (2020).

    CAS  PubMed  Google Scholar 

  96. 96.

    Daubin, V., Lerat, E. & Perrière, G. The source of laterally transferred genes in bacterial genomes. Genome Biol. 4, R57 (2003).

    PubMed  PubMed Central  Google Scholar 

  97. 97.

    Stepanauskas, R. et al. Improved genome recovery and integrated cell-size analyses of individual uncultured microbial cells and viral particles. Nat. Commun. 8, 84 (2017).

    PubMed  PubMed Central  Google Scholar 

  98. 98.

    de Bourcy, C. F. A. et al. A quantitative comparison of single-cell whole genome amplification methods. PLoS ONE 9, e105585 (2014).

    PubMed  PubMed Central  Google Scholar 

  99. 99.

    Xu, L., Brito, I. L., Alm, E. J. & Blainey, P. C. Virtual microfluidics for digital quantification and single-cell sequencing. Nat. Methods 13, 759–762 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. 100.

    Labonté, J. M. et al. Single cell genomics indicates horizontal gene transfer and viral infections in a deep subsurface Firmicutes population. Front. Microbiol. 6, 349 (2015).

    PubMed  PubMed Central  Google Scholar 

  101. 101.

    Licht, T. R., Christensen, B. B., Krogfelt, K. A. & Molin, S. Plasmid transfer in the animal intestine and other dynamic bacterial populations: the role of community structure and environment. Microbiol. Read. Engl. 145, 2615–2622 (1999).

    CAS  Google Scholar 

  102. 102.

    Haagensen, J. A. J., Hansen, S. K., Johansen, T. & Molin, S. In situ detection of horizontal transfer of mobile genetic elements. FEMS Microbiol. Ecol. 42, 261–268 (2002).

    CAS  PubMed  Google Scholar 

  103. 103.

    Stalder, T. & Top, E. Plasmid transfer in biofilms: a perspective on limitations and opportunities. NPJ Biofilms Microbiomes 2, 16022 (2016).

    PubMed  PubMed Central  Google Scholar 

  104. 104.

    Diard, M. et al. Inflammation boosts bacteriophage transfer between Salmonella spp. Science 355, 1211–1215 (2017). Barcoded phages are used to monitor transfer between two Salmonella phages transduced as a result of inflammation.

    CAS  PubMed  Google Scholar 

  105. 105.

    Klümper, U. et al. Broad host range plasmids can invade an unexpectedly diverse fraction of a soil bacterial community. ISME J. 9, 934–945 (2015). Using fluorescence-activated cell sorting, the authors track a GFP-tagged plasmid between species within a soil community.

    PubMed  Google Scholar 

  106. 106.

    de Jonge, P. A. et al. Adsorption sequencing as a rapid method to link environmental bacteriophages to hosts. iScience 23, 101439 (2020).

    PubMed  PubMed Central  Google Scholar 

  107. 107.

    Deng, L. et al. Viral tagging reveals discrete populations in Synechococcus viral genome sequence space. Nature 513, 242–245 (2014).

    CAS  PubMed  Google Scholar 

  108. 108.

    Deng, L. et al. Contrasting life strategies of viruses that infect photo- and heterotrophic bacteria, as revealed by viral tagging. mBio 3, e00373 (2012).

    PubMed  PubMed Central  Google Scholar 

  109. 109.

    Džunková, M. et al. Defining the human gut host-phage network through single-cell viral tagging. Nat. Microbiol. 4, 2192–2203 (2019). This article presents a community-level variation on viral tagging, in which phages are isolated from a gut microbiome sample, fluorescently labelled and restored with the gut bacteria to allow sorting and single-cell sequencing, thereby linking phages with their host genomes.

    PubMed  Google Scholar 

  110. 110.

    Munck, C., Sheth, R. U., Freedberg, D. E. & Wang, H. H. Real-time capture of horizontal gene transfers from gut microbiota by engineered CRISPR-Cas acquisition. Preprint at bioRxiv https://doi.org/10.1101/492751 (2018).

    Article  Google Scholar 

  111. 111.

    Burton, J. N., Liachko, I., Dunham, M. J. & Shendure, J. Species-level deconvolution of metagenome assemblies with Hi-C-based contact probability maps. G3 4, 1339–1346 (2014).

    PubMed  Google Scholar 

  112. 112.

    Beitel, C. W. et al. Strain- and plasmid-level deconvolution of a synthetic metagenome by sequencing proximity ligation products. PeerJ 2, e415 (2014).

    PubMed  PubMed Central  Google Scholar 

  113. 113.

    Bickhart, D. M. et al. Assignment of virus and antimicrobial resistance genes to microbial hosts in a complex microbial community by combined long-read assembly and proximity ligation. Genome Biol. 20, 153 (2019).

    PubMed  PubMed Central  Google Scholar 

  114. 114.

    Stalder, T., Press, M. O., Sullivan, S., Liachko, I. & Top, E. M. Linking the resistome and plasmidome to the microbiome. ISME J. 13, 2437–2446 (2019).

    PubMed  PubMed Central  Google Scholar 

  115. 115.

    Press, M. O. et al. Hi-C deconvolution of a human gut microbiome yields high-quality draft genomes and reveals plasmid-genome interactions. Preprint at bioRxiv https://doi.org/10.1101/198713 (2017).

    Article  Google Scholar 

  116. 116.

    Yaffe, E. & Relman, D. A. Tracking microbial evolution in the human gut using Hi-C reveals extensive horizontal gene transfer, persistence and adaptation. Nat. Microbiol. https://doi.org/10.1038/s41564-019-0625-0 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  117. 117.

    Kent, A. G., Vill, A. C., Shi, Q., Satlin, M. J. & Brito, I. L. Widespread transfer of mobile antibiotic resistance genes within individual gut microbiomes revealed through bacterial Hi-C. Nat. Commun. 11, 4379 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  118. 118.

    Ignacio-Espinoza, J. C. et al. Ribosome-linked mRNA-rRNA chimeras reveal active novel virus host associations. Preprint at bioRxiv https://doi.org/10.1101/2020.10.30.332502 (2020).

    Article  Google Scholar 

  119. 119.

    Spencer, S. J. et al. Massively parallel sequencing of single cells by epicPCR links functional genes with phylogenetic markers. ISME J. 10, 427–436 (2016).

    CAS  PubMed  Google Scholar 

  120. 120.

    Hultman, J. et al. Host range of antibiotic resistance genes in wastewater treatment plant influent and effluent. FEMS Microbiol. Ecol. 94, fiy038 (2018).

    PubMed Central  Google Scholar 

  121. 121.

    Diebold, P. J., New, F. N., Hovan, M., Satlin, M. J. & Brito, I. L. Linking plasmid-based beta-lactamases to their bacterial hosts using single-cell fusion PCR. Preprint at bioRxiv https://doi.org/10.1101/2021.01.22.427834 (2021). The authors develop an easy-to-use, versatile platform for linking specific plasmid genes to taxonomic markers.

    Article  Google Scholar 

  122. 122.

    Ronda, C., Chen, S. P., Cabral, V., Yaung, S. J. & Wang, H. H. Metagenomic engineering of the mammalian gut microbiome in situ. Nat. Methods 16, 167–170 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  123. 123.

    Langelier, C. et al. Microbiome and antimicrobial resistance gene dynamics in international travelers. Emerg. Infect. Dis. 25, 1380–1383 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  124. 124.

    Zwanzig, M. et al. Mobile compensatory mutations promote plasmid survival. mSystems https://doi.org/10.1128/mSystems.00186-18 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  125. 125.

    Kintses, B. et al. Phylogenetic barriers to horizontal transfer of antimicrobial peptide resistance genes in the human gut microbiota. Nat. Microbiol. 4, 447–458 (2019).

    CAS  PubMed  Google Scholar 

  126. 126.

    Rabinovich, L., Sigal, N., Borovok, I., Nir-Paz, R. & Herskovits, A. A. Prophage excision activates Listeria competence genes that promote phagosomal escape and virulence. Cell 150, 792–802 (2012).

    CAS  PubMed  Google Scholar 

  127. 127.

    Faure, G. et al. CRISPR-Cas in mobile genetic elements: counter-defence and beyond. Nat. Rev. Microbiol. 17, 513–525 (2019).

    CAS  PubMed  Google Scholar 

  128. 128.

    Truong, D. T., Tett, A., Pasolli, E., Huttenhower, C. & Segata, N. Microbial strain-level population structure and genetic diversity from metagenomes. Genome Res. 27, 626–638 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  129. 129.

    Wang, R. et al. The global distribution and spread of the mobilized colistin resistance gene mcr-1. Nat. Commun. 9, 1179 (2018).

    PubMed  PubMed Central  Google Scholar 

  130. 130.

    Fulsundar, S. et al. Gene transfer potential of outer membrane vesicles of Acinetobacter baylyi and effects of stress on vesiculation. Appl. Environ. Microbiol. 80, 3469–3483 (2014).

    PubMed  PubMed Central  Google Scholar 

  131. 131.

    Tran, F. & Boedicker, J. Q. Genetic cargo and bacterial species set the rate of vesicle-mediated horizontal gene transfer. Sci. Rep. 7, 8813 (2017).

    PubMed  PubMed Central  Google Scholar 

  132. 132.

    Domingues, S. & Nielsen, K. M. Membrane vesicles and horizontal gene transfer in prokaryotes. Curr. Opin. Microbiol. 38, 16–21 (2017).

    CAS  PubMed  Google Scholar 

  133. 133.

    Li, J. et al. Antibiotic treatment drives the diversification of the human gut resistome. Genomics Proteom. Bioinforma. 17, 39–51 (2019).

    CAS  Google Scholar 

  134. 134.

    Baltrus, D. A. Exploring the costs of horizontal gene transfer. Trends Ecol. Evol. 28, 489–495 (2013).

    PubMed  Google Scholar 

  135. 135.

    van Houte, S. et al. The diversity-generating benefits of a prokaryotic adaptive immune system. Nature 532, 385–388 (2016).

    PubMed  PubMed Central  Google Scholar 

  136. 136.

    Chaikeeratisak, V. et al. Assembly of a nucleus-like structure during viral replication in bacteria. Science 355, 194–197 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  137. 137.

    Trappe, K., Marschall, T. & Renard, B. Y. Detecting horizontal gene transfer by mapping sequencing reads across species boundaries. Bioinforma. Oxf. Engl. 32, i595–i604 (2016).

    CAS  Google Scholar 

  138. 138.

    Durrant, M. G., Li, M. M., Siranosian, B. A., Montgomery, S. B. & Bhatt, A. S. A bioinformatic analysis of integrative mobile genetic elements highlights their role in bacterial adaptation. Cell Host Microbe 28, 767 (2020).

    CAS  PubMed  Google Scholar 

  139. 139.

    Sentchilo, V. et al. Community-wide plasmid gene mobilization and selection. ISME J. 7, 1173–1186 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  140. 140.

    Beaulaurier, J. et al. Metagenomic binning and association of plasmids with bacterial host genomes using DNA methylation. Nat. Biotechnol. 36, 61–69 (2018).

    CAS  PubMed  Google Scholar 

  141. 141.

    Marbouty, M., Baudry, L., Cournac, A. & Koszul, R. Scaffolding bacterial genomes and probing host-virus interactions in gut microbiome by proximity ligation (chromosome capture) assay. Sci. Adv. 3, e1602105 (2017).

    PubMed  PubMed Central  Google Scholar 

  142. 142.

    Marbouty, M. et al. Metagenomic chromosome conformation capture (meta3C) unveils the diversity of chromosome organization in microorganisms. eLife 3, e03318 (2014).

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The author is a Packard Fellow of Science and Engineering, a Pew Biomedical Scholar and a Sloan Foundation Research Fellow. This research was funded by the Sloan Foundation Microbes in the Built Environment programme (2018-11009), the US National Sciences Foundation (ABI 1661338, EAGER 1650122), the US National Institutes of Health (1DP2HL141007), the US Department of Agriculture (BRAG:2017-03796) and the Bill & Melinda Gates Grand Challenges Program (OPP1161064). The author thanks members of the Brito laboratory for comments on the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ilana Lauren Brito.

Ethics declarations

Competing interests

The author declares no competing interests.

Additional information

Peer review information

Nature Reviews Microbiology thanks H. Wang and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Glossary

Mobile genetic elements

(MGEs). Units of DNA that can be transferred within a genome or between genomes.

Speciation

The evolution of a clade of organisms that are genetically and often ecologically distinct from neighbouring clades.

Genotoxins

Chemicals that can elicit changes in the DNA, including but not limited to strand breakage, deamination and cross-linking, which can lead to mutation.

Biofilms

The organization of unicellular organisms, often multiple species, into an adherent, cohesive mat, often involving extracellular polymeric substances and distinct changes in function compared with planktonic cells.

k-mer composition

A tally of the unique DNA fragments k base pairs long in a genome or a dataset of sequencing reads or contigs.

Prophages

Phage genomes that are integrated and replicated along within the genome of their host. These are either phages in their lysogenic phase or they are inactive (mutated so they no longer can enter a lytic phase).

Lytic phages

Phages that reproduce within a cell and subsequently lyse the cell to release the virions.

Culturomics

The study of bacterial cell culture using high-throughput methods, usually with the goal of isolating diverse organisms from complex microbial communities.

Protospacers

Small DNA fragments found within CRISPR arrays that are derived from invading mobile genetic DNA (plasmids or phages).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Brito, I.L. Examining horizontal gene transfer in microbial communities. Nat Rev Microbiol 19, 442–453 (2021). https://doi.org/10.1038/s41579-021-00534-7

Download citation

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing