Prophage-encoded antibiotic resistance genes are enriched in human-impacted environments.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
27 Sep 2024
27 Sep 2024
Historique:
received:
24
10
2023
accepted:
07
09
2024
medline:
28
9
2024
pubmed:
28
9
2024
entrez:
27
9
2024
Statut:
epublish
Résumé
The spread of antibiotic resistance genes (ARGs) poses a substantial threat to human health. Phage-mediated transduction could exacerbate ARG transmission. While several case studies exist, it is yet unclear to what extent phages encode and mobilize ARGs at the global scale and whether human impacts play a role in this across different habitats. Here, we combine 38,605 bacterial genomes, 1432 metagenomes, and 1186 metatranscriptomes across 12 contrasting habitats to explore the distribution of prophages and their cargo ARGs in natural and human-impacted environments. Worldwide, we observe a significant increase in the abundance, diversity, and activity of prophage-encoded ARGs in human-impacted habitats linked with relatively higher risk of past antibiotic exposure. This effect was driven by phage-encoded cargo ARGs that could be mobilized to provide increased resistance in heterologous E. coli host for a subset of analyzed strains. Our findings suggest that human activities have altered bacteria-phage interactions, enriching ARGs in prophages and making ARGs more mobile across habitats globally.
Identifiants
pubmed: 39333115
doi: 10.1038/s41467-024-52450-y
pii: 10.1038/s41467-024-52450-y
doi:
Substances chimiques
Anti-Bacterial Agents
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
8315Informations de copyright
© 2024. The Author(s).
Références
Chevallereau, A., Pons, B. J., van Houte, S. & Westra, E. R. Interactions between bacterial and phage communities in natural environments. Nat. Rev. Microbiol. 20, 49–62 (2022).
pubmed: 34373631
doi: 10.1038/s41579-021-00602-y
Schulz, F. et al. Giant virus diversity and host interactions through global metagenomics. Nature 578, 432–436 (2020).
pubmed: 31968354
pmcid: 7162819
doi: 10.1038/s41586-020-1957-x
Jansson, J. K. & Wu, R. Soil viral diversity, ecology, and climate change. Nat. Rev. Microbiol. 21, 296–311 (2022).
pubmed: 36352025
doi: 10.1038/s41579-022-00811-z
Yi, Y. et al. A systematic analysis of marine lysogens and proviruses. Nat. Commun. 14, 6013 (2023).
pubmed: 37758717
pmcid: 10533544
doi: 10.1038/s41467-023-41699-4
Tang, X. et al. Lysogenic bacteriophages encoding arsenic resistance determinants promote bacterial community adaptation to arsenic toxicity. ISME J. 17, 1104–1115 (2023).
pubmed: 37161002
pmcid: 10284793
doi: 10.1038/s41396-023-01425-w
Wendling, C. C., Refardt, D. & Hall, A. R. Fitness benefits to bacteria of carrying prophages and prophage-encoded antibiotic-resistance genes peak in different environments. Evolution 75, 515–528 (2021).
pubmed: 33347602
pmcid: 7986917
doi: 10.1111/evo.14153
Howard-Varona, C., Hargreaves, K. R., Abedon, S. T. & Sullivan, M. B. Lysogeny in nature: mechanisms, impact, and ecology of temperate phages. ISME J. 11, 1511–1520 (2017).
pubmed: 28291233
pmcid: 5520141
doi: 10.1038/ismej.2017.16
Huang, D. et al. Adaptive strategies and ecological roles of phages in habitats under physicochemical stress. Trends Microbiol. 32, 902–916 (2024).
pubmed: 38433027
doi: 10.1016/j.tim.2024.02.002
Tang, X. et al. Bacteriophages from arsenic-resistant bacteria transduced resistance genes, which changed arsenic speciation and increased soil toxicity. Environ. Sci. Technol. Lett. 6, 675–680 (2019).
doi: 10.1021/acs.estlett.9b00600
Haak, B. W. & Wiersinga, W. J. Uncovering hidden antimicrobial resistance patterns within the hospital microbiome. Nat. Med. 26, 826–828 (2020).
pubmed: 32514170
doi: 10.1038/s41591-020-0919-z
Wang, M. et al. Role of enterotoxigenic Escherichia coli prophage in spreading antibiotic resistance in a porcine-derived environment. Environ. Microbiol. 22, 4974–4984 (2020).
pubmed: 32419209
doi: 10.1111/1462-2920.15084
Lucidi, M. et al. Phage-mediated colistin resistance in Acinetobacter baumannii. Drug Resist. Update 73, 101061 (2024).
doi: 10.1016/j.drup.2024.101061
Kauffman, K. M. et al. Resolving the structure of phage–bacteria interactions in the context of natural diversity. Nat. Commun. 13, 372 (2022).
pubmed: 35042853
pmcid: 8766483
doi: 10.1038/s41467-021-27583-z
Piel, D. et al. Phage–host coevolution in natural populations. Nat. Microbiol. 7, 1075–1086 (2022).
pubmed: 35760840
doi: 10.1038/s41564-022-01157-1
Wright, R. C. T., Friman, V.-P., Smith, M. C. M. & Brockhurst, M. A. Cross-resistance is modular in bacteria–phage interactions. PLOS Biol. 16, e2006057 (2018).
pubmed: 30281587
pmcid: 6188897
doi: 10.1371/journal.pbio.2006057
Moniruzzaman, M. et al. Virus-host relationships of marine single-celled eukaryotes resolved from metatranscriptomics. Nat. Commun. 8, 16054 (2017).
pubmed: 28656958
pmcid: 5493757
doi: 10.1038/ncomms16054
Liu, J., Gefen, O., Ronin, I., Bar-Meir, M. & Balaban, N. Q. Effect of tolerance on the evolution of antibiotic resistance under drug combinations. Science 367, 200–204 (2020).
pubmed: 31919223
doi: 10.1126/science.aay3041
Yang, Q. E. et al. Interphylum dissemination of NDM-5-positive plasmids in hospital wastewater from Fuzhou, China: a single-center, culture-independent, plasmid transmission study. Lancet Microbe 5, e13–e23 (2024).
pubmed: 38006896
doi: 10.1016/S2666-5247(23)00227-6
Castañeda-Barba, S., Top, E. M. & Stalder, T. Plasmids, a molecular cornerstone of antimicrobial resistance in the One Health era. Nat. Rev. Microbiol. 22, 18–32 (2024).
pubmed: 37430173
doi: 10.1038/s41579-023-00926-x
Gabashvili, E. et al. Phage transduction is involved in the intergeneric spread of antibiotic resistance-associated blaCTX-M, Mel, and tetM loci in natural populations of some human and animal bacterial pathogens. Curr. Microbiol. 77, 185–193 (2020).
pubmed: 31754824
doi: 10.1007/s00284-019-01817-2
Sun, R., Yu, P., Zuo, P. & Alvarez, P. J. J. Bacterial concentrations and water turbulence influence the importance of conjugation versus phage-mediated antibiotic resistance gene transfer in suspended growth systems. ACS Environ. Au 2, 156–165 (2022).
pubmed: 37101581
doi: 10.1021/acsenvironau.1c00027
Chen, J. et al. Genome hypermobility by lateral transduction. Science 362, 207–212 (2018).
pubmed: 30309949
doi: 10.1126/science.aat5867
Kondo, K., Kawano, M. & Sugai, M. Distribution of antimicrobial resistance and virulence genes within the prophage-associated regions in nosocomial pathogens. mSphere 6, e00452–00421 (2021).
pubmed: 34232073
pmcid: 8386436
doi: 10.1128/mSphere.00452-21
Huang, J. et al. Conjugative transfer of streptococcal prophages harboring antibiotic resistance and virulence genes. ISME J. 17, 1467–1481 (2023).
pubmed: 37369704
pmcid: 10432423
doi: 10.1038/s41396-023-01463-4
Coban, O., De Deyn, G. B. & van der Ploeg, M. Soil microbiota as game-changers in restoration of degraded lands. Science 375, abe0725 (2022).
pubmed: 35239372
doi: 10.1126/science.abe0725
Hampton, H. G., Watson, B. N. J. & Fineran, P. C. The arms race between bacteria and their phage foes. Nature 577, 327–336 (2020).
pubmed: 31942051
doi: 10.1038/s41586-019-1894-8
Van Boeckel, T. P. et al. Reducing antimicrobial use in food animals. Science 357, 1350–1352 (2017).
pubmed: 28963240
doi: 10.1126/science.aao1495
Tang, K. L. et al. Restricting the use of antibiotics in food-producing animals and its associations with antibiotic resistance in food-producing animals and human beings: a systematic review and meta-analysis. Lancet Planet. Health 1, e316–e327 (2017).
pubmed: 29387833
pmcid: 5785333
doi: 10.1016/S2542-5196(17)30141-9
Gauthier, C. H. et al. DEPhT: a novel approach for efficient prophage discovery and precise extraction. Nucleic Acids Res. 50, e75–e75 (2022).
pubmed: 35451479
pmcid: 9303363
doi: 10.1093/nar/gkac273
Alcock, B. P. et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res. 48, 517–525 (2020).
Dong, X. et al. Phylogenetically and catabolically diverse diazotrophs reside in deep-sea cold seep sediments. Nat. Commun. 13, 4885 (2022).
pubmed: 35985998
pmcid: 9391474
doi: 10.1038/s41467-022-32503-w
Jancheva, M. & Böttcher, T. A metabolite of Pseudomonas triggers prophage-selective lysogenic to lytic conversion in Staphylococcus aureus. J. Am. Chem. Soc. 143, 8344–8351 (2021).
pubmed: 33978401
pmcid: 8193634
doi: 10.1021/jacs.1c01275
Castillo, D. et al. Widespread distribution of prophage-encoded virulence factors in marine Vibrio communities. Sci. Rep. 8, 9973 (2018).
pubmed: 29967440
pmcid: 6028584
doi: 10.1038/s41598-018-28326-9
Touchon, M., Bernheim, A. & Rocha, E. P. C. Genetic and life-history traits associated with the distribution of prophages in bacteria. ISME J. 10, 2744–2754 (2016).
pubmed: 27015004
pmcid: 5113838
doi: 10.1038/ismej.2016.47
Enault, F. et al. Phages rarely encode antibiotic resistance genes: a cautionary tale for virome analyses. ISME J. 11, 237–247 (2017).
pubmed: 27326545
doi: 10.1038/ismej.2016.90
Debroas, D. & Siguret, C. Viruses as key reservoirs of antibiotic resistance genes in the environment. ISME J. 13, 2856–2867 (2019).
pubmed: 31358910
pmcid: 6794266
doi: 10.1038/s41396-019-0478-9
Billaud, M. et al. Analysis of viromes and microbiomes from pig fecal samples reveals that phages and prophages rarely carry antibiotic resistance genes. ISME Commun. 1, 55 (2021).
pubmed: 37938642
pmcid: 9723715
doi: 10.1038/s43705-021-00054-8
Dragoš, A. et al. Phages carry interbacterial weapons encoded by biosynthetic gene clusters. Curr. Biol. 31, 3479–3489 (2021).
pubmed: 34186025
doi: 10.1016/j.cub.2021.05.046
Penadés, J. R., Chen, J., Quiles-Puchalt, N., Carpena, N. & Novick, R. P. Bacteriophage-mediated spread of bacterial virulence genes. Curr. Opin. Microbiol. 23, 171–178 (2015).
pubmed: 25528295
doi: 10.1016/j.mib.2014.11.019
Shkoporov, A. N., Turkington, C. J. & Hill, C. Mutualistic interplay between bacteriophages and bacteria in the human gut. Nat. Rev. Microbiol. 20, 737–749 (2022).
pubmed: 35773472
doi: 10.1038/s41579-022-00755-4
Hwang, Y., Roux, S., Coclet, C., Krause, S. J. E. & Girguis, P. R. Viruses interact with hosts that span distantly related microbial domains in dense hydrothermal mats. Nat. Microbiol. 06, 946–957 (2023).
doi: 10.1038/s41564-023-01347-5
Zhu, Y.-G. et al. Microbial mass movements. Science 357, 1099–1100 (2017).
pubmed: 28912233
doi: 10.1126/science.aao3007
Redondo-Salvo, S. et al. Pathways for horizontal gene transfer in bacteria revealed by a global map of their plasmids. Nat. Commun. 11, 3602 (2020).
pubmed: 32681114
pmcid: 7367871
doi: 10.1038/s41467-020-17278-2
Xiong, W. et al. Antibiotic-mediated changes in the fecal microbiome of broiler chickens define the incidence of antibiotic-resistance genes. Microbiome 6, 34 (2018).
pubmed: 29439741
pmcid: 5811963
doi: 10.1186/s40168-018-0419-2
Lopatkin, A. J. et al. Antibiotics as a selective driver for conjugation dynamics. Nat. Microbiol 1, 1–8 (2016).
doi: 10.1038/nmicrobiol.2016.44
Buelow, E., Ploy, M.-C. & Dagot, C. Role of pollution on the selection of antibiotic resistance and bacterial pathogens in the environment. Curr. Opin. Microbiol. 64, 117–124 (2021).
pubmed: 34700125
doi: 10.1016/j.mib.2021.10.005
Zheng, D. et al. Global biogeography and projection of soil antibiotic resistance genes. Sci. Adv. 8, eabq8015 (2022).
pubmed: 36383677
pmcid: 9668297
doi: 10.1126/sciadv.abq8015
Kieft, K., Zhou, Z. & Anantharaman, K. VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences. Microbiome 8, 90 (2020).
pubmed: 32522236
pmcid: 7288430
doi: 10.1186/s40168-020-00867-0
Nayfach, S. et al. CheckV assesses the quality and completeness of metagenome-assembled viral genomes. Nat. Biotechnol. 39, 578–585 (2021).
pubmed: 33349699
doi: 10.1038/s41587-020-00774-7
Luo, X.-Q. et al. Viral community-wide auxiliary metabolic genes differ by lifestyles, habitats, and hosts. Microbiome 10, 190 (2022).
pubmed: 36333738
pmcid: 9636769
doi: 10.1186/s40168-022-01384-y
Liao, H. et al. Mesophilic and thermophilic viruses are associated with nutrient cycling during hyperthermophilic composting. ISME J. 17, 916–930 (2023).
pubmed: 37031344
pmcid: 10202948
doi: 10.1038/s41396-023-01404-1
Jiang, J. Z. et al. Virus classification for viral genomic fragments using PhaGCN2. Brief. Bioinform. 24, bbac505 (2023).
pubmed: 36464489
doi: 10.1093/bib/bbac505
Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 11, 119 (2010).
doi: 10.1186/1471-2105-11-119
Axelsson, E. et al. Natural selection in avian protein‐coding genes expressed in brain. Mol. Ecol. 17, 3008–3017 (2008).
pubmed: 18482257
doi: 10.1111/j.1365-294X.2008.03795.x
Emerson, J. B. et al. Host-linked soil viral ecology along a permafrost thaw gradient. Nat. Microbiol. 3, 870–880 (2018).
pubmed: 30013236
pmcid: 6786970
doi: 10.1038/s41564-018-0190-y
Zhang, L. et al. CRISPR arrays as high-resolution markers to track microbial transmission during influenza infection. Microbiome 11, 136 (2023).
pubmed: 37330554
pmcid: 10276449
doi: 10.1186/s40168-023-01568-0
Kim, M.-S. & Bae, J.-W. Lysogeny is prevalent and widely distributed in the murine gut microbiota. ISME J. 12, 1127–1141 (2018).
pubmed: 29416123
pmcid: 5864201
doi: 10.1038/s41396-018-0061-9
Bland, C. et al. CRISPR recognition tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinform. 8, 209 (2007).
doi: 10.1186/1471-2105-8-209
Li, Z. et al. Deep sea sediments associated with cold seeps are a subsurface reservoir of viral diversity. ISME J. 15, 2366–2378 (2021).
pubmed: 33649554
pmcid: 8319345
doi: 10.1038/s41396-021-00932-y
Krivoruchko, K & Gribov, A. Pragmatic Bayesian kriging for non-stationary and moderately non-Gaussian data. Mathematics of Planet Earth. In: Proc. 15th Annual Conference of the International Association for Mathematical Geosciences) 61–65 (Springer, 2014).
Kopylova, E., Noé, L. & Touzet, H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28, 3211–3217 (2012).
pubmed: 23071270
doi: 10.1093/bioinformatics/bts611
Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).
pubmed: 29750242
pmcid: 6137996
doi: 10.1093/bioinformatics/bty191
Huang, D. et al. Enhanced mutualistic symbiosis between soil phages and bacteria with elevated chromium-induced environmental stress. Microbiome 9, 150 (2021).
pubmed: 34183048
pmcid: 8240259
doi: 10.1186/s40168-021-01074-1
Wiegand, I., Hilpert, K. & Hancock, R. E. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc. 3, 163–175 (2008).
pubmed: 18274517
doi: 10.1038/nprot.2007.521
Team, R. C. R: a language and environment for statistical computing. R. Found. Stat. Comput. 201, 12 (2019).
Jiao, S. et al. Soil microbiomes with distinct assemblies through vertical soil profiles drive the cycling of multiple nutrients in reforested ecosystems. Microbiome 6, 1–13 (2018).
doi: 10.1186/s40168-018-0526-0
Liaw, A. & Wiener, MJRn. Classification and regression by randomForest. R. N. 2, 18–22 (2002).
Yin, X. et al. ARGs-OAP v2.0 with an expanded SARG database and hidden Markov models for enhancement characterization and quantification of antibiotic resistance genes in environmental metagenomes. Bioinformatics 34, 2263–2270 (2018).
pubmed: 29408954
doi: 10.1093/bioinformatics/bty053