Detecting horizontal gene transfer among microbiota: an innovative pipeline for identifying co-shared genes within the mobilome through advanced comparative analysis
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
GA22-16786S
Czech Science Foundation
206/2023/FVHE
Internal Grant Agency of the University of Veterinary Sciences Brno
PubMed
38099617
PubMed Central
PMC10782964
DOI
10.1128/spectrum.01964-23
Knihovny.cz E-zdroje
- Klíčová slova
- animal microbiome, genome evolution, gut microbiota, horizontal gene transfer, mobile genetic elements, mobilome, resistance genes,
- MeSH
- antibakteriální látky MeSH
- Bacteria genetika MeSH
- bakteriální geny MeSH
- genom bakteriální MeSH
- mikrobiota * MeSH
- prasata MeSH
- přenos genů horizontální * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- antibakteriální látky MeSH
Horizontal gene transfer (HGT) is a key driver in the evolution of bacterial genomes. The acquisition of genes mediated by HGT may enable bacteria to adapt to ever-changing environmental conditions. Long-term application of antibiotics in intensive agriculture is associated with the dissemination of antibiotic resistance genes among bacteria with the consequences causing public health concern. Commensal farm-animal-associated gut microbiota are considered the reservoir of the resistance genes. Therefore, in this study, we identified known and not-yet characterized mobilized genes originating from chicken and porcine fecal samples using our innovative pipeline followed by network analysis to provide appropriate visualization to support proper interpretation.
Biomedical Center Faculty of Medicine Charles University Pilsen Czech Republic
Central European Institute of Technology University of Veterinary Sciences Brno Brno Czech Republic
Department of Biology University of Oxford Oxford United Kingdom
Department of Physiology Faculty of Medicine Masaryk University Brno Czech Republic
Veterinary Research Institute Brno Czech Republic
Vienna Metabolomics Center University of Vienna Vienna Austria
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Yutin N. 2013. Horizontal gene transfer, p 530–532. In Brenner’s encyclopedia of genetics, 2nd ed. Elsevier Inc.
Gullberg E, Cao S, Berg OG, Ilbäck C, Sandegren L, Hughes D, Andersson DI. 2011. Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog 7:e1002158. doi:10.1371/journal.ppat.1002158 PubMed DOI PMC
Audrain B, Farag MA, Ryu CM, Ghigo JM. 2015. Role of bacterial volatile compounds in bacterial biology. FEMS Microbiol Rev 39:222–233. doi:10.1093/femsre/fuu013 PubMed DOI
Wiedenbeck J, Cohan FM. 2011. Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol Rev 35:957–976. doi:10.1111/j.1574-6976.2011.00292.x PubMed DOI
Sevillya G, Adato O, Snir S. 2020. Detecting horizontal gene transfer: a probabilistic approach. BMC Genomics 21:106. doi:10.1186/s12864-019-6395-5 PubMed DOI PMC
Saak CC, Dinh CB, Dutton RJ. 2020. Experimental approaches to tracking mobile genetic elements in microbial communities. FEMS Microbiol Rev 44:606–630. doi:10.1093/femsre/fuaa025 PubMed DOI PMC
Schwarzerova J, Zeman M, Rychlik I, Weckwerth W, Provaznik I, Dolejska M, Cejkova D. 2022. Systems biology approach for analysis of mobile genetic elements in chicken gut microbiome, p 2865–2870. In Proceedings - 2022 IEEE international conference on bioinformatics and biomedicine, BIBM. Institute of Electrical and Electronics Engineers Inc.
Ejigu GF, Jung J. 2020. Review on the computational genome annotation of sequences obtained by next-generation sequencing. Biology (Basel) 9:295. doi:10.3390/biology9090295 PubMed DOI PMC
Schwarzerova J, Labanava A, Rychlik I, Varga M, Cejkova D. 2023. A minireview on the bioinformatics analysis of mobile gene elements in microbiome research. Front Bacteriol 2:1275910. doi:10.3389/fbrio.2023.1275910 DOI
Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter MC, Rattei T, Mende DR, Sunagawa S, Kuhn M, Jensen LJ, von Mering C, Bork P. 2016. EGGNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res 44:D286–D293. doi:10.1093/nar/gkv1248 PubMed DOI PMC
Adato O, Ninyo N, Gophna U, Snir S. 2015. Detecting horizontal gene transfer between closely related taxa. PLoS Comput Biol 11:e1004408. doi:10.1371/journal.pcbi.1004408 PubMed DOI PMC
Wyres KL, Holt KE. 2018. Klebsiella pneumoniae as a key trafficker of drug resistance genes from environmental to clinically important bacteria. Curr Opin Microbiol 45:131–139. doi:10.1016/j.mib.2018.04.004 PubMed DOI
Highlander SK, Hultén KG, Qin X, Jiang H, Yerrapragada S, Mason EO, Shang Y, Williams TM, Fortunov RM, Liu Y, et al. . 2007. Subtle genetic changes enhance virulence of methicillin resistant and sensitive Staphylococcus aureus. BMC Microbiol 7:99. doi:10.1186/1471-2180-7-99 PubMed DOI PMC
Caruso G, Buschmann A, Tomova A. 2016. Antibiotic resistance in fish farming environments: a global concern. Available from: www.isheriessciences.com
Int J of Food Sci Tech . 2003. Alderman - antibiotic use in aquaculture development of antibiotic resistance potential
Mishra RPN, Oviedo-Orta E, Prachi P, Rappuoli R, Bagnoli F. 2012. Vaccines and antibiotic resistance. Curr Opin Microbiol 15:596–602. doi:10.1016/j.mib.2012.08.002 PubMed DOI
Sitaraman R. 2018. Prokaryotic horizontal gene transfer within the human holobiont: ecological-evolutionary inferences, implications and possibilities. Microbiome 6:163. doi:10.1186/s40168-018-0551-z PubMed DOI PMC
Saak CC, Dinh CB, Dutton RJ. 2020. Experimental approaches to tracking mobile genetic elements in microbial communities. FEMS Microbiol Rev 44:606–630. doi:10.1093/femsre/fuaa025 PubMed DOI PMC
Sánchez-Soto D, Agüero-Chapin G, Armijos-Jaramillo V, Perez-Castillo Y, Tejera E, Antunes A, Sánchez-Rodríguez A. 2020. Shadowcaster: compositional methods under the shadow of phylogenetic models to detect horizontal gene transfers in prokaryotes. Genes (Basel) 11:756. doi:10.3390/genes11070756 PubMed DOI PMC
Douglas GM, Langille MGI. 2019. Current and promising approaches to identify horizontal gene transfer events in metagenomes. Genome Biol Evol 11:2750–2766. doi:10.1093/gbe/evz184 PubMed DOI PMC
Vernikos GS, Parkhill J. 2006. Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics 22:2196–2203. doi:10.1093/bioinformatics/btl369 PubMed DOI
Zhu Q, Kosoy M, Dittmar K. 2014. HGTector: an automated method facilitating genome-wide discovery of putative horizontal gene transfers. BMC Genomics 15:717. doi:10.1186/1471-2164-15-717 PubMed DOI PMC
Song W, Wemheuer B, Zhang S, Steensen K, Thomas T. 2019. MetaCHIP: community-level horizontal gene transfer identification through the combination of best-match and phylogenetic approaches. Microbiome 7:36. doi:10.1186/s40168-019-0649-y PubMed DOI PMC
Sevillya G, Adato O, Snir S. 2020. Detecting horizontal gene transfer: a probabilistic approach. BMC Genomics 21:106. doi:10.1186/s12864-019-6395-5 PubMed DOI PMC
He Y, Yuan Q, Mathieu J, Stadler L, Senehi N, Sun R, Alvarez PJJ. 2020. Antibiotic resistance genes from livestock waste: occurrence, dissemination, and treatment. npj Clean Water 3. doi:10.1038/s41545-020-0051-0 DOI
Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil P-A, Hugenholtz P. 2018. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 36:996–1004. doi:10.1038/nbt.4229 PubMed DOI
Parks DH, Chuvochina M, Chaumeil PA, Rinke C, Mussig AJ, Hugenholtz P. 2020. A complete domain-to-species taxonomy for bacteria and archaea. Nat Biotechnol 38:1079–1086. doi:10.1038/s41587-020-0539-7 PubMed DOI
Groussin M, Poyet M, Sistiaga A, Kearney SM, Moniz K, Noel M, Hooker J, Gibbons SM, Segurel L, Froment A, et al. . 2021. Elevated rates of horizontal gene transfer in the industrialized human microbiome. Cell 184:2053–2067. doi:10.1016/j.cell.2021.02.052 PubMed DOI
Evans DR, Griffith MP, Sundermann AJ, Shutt KA, Saul MI, Mustapha MM, Marsh JW, Cooper VS, Harrison LH, Van Tyne D. 2020. Systematic detection of horizontal gene transfer across genera among multidrug-resistant bacteria in a single hospital. Elife 9:e53886. doi:10.7554/eLife.53886 PubMed DOI PMC
Zhou H, Beltrán JF, Brito IL. 2021. Functions predict horizontal gene transfer and the emergence of antibiotic resistance. Sci Adv 7:eabj5056. doi:10.1126/sciadv.abj5056 PubMed DOI PMC
Juricova H, Matiasovicova J, Kubasova T, Cejkova D, Rychlik I. 2021. The distribution of antibiotic resistance genes in chicken gut microbiota commensals. Sci Rep 11:3290. doi:10.1038/s41598-021-82640-3 PubMed DOI PMC
Callens M, Scornavacca C, Bedhomme S. 2021. Evolutionary responses to codon usage of horizontally transferred genes in Pseudomonas aeruginosa: gene retention, amelioration and compensatory evolution. Microb Genom 7:000587. doi:10.1099/mgen.0.000587 PubMed DOI PMC
Bolotin E, Hershberg R. 2017. Horizontally acquired genes are often shared between closely related bacterial species. Front Microbiol 8:1536. doi:10.3389/fmicb.2017.01536 PubMed DOI PMC
Redondo-Salvo S, Fernández-López R, Ruiz R, Vielva L, de Toro M, Rocha EPC, Garcillán-Barcia MP, de la Cruz F. 2020. Pathways for horizontal gene transfer in bacteria revealed by a global map of their plasmids. Nat Commun 11:3602. doi:10.1038/s41467-020-17278-2 PubMed DOI PMC
Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. 2018. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 9:5114. doi:10.1038/s41467-018-07641-9 PubMed DOI PMC
Rodriguez-R LM, Castro JC, Kyrpides NC, Cole JR, Tiedje JM, Konstantinidis KT, Löffler FE. 2018. How much do rRNA gene surveys underestimate extant bacterial diversity. Appl Environ Microbiol 84:e00014-18. doi:10.1128/AEM.00014-18 PubMed DOI PMC
Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W, Schleifer K-H, Whitman WB, Euzéby J, Amann R, Rosselló-Móra R. 2014. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12:635–645. doi:10.1038/nrmicro3330 PubMed DOI
Kloub L, Gosselin S, Fullmer M, Graf J, Gogarten JP, Bansal MS. 2021. Systematic detection of large-scale multigene horizontal transfer in prokaryotes. Mol Biol Evol 38:2639–2659. doi:10.1093/molbev/msab043 PubMed DOI PMC
Das B, Emon MI, Moumi NA, Sein J, Pruden A, Heath LS, Zhang L. 2022. HT-ARGfinder: a comprehensive pipeline for identifying horizontally transferred antibiotic resistance genes and directionality in metagenomic sequencing data. Front Environ Sci 10. doi:10.3389/fenvs.2022.901917 DOI
Sheinman M, Arkhipova K, Arndt PF, Dutilh BE, Hermsen R, Massip F. 2021. Identical sequences found in distant genomes reveal frequent horizontal transfer across the bacterial domain. Elife 10:e62719. doi:10.7554/eLife.62719 PubMed DOI PMC
Daugavet MA, Shabelnikov SV, Podgornaya OI. 2020. Amino acid sequence associated with bacteriophage recombination site helps to reveal genes potentially acquired through horizontal gene transfer. BMC Bioinformatics 21:305. doi:10.1186/s12859-020-03599-y PubMed DOI PMC
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10:421. doi:10.1186/1471-2105-10-421 PubMed DOI PMC
Alcock BP, Huynh W, Chalil R, Smith KW, Raphenya AR, Wlodarski MA, Edalatmand A, Petkau A, Syed SA, Tsang KK, et al. . 2023. CARD 2023: expanded curation, support for machine learning, and resistome prediction at the comprehensive antibiotic resistance database. Nucleic Acids Res 51:D690–D699. doi:10.1093/nar/gkac920 PubMed DOI PMC
Sayers EW, Bolton EE, Brister JR, Canese K, Chan J, Comeau DC, Connor R, Funk K, Kelly C, Kim S, Madej T, Marchler-Bauer A, Lanczycki C, Lathrop S, Lu Z, Thibaud-Nissen F, Murphy T, Phan L, Skripchenko Y, Tse T, Wang J, Williams R, Trawick BW, Pruitt KD, Sherry ST. 2022. Database resources of the national center for biotechnology information. Nucleic Acids Res 50:D20–D26. doi:10.1093/nar/gkab1112 PubMed DOI PMC
Ricard G, McEwan NR, Dutilh BE, Jouany J-P, Macheboeuf D, Mitsumori M, McIntosh FM, Michalowski T, Nagamine T, Nelson N, Newbold CJ, Nsabimana E, Takenaka A, Thomas NA, Ushida K, Hackstein JHP, Huynen MA. 2006. Horizontal gene transfer from bacteria to rumen ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment. BMC Genomics 7:22. doi:10.1186/1471-2164-7-22 PubMed DOI PMC
Tripathi LP, Sowdhamini R. 2008. Genome-wide survey of prokaryotic serine proteases: analysis of distribution and domain architectures of five serine protease families in prokaryotes. BMC Genomics 9:549. doi:10.1186/1471-2164-9-549 PubMed DOI PMC
Medvecky M, Cejkova D, Polansky O, Karasova D, Kubasova T, Cizek A, Rychlik I. 2018. Whole genome sequencing and function prediction of 133 gut anaerobes isolated from chicken caecum in pure cultures. BMC Genomics 19:561. doi:10.1186/s12864-018-4959-4 PubMed DOI PMC
Fogg PCM, Colloms S, Rosser S, Stark M, Smith MCM. 2014. New applications for phage integrases. J Mol Biol 426:2703–2716. doi:10.1016/j.jmb.2014.05.014 PubMed DOI PMC
Seemann T. 2014. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069. doi:10.1093/bioinformatics/btu153 PubMed DOI
Galperin MY, Wolf YI, Makarova KS, Vera Alvarez R, Landsman D, Koonin EV. 2021. COG database update: focus on microbial diversity, model organisms, and widespread pathogens. Nucleic Acids Res 49:D274–D281. doi:10.1093/nar/gkaa1018 PubMed DOI PMC
Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. 2021. eggNOG-mapper V2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol 38:5825–5829. doi:10.1093/molbev/msab293 PubMed DOI PMC
Letunic I, Khedkar S, Bork P. 2021. SMART: recent updates, new developments and status in 2020. Nucleic Acids Res 49:D458–D460. doi:10.1093/nar/gkaa937 PubMed DOI PMC
Lu S, Wang J, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Marchler GH, Song JS, Thanki N, Yamashita RA, Yang M, Zhang D, Zheng C, Lanczycki CJ, Marchler-Bauer A. 2020. CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Res 48:D265–D268. doi:10.1093/nar/gkz991 PubMed DOI PMC
Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S, Cattoir V, Philippon A, Allesoe RL, Rebelo AR, Florensa AF, et al. . 2020. Resfinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 75:3491–3500. doi:10.1093/jac/dkaa345 PubMed DOI PMC
Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH, Hancock J. 2020. GTDB-Tk: a toolkit to classify genomes with the genome taxonomy database. Bioinformatics 36:1925–1927. doi:10.1093/bioinformatics/btz848 PubMed DOI PMC
Kim J, Na S-I, Kim D, Chun J. 2021. UBCG2: up-to-date bacterial core genes and pipeline for phylogenomic analysis. J Microbiol 59:609–615. doi:10.1007/s12275-021-1231-4 PubMed DOI
Sievers F, Higgins DG. 2021. The clustal omega multiple alignment package. Available from: http://www.springer.com/series/7651 PubMed
Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. 2019. RaxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35:4453–4455. doi:10.1093/bioinformatics/btz305 PubMed DOI PMC
Letunic I, Bork P. 2021. Interactive tree of life (iTOL) V5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49:W293–W296. doi:10.1093/nar/gkab301 PubMed DOI PMC
Olm MR, Brown CT, Brooks B, Banfield JF. 2017. DRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J 11:2864–2868. doi:10.1038/ismej.2017.126 PubMed DOI PMC
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. 2015. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25:1043–1055. doi:10.1101/gr.186072.114 PubMed DOI PMC
Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH, Koren S, Phillippy AM. 2016. Mash: fast genome and metagenome distance estimation using minhash. Genome Biol 17:132. doi:10.1186/s13059-016-0997-x PubMed DOI PMC
Marçais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL, Zimin A. 2018. Mummer4: a fast and versatile genome alignment system. PLoS Comput Biol 14:e1005944. doi:10.1371/journal.pcbi.1005944 PubMed DOI PMC
Fu L, Niu B, Zhu Z, Wu S, Li W. 2012. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28:3150–3152. doi:10.1093/bioinformatics/bts565 PubMed DOI PMC
Dimonaco NJ, Aubrey W, Kenobi K, Clare A, Creevey CJ. 2022. No one tool to rule them all: prokaryotic gene prediction tool annotations are highly dependent on the organism of study. Bioinformatics 38:1198–1207. doi:10.1093/bioinformatics/btab827 PubMed DOI PMC
Erich Neuwirth M. 2014. Package rcolorbrewer. Available from: http://www.colorbrewer.org
Charif D, Lobry JR. 2007. SeqinR 1.0-3: a contributed package to the R project for statistical computing devoted to biological sequences retrieval and analysis. Available from: http://pbil.univ-lyon1.fr/members/lobry/
Maintainer B, Bolar K. 2019. Package “STAT” type package title interactive document for working with basic statistical analysis. Available from: https://jarvisatharva.shinyapps.io/StatisticsPrimer/
Couch S, Bray A, Ismay C, Chasnovski E, Baumer B, Çetinkaya-Rundel M. 2021. An R package for tidyverse-friendly statistical inference. JOSS 6:3661. doi:10.21105/joss.03661 DOI
Su G, Morris JH, Demchak B, Bader GD. 2014. Biological network exploration with cytoscape 3. Curr Protoc Bioinformatics 47:8. doi:10.1002/0471250953.bi0813s47 PubMed DOI PMC
Settle B, Otasek D, Morris JH, Demchak B. 2018. aMatReader: importing adjacency matrices via cytoscape automation. F1000Res 7:ISCB Comm J-823. doi:10.12688/f1000research.15146.2 PubMed DOI PMC