Escaping the fate of Sisyphus: assessing resistome hybridization baits for antimicrobial resistance gene capture.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
12 2021
12 2021
Historique:
revised:
03
09
2021
received:
21
07
2021
accepted:
07
09
2021
pubmed:
15
9
2021
medline:
18
3
2022
entrez:
14
9
2021
Statut:
ppublish
Résumé
Finding, characterizing and monitoring reservoirs for antimicrobial resistance (AMR) is vital to protecting public health. Hybridization capture baits are an accurate, sensitive and cost-effective technique used to enrich and characterize DNA sequences of interest, including antimicrobial resistance genes (ARGs), in complex environmental samples. We demonstrate the continued utility of a set of 19 933 hybridization capture baits designed from the Comprehensive Antibiotic Resistance Database (CARD)v1.1.2 and Pathogenicity Island Database (PAIDB)v2.0, targeting 3565 unique nucleotide sequences that confer resistance. We demonstrate the efficiency of our bait set on a custom-made resistance mock community and complex environmental samples to increase the proportion of on-target reads as much as >200-fold. However, keeping pace with newly discovered ARGs poses a challenge when studying AMR, because novel ARGs are continually being identified and would not be included in bait sets designed prior to discovery. We provide imperative information on how our bait set performs against CARDv3.3.1, as well as a generalizable approach for deciding when and how to update hybridization capture bait sets. This research encapsulates the full life cycle of baits for hybridization capture of the resistome from design and validation (both in silico and in vitro) to utilization and forecasting updates and retirement.
Identifiants
pubmed: 34519156
doi: 10.1111/1462-2920.15767
doi:
Substances chimiques
Anti-Bacterial Agents
0
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, U.S. Gov't, P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
7523-7537Informations de copyright
© 2021 Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Alcock, B.P., Raphenya, A.R., Lau, T.T.Y., Tsang, K.K., Bouchard, M., Edalatmand, A., et al. (2020) CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 48: D517-D525.
Alsan, M., Kammili, N., Lakshmi, J., Xing, A., Khan, A., Rani, M., et al. (2018) Poverty and community-acquired antimicrobial resistance with extended-spectrum beta-lactamase-producing organisms, Hyderabad, India. Emerg Infect Dis 24: 1490-1496.
Amalfitano, S., Levantesi, C., Garrelly, L., Giacosa, D., Bersani, F., and Rossetti, S. (2018) Water quality and total microbial load: a double-threshold identification procedure intended for space applications. Front Microbiol 9: 2903.
Arango-Argoty, G., Garner, E., Pruden, A., Heath, L.S., Vikesland, P., and Zhang, L. (2018) DeepARG: a deep learning approach for predicting antibiotic resistance genes from metagenomic data. Microbiome 6: 23.
Beaudry, M.S., Wang, J., Kieran, T.J., Thomas, J., Bayona-Vásquez, N.J., Gao, B., et al. (2021) Improved microbial community characterization of 16S rRNA via metagenome hybridization capture enrichment. Front Microbiol 12: 1-14.
Bolger, A.M., Lohse, M., and Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114-2120.
Brooks, B., Olm, M.R., Firek, B.A., Baker, R., Thomas, B.C., Morowitz, M.J., and Banfield, J.F. (2017) Strain-resolved analysis of hospital rooms and infants reveals overlap between the human and room microbiome. Nat Commun 8: 1814.
Buckner, M.M.C., Ciusa, M.L., and Piddock, L.J.V. (2018) Strategies to combat antimicrobial resistance: anti-plasmid and plasmid curing. FEMS Microbiol Rev 42: 781-804.
CDC. (2019) Antibiotic Resistance Threats in the United States 2019. Atlanta, GA: Center for Disease Control & Prevention, US Department of Health and Human Services.
Chen, C.H., Tu, C.C., Kuo, H.Y., Zeng, R.F., Yu, C.S., Lu, H.H., and Liou, M.L. (2017) Dynamic change of surface microbiota with different environmental cleaning methods between two wards in a hospital. Appl Microbiol Biotechnol 101: 771-781.
Costea, P.I., Zeller, G., Sunagawa, S., Pelletier, E., Alberti, A., Levenez, F., et al. (2017) Towards standards for human fecal sample processing in metagenomic studies. Nat Biotechnol 35: 1069-1076.
Edgar, R.C. (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
Faircloth, B.C., McCormack, J.E., Crawford, N.G., Harvey, M.G., Brumfield, R.T., and Glenn, T.C. (2012) Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales. Syst Biol 61: 717-726.
Gasc, C., and Peyret, P. (2018) Hybridization capture reveals microbial diversity missed using current profiling methods. Microbiome 6: 61.
Gibbons, S.M., Schwartz, T., Fouquier, J., Mitchell, M., Sangwan, N., Gilbert, J.A., and Kelley, S.T. (2015) Ecological succession and viability of human-associated microbiota on restroom surfaces. Appl Environ Microbiol 81: 765-773.
Glenn, T.C., and Faircloth, B.C. (2016) Capturing Darwin's dream. Mol Ecol Resour 16: 1051-1058.
Glenn, T.C., Nilsen, R.A., Kieran, T.J., Sanders, J.G., Bayona-Vasquez, N.J., Finger, J.W., et al. (2019) Adapterama I: universal stubs and primers for 384 unique dual-indexed or 147,456 combinatorially-indexed Illumina libraries (iTru & iNext). PeerJ 7: e7755.
Guitor, A.K., Raphenya, A.R., Klunk, J., Kuch, M., Alcock, B., Surette, M.G., et al. (2019) Capturing the resistome: a targeted capture method to reveal antibiotic resistance determinants in metagenomes. Antimicrob Agents Chemother 64: e01324-19.
Huang, W., Li, L., Myers, J.R., and Marth, G.T. (2012) ART: a next-generation sequencing read simulator. Bioinformatics 28: 593-594.
Koser, C.U., Ellington, M.J., and Peacock, S.J. (2014) Whole-genome sequencing to control antimicrobial resistance. Trends Genet 30: 401-407.
Lanza, V.F., Baquero, F., Martinez, J.L., Ramos-Ruiz, R., Gonzalez-Zorn, B., Andremont, A., et al. (2018) In-depth resistome analysis by targeted metagenomics. Microbiome 6: 11.
Lasa, A., di Cesare, A., Tassistro, G., Borello, A., Gualdi, S., Furones, D., et al. (2019) Dynamics of the Pacific oyster pathobiota during mortality episodes in Europe assessed by 16S rRNA gene profiling and a new target enrichment next-generation sequencing strategy. Environ Microbiol 21: 4548-4562.
Li, C., Hofreiter, M., Straube, N., Corrigan, S., and Naylor, G.J. (2013) Capturing protein-coding genes across highly divergent species. Biotechniques 54: 321-326.
Li, H., and Durbin, R. (2009) Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25: 1754-1760.
Li, R., Yu, C., Li, Y., Lam, T.W., Yiu, S.M., Kristiansen, K., and Wang, J. (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25: 1966-1967.
Luby, E., Ibekwe, A.M., Zilles, J., and Pruden, A. (2016) Molecular methods for assessment of antibiotic resistance in agricultural ecosystems: prospects and challenges. J Environ Qual 45: 441-453.
Mahnert, A., Moissl-Eichinger, C., Zojer, M., Bogumil, D., Mizrahi, I., Rattei, T., et al. (2019) Man-made microbial resistances in built environments. Nat Commun 10: 968.
Mamanova, L., Coffey, A.J., Scott, C.E., Kozarewa, I., Turner, E.H., Kumar, A., et al. (2010) Target-enrichment strategies for next-generation sequencing. Nat Methods 7: 111-118.
McCormack, J.E., Faircloth, B.C., Crawford, N.G., Gowaty, P.A., Brumfield, R.T., and Glenn, T.C. (2012) Ultraconserved elements are novel phylogenomic markers that resolve placental mammal phylogeny when combined with species-tree analysis. Genome Res 22: 746-754.
Metsky, H.C., Siddle, K.J., Gladden-Young, A., Qu, J., Yang, D.K., Brehio, P., et al. (2019) Capturing sequence diversity in metagenomes with comprehensive and scalable probe design. Nat Biotechnol 37: 160-168.
Morgulis, A., Coulouris, G., Raytselis, Y., Madden, T.L., Agarwala, R., and Schaffer, A.A. (2008) Database indexing for production MegaBLAST searches. Bioinformatics 24: 1757-1764.
Noyes, N.R., Weinroth, M.E., Parker, J.K., Dean, C.J., Lakin, S.M., Raymond, R.A., et al. (2017) Enrichment allows identification of diverse, rare elements in metagenomic resistome-virulome sequencing. Microbiome 5: 142.
Nurk, S., Meleshko, D., Korobeynikov, A., and Pevzner, P.A. (2017) metaSPAdes: a new versatile metagenomic assembler. Genome Res 27: 824-834.
O'Neill, J. (2014). Antimicrobial resistance: tackling a crisis for the health and wealth of nations. London, UK: The Review on Antimicrobial Resistance.
Oladeinde, A., Cook, K., Lakin, S.M., Woyda, R., Abdo, Z., Looft, T., et al. (2019) Horizontal gene transfer and acquired antibiotic resistance in salmonella enterica Serovar Heidelberg following in vitro incubation in broiler ceca. Appl Environ Microbiol 85: 1-16.
Oladeinde, A., Cook, K., Orlek, A., Zock, G., Herrington, K., Cox, N., et al. (2018) Hotspot mutations and ColE1 plasmids contribute to the fitness of salmonella Heidelberg in poultry litter. PLoS One 13: e0202286.
Paterson, G.K., Harrison, E.M., and Holmes, M.A. (2014) The emergence of mecC methicillin-resistant Staphylococcus aureus. Trends Microbiol 22: 42-47.
Pendleton, J.N., Gorman, S.P., and Gilmore, B.F. (2013) Clinical relevance of the ESKAPE pathogens. Expert Rev Anti Infect Ther 11: 297-308.
Port, J.A., Cullen, A.C., Wallace, J.C., Smith, M.N., and Faustman, E.M. (2014) Metagenomic frameworks for monitoring antibiotic resistance in aquatic environments. Environ Health Perspect 122: 222-228.
R Development Core Team (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Rausch, P., Ruhlemann, M., Hermes, B.M., Doms, S., Dagan, T., Dierking, K., et al. (2019) Comparative analysis of amplicon and metagenomic sequencing methods reveals key features in the evolution of animal metaorganisms. Microbiome 7: 133.
Rohland, N., and Reich, D. (2012) Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Res 22: 939-946.
Rolo, J., Worning, P., Boye Nielsen, J., Sobral, R., Bowden, R., Bouchami, O., et al. (2017) Evidence for the evolutionary steps leading to mecA-mediated beta-lactam resistance in staphylococci. PLoS Genet 13: e1006674.
Samorodnitsky, E., Jewell, B.M., Hagopian, R., Miya, J., Wing, M.R., Lyon, E., et al. (2015) Evaluation of hybridization capture versus amplicon-based methods for whole-exome sequencing. Hum Mutat 36: 903-914.
Schmidt, H., and Hensel, M. (2004) Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev 17: 14-56.
Shen, W., Le, S., Li, Y., and Hu, F. (2016) SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PLoS One 11: e0163962.
Sommer, M.O., Church, G.M., and Dantas, G. (2010) The human microbiome harbors a diverse reservoir of antibiotic resistance genes. Virulence 1: 299-303.
Teachey, M.E., McDonald, J.M., and Ottesen, E.A. (2019) Rapid and stable microbial community assembly in the headwaters of a third-order stream. Appl Environ Microbiol 85: e00188-00119.
Teer, J.K., Bonnycastle, L.L., Chines, P.S., Hansen, N.F., Aoyama, N., Swift, A.J., et al. (2010) Systematic comparison of three genomic enrichment methods for massively parallel DNA sequencing. Genome Res 20: 1420-1431.
Thomas, J.C.T., Oladeinde, A., Kieran, T.J., Finger, J.W., Jr., Bayona-Vasquez, N.J., Cartee, J.C., et al. (2020) Co-occurrence of antibiotic, biocide, and heavy metal resistance genes in bacteria from metal and radionuclide contaminated soils at the Savannah River Site. J Microbial Biotechnol 13: 1179-1200.
Van Camp, P.J., Haslam, D.B., and Porollo, A. (2020) Bioinformatics approaches to the understanding of molecular mechanisms in antimicrobial resistance. Int J Mol Sci 21: 1363.
Wickham, H., Averick, M., Bryan, J., Chang, W., McGowan, L., François, R., et al. (2019) Welcome to the Tidyverse. J Open Source Software 4: 1686.
Yoon, S.H., Park, Y.K., and Kim, J.F. (2015) PAIDB v2.0: exploration and analysis of pathogenicity and resistance islands. Nucleic Acids Res 43: D624-D630.