Novel Qnr Families as Conserved and Intrinsic Quinolone Resistance Determinants in Aeromonas spp.
1
조회
0
다운로드
0
인용
0
참고문헌
키워드
초록
The environment has been identified as an origin, reservoir, and transmission route of antibiotic resistance genes (ARGs). Among diverse environments, freshwater environments have been recognized as pivotal in the transmission of ARGs between opportunistic pathogens and autochthonous bacteria such as Aeromonas spp. In this study, five environmental strains of Aeromonas spp. exhibiting multidrug resistance (MDR) were selected for whole-genome sequencing to ascertain their taxonomic assignment at the species-level and to delineate their ARG repertoires. Analyses of their genomes revealed the presence of one protein almost identical to AhQnr (A. hydrophila Qnr protein) and four novel proteins similar to AhQnr. To scrutinize the classification and taxonomic distribution of these proteins, all Aeromonas genomes deposited in the NCBI RefSeq genome database (1,222 genomes) were investigated. This revealed that these Aeromonas Qnr (AQnr) proteins are conserved intrinsic resistance determinants of the genus, exhibiting speciesspecific diversity. Additionally, structure prediction and analysis of contribution to quinolone resistance by AQnr proteins of the isolates, confirmed their functionality as quinolone resistance determinants. Given the origin of mobile qnr genes from aquatic bacteria and the crucial role of Aeromonas spp. in ARG dissemination in aquatic environments, a thorough understanding and strict surveillance of AQnr families prior to the clinical emergence are imperative. In this study, using comparative genome analyses and functional characterization of AQnr proteins in the genus Aeromonas, novel Aeromonas ARGs requiring surveillance has suggested.
Abstract
The environment has been identified as an origin, reservoir, and transmission route of antibiotic resistance genes (ARGs). Among diverse environments, freshwater environments have been recognized as pivotal in the transmission of ARGs between opportunistic pathogens and autochthonous bacteria such as Aeromonas spp. In this study, five environmental strains of Aeromonas spp. exhibiting multidrug resistance (MDR) were selected for whole-genome sequencing to ascertain their taxonomic assignment at the species-level and to delineate their ARG repertoires. Analyses of their genomes revealed the presence of one protein almost identical to AhQnr (A. hydrophila Qnr protein) and four novel proteins similar to AhQnr. To scrutinize the classification and taxonomic distribution of these proteins, all Aeromonas genomes deposited in the NCBI RefSeq genome database (1,222 genomes) were investigated. This revealed that these Aeromonas Qnr (AQnr) proteins are conserved intrinsic resistance determinants of the genus, exhibiting speciesspecific diversity. Additionally, structure prediction and analysis of contribution to quinolone resistance by AQnr proteins of the isolates, confirmed their functionality as quinolone resistance determinants. Given the origin of mobile qnr genes from aquatic bacteria and the crucial role of Aeromonas spp. in ARG dissemination in aquatic environments, a thorough understanding and strict surveillance of AQnr families prior to the clinical emergence are imperative. In this study, using comparative genome analyses and functional characterization of AQnr proteins in the genus Aeromonas, novel Aeromonas ARGs requiring surveillance has suggested.
참고문헌 (64)
- Aminov RI, "The role of antibiotics and antibiotic resistance in nature", Environ. Microbiol, 11, pp.2970~2988 (2009)
- Davies J, "Origins and evolution of antibiotic resistance", Microbiol. Mol. Biol. Rev, 74, pp.417~433 (2010)
- D'Costa VM, "Sampling the antibiotic resistome", Science, 311, pp.374~377 (2006)
- Surette MD, "Lessons from the environmental antibiotic resistome", Annu. Rev. Microbiol, 71, pp.309~329 (2017)
- Perry JA, "The antibiotic resistome : what's new?", Curr. Opin. Microbiol, 21, pp.45~50 (2014)
- Kim DW, "Antibiotic resistome from the one-health perspective : understanding and controlling antimicrobial resistance transmission", Exp. Mol. Med, 53, pp.301~309 (2021)
- Larsson D, "Antibiotic resistance in the environment", Nat. Rev. Microbiol, 20, pp.257~269 (2022)
- Pessoa RBG, "The genus Aeromonas : a general approach", Microb. Pathog, 130, pp.81~94 (2019)
- Beaz-Hidalgo R, "Aeromonas spp. whole genomes and virulence factors implicated in fish disease", J. Fish Dis, 36, pp.371~388 (2013)
- Janda JM, "The genus Aeromonas : taxonomy, pathogenicity, and infection", Clin. Microbiol. Rev, 23, pp.35~73 (2010)
- Baron S, "Aeromonas diversity and antimicrobial susceptibility in freshwater—an attempt to set generic epidemiological cut-off values", Front. Microbiol, 8, pp.231406~ (2017)
- Citterio B, "Aeromonas hydrophila virulence", Virulence, 6, pp.417~418 (2015)
- Reines HD, "Pneumonia and bacteremia due to Aeromonas hydrophila", Chest, 80, pp.264~267 (1981)
- Brouqui P, "Endocarditis due to rare and fastidious bacteria", Clin. Microbiol. Rev, 14, pp.177~207 (2001)
- Chen PL, "Aeromonas dhakensis, an increasingly recognized human pathogen", Front. Microbiol, 7, pp.198504~ (2016)
- Pessoa R, "Molecular characterization and evaluation of virulence traits of Aeromonas spp. isolated from the tambaqui fish (Colossoma macropomum)", Microb. Pathog, 147, pp.104273~ (2020)
- Bello-López JM, "Horizontal gene transfer and its association with antibiotic resistance in the genus Aeromonas spp", Microorganisms, 7, pp.363~ (2019)
- Piotrowska M, "The prevalence of antibiotic resistance genes among Aeromonas species in aquatic environments", Ann. Microbiol, 64, pp.921~934 (2014)
- Lee K, "Mobile resistome of human gut and pathogen drives anthropogenic bloom of antibiotic resistance", Microbiome, 8, pp.2~ (2020)
- Marti E, "The role of aquatic ecosystems as reservoirs of antibiotic resistance", Trends Microbiol, 22, pp.36~41 (2014)
- Baquero F, "Antibiotics and antibiotic resistance in water environments", Curr. Opin. Biotechnol, 19, pp.260~265 (2008)
- Lesher GY, "1, 8-Naphthyridine derivatives. A new class of chemotherapeutic agents", J. Med. Chem, 5, pp.1063~1065 (1962)
- Pham TD, "Quinolone antibiotics", Medchemcomm, 10, pp.1719~1739 (2019)
- Hooper DC, "Mechanisms of drug resistance : quinolone resistance", Ann. N. Y. Acad. Sci, 1354, pp.12~31 (2015)
- Aldred KJ, "Mechanism of quinolone action and resistance", Biochemistry, 53, pp.1565~1574 (2014)
- Bush NG, "Quinolones : mechanism, lethality and their contributions to antibiotic resistance", Molecules, 25, pp.5662~ (2020)
- Rodríguez-Martínez JM, "Plasmid-mediated quinolone resistance : two decades on", Drug Resist. Updat, 29, pp.13~29 (2016)
- Ruiz J, "Transferable mechanisms of quinolone resistance from 1998 onward", Clin. Microbiol. Rev, 32, pp.e00007-19~ (2019)
- Martínez-Martínez L, "Quinolone resistance from a transferable plasmid", Lancet, 351, pp.797~799 (1998)
- Fàbrega A, "Mechanism of action of and resistance to quinolones", Microb. Biotechnol, 2, pp.40~61 (2009)
- Jacoby GA, "Phylogenetic analysis of chromosomally determined qnr and related proteins", Antimicrob. Agents Chemother, 57, pp.1930~1934 (2013)
- Hegde SS, "A fluoroquinolone resistance protein from Mycobacterium tuberculosis that mimics DNA", Science, 308, pp.1480~1483 (2005)
- Shimizu K, "Smqnr, a new chromosome-carried quinolone resistance gene in Stenotrophomonas maltophilia", Antimicrob. Agents Chemother, 52, pp.3823~3825 (2008)
- Velasco C, "Smaqnr, a new chromosome-encoded quinolone resistance determinant in Serratia marcescens", J. Antimicrob. Chemother, 65, pp.239~242 (2010)
- Rodríguez-Martínez J, "Qnr-like pentapeptide repeat proteins in Grampositive bacteria", J. Antimicrob. Chemother, 61, pp.1240~1243 (2008)
- Xiong X, "Structural insights into quinolone antibiotic resistance mediated by pentapeptide repeat proteins : conserved surface loops direct the activity of a Qnr protein from a Gram-negative bacterium", Nucleic Acids Res, 39, pp.3917~3927 (2011)
- Poirel L, "Origin of plasmid-mediated quinolone resistance determinant QnrA", Antimicrob. Agents Chemother, 49, pp.3523~3525 (2005)
- Cattoir V, "Unexpected occurrence of plasmid-mediated quinolone resistance determinants in environmental Aeromonas spp", Emerg. Infect. Dis, 14, pp.231~ (2008)
- Xia R, "qnrVC-like gene located in a novel complex class 1 integron harboring the IS CR1 element in an Aeromonas punctata strain from an aquatic environment in Shandong Province, China", Antimicrob Agents Chemother, 54, pp.3471~3474 (2010)
- Sánchez MB, "Predictive analysis of transmissible quinolone resistance indicates Stenotrophomonas maltophilia as a potential source of a novel family of Qnr determinants", BMC Microbiol, 8, pp.148~ (2008)
- Weisburg WG, "16S ribosomal DNA amplification for phylogenetic study", J. Bacteriol, 173, pp.697~703 (1991)
- Yoon SH, "Introducing EzBioCloud : a taxonomically united database of 16S rRNA and whole genome assemblies", Int. J. Syst. Evol. Microbiol, 67, pp.1613~1617 (2017)
- Wiegand I, "Agar and broth dilution methods to determine the minimal inhibitory concentration(MIC)of antimicrobial substances", Nat. Protoc, 3, pp.163~175 (2008)
- Chin CS, "Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data", Nat. Methods, 10, pp.563~569 (2013)
- Seemann T, "Prokka : rapid prokaryotic genome annotation", Bioinformatics, 30, pp.2068~2069 (2014)
- Jain C, "High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries", Nat. Commun, 9, pp.5114~ (2018)
- Bayliss SC, "PIRATE : a fast and scalable pangenomics toolbox for clustering diverged orthologues in bacteria", Gigascience, 8, pp.giz119~ (2019)
- Nakamura T, "Parallelization of MAFFT for large-scale multiple sequence alignments", Bioinformatics, 34, pp.2490~2492 (2018)
- Price MN, "FastTree 2–approximately maximum-likelihood trees for large alignments", PLoS One, 5, pp.e9490~ (2010)
- Letunic I, "Interactive Tree Of Life(iTOL)v5 : an online tool for phylogenetic tree display and annotation", Nucleic Acids Res, 49, pp.W293~W296 (2021)
- Alcock BP, "CARD 2023 : expanded curation, support for machine learning, and resistome prediction at the comprehensive antibiotic resistance database", Nucleic Acids Res, 51, pp.D690~D699 (2023)
- Fu L, "CD-HIT : accelerated for clustering the next-generation sequencing data", Bioinformatics, 28, pp.3150~3152 (2012)
- Mirdita M, "ColabFold : making protein folding accessible to all", Nat. Methods, 19, pp.679~682 (2022)
- Meng EC, "UCSF ChimeraX : tools for structure building and analysis", Protein Sci, 32, pp.e4792~ (2023)
- Vetting MW, "Pentapeptide repeat proteins", Biochemistry, 45, pp.1~10 (2006)
- Park KS, "Determination of pentapeptide repeat units in Qnr proteins by the structure-based alignment approach", Antimicrob. Agents Chemother, 55, pp.4475~4478 (2011)
- Nilsson SV, "Sealing of gaps in duplex DNA by T4 DNA ligase", Nucleic Acids Res, 10, pp.1425~1437 (1982)
- Barco R, "A genus definition for bacteria and archaea based on a standard genome relatedness index", mBio, 11, pp.e02475-19~ (2020)
- Strahilevitz J, "Plasmid-mediated quinolone resistance : a multifaceted threat", Clin. Microbiol. Rev, 22, pp.664~689 (2009)
- Vetting MW, "Structure of QnrB1, a plasmid-mediated fluoroquinolone resistance factor", J. Biol. Chem, 286, pp.25265~25273 (2011)
- Hegde SS, "Structural and biochemical analysis of the pentapeptide repeat protein EfsQnr, a potent DNA gyrase inhibitor", Antimicrob. Agents Chemother, 55, pp.110~117 (2011)
- Takeshita S, "High-copy-number and low-copy-number plasmid vectors for lacZα-complementation and chloramphenicol-or kanamycin-resistance selection", Gene, 61, pp.63~74 (1987)
- Poirel L, "Vibrionaceae as a possible source of Qnr-like quinolone resistance determinants", J. Antimicrob. Chemother, 56, pp.1118~1121 (2005)
- Feng L, "The pentapeptide-repeat protein, MfpA, interacts with mycobacterial DNA gyrase as a DNA T-segment mimic", Proc. Natl. Acad. Sci. USA, 118, pp.e2016705118~ (2021)
