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An in silico analysis of acquired antimicrobial resistance genes in Aeromonas plasmids

  • Received: 12 February 2020 Accepted: 13 March 2020 Published: 16 March 2020
  • Sequences of 105 Aeromonas species plasmids were probed for acquired anti-microbial resistance (AMR) genes using a bioinformatics approach. The plasmids showed no positive linear correlation between size and GC content and up to 55 acquired AMR genes were found in 39 (37%) plasmids after in silico screening for resistance against 15 antibiotic drug classes. Overall, potential multiple antibiotic resistance (p-MAR) index ranged from 0.07 to 0.53. Up to 18 plasmids were predicted to mediate multiple drug resistance (MDR). Plasmids pS121-1a (A. salmonicida), pWCX23_1 (A. hydrophila) and pASP-a58 (A. veronii) harboured 18, 15 and 14 AMR genes respectively. The five most occurring drug classes for which AMR genes were detected were aminoglycosides (27%), followed by beta-lactams (17%), sulphonamides (13%), fluoroquinolones (13%), and phenicols (10%). The most prevalent genes were a sulphonamide resistant gene Sul1, the gene aac (6′)-Ib-cr (aminoglycoside 6′-N-acetyl transferase type Ib-cr) resistant to aminoglycosides and the blaKPC-2 gene, which encodes carbapenemase-production. Plasmid acquisition of AMR genes was mainly inter-genus rather than intra-genus. Eighteen plasmids showed template or host genes acquired from Pseudomonas monteilii, Salmonella enterica or Escherichia coli. The most occurring antimicrobial resistance determinants (ARDs) were beta-lactamase, followed by aminoglycosides acetyl-transferases, and then efflux pumps. Screening of new isolates in vitro and in vivo is required to ascertain the level of phenotypic expression of colistin and other acquired AMR genes detected.

    Citation: Ogueri Nwaiwu, Chiugo Claret Aduba. An in silico analysis of acquired antimicrobial resistance genes in Aeromonas plasmids[J]. AIMS Microbiology, 2020, 6(1): 75-91. doi: 10.3934/microbiol.2020005

    Related Papers:

  • Sequences of 105 Aeromonas species plasmids were probed for acquired anti-microbial resistance (AMR) genes using a bioinformatics approach. The plasmids showed no positive linear correlation between size and GC content and up to 55 acquired AMR genes were found in 39 (37%) plasmids after in silico screening for resistance against 15 antibiotic drug classes. Overall, potential multiple antibiotic resistance (p-MAR) index ranged from 0.07 to 0.53. Up to 18 plasmids were predicted to mediate multiple drug resistance (MDR). Plasmids pS121-1a (A. salmonicida), pWCX23_1 (A. hydrophila) and pASP-a58 (A. veronii) harboured 18, 15 and 14 AMR genes respectively. The five most occurring drug classes for which AMR genes were detected were aminoglycosides (27%), followed by beta-lactams (17%), sulphonamides (13%), fluoroquinolones (13%), and phenicols (10%). The most prevalent genes were a sulphonamide resistant gene Sul1, the gene aac (6′)-Ib-cr (aminoglycoside 6′-N-acetyl transferase type Ib-cr) resistant to aminoglycosides and the blaKPC-2 gene, which encodes carbapenemase-production. Plasmid acquisition of AMR genes was mainly inter-genus rather than intra-genus. Eighteen plasmids showed template or host genes acquired from Pseudomonas monteilii, Salmonella enterica or Escherichia coli. The most occurring antimicrobial resistance determinants (ARDs) were beta-lactamase, followed by aminoglycosides acetyl-transferases, and then efflux pumps. Screening of new isolates in vitro and in vivo is required to ascertain the level of phenotypic expression of colistin and other acquired AMR genes detected.


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    Acknowledgments



    Authors acknowledge Center for Genomic Epidemiology, Denmark for the use of web tools.

    Conflict of interest



    Authors declare no conflict of interest.

    [1] Gonçalves Pessoa RB, de Oliveira WF, Marques DSC, et al. (2019) The genus Aeromonas: A general approach. Microb Patho 130: 81-94. doi: 10.1016/j.micpath.2019.02.036
    [2] Isonhood JH, Drake M (2002) Aeromonas species in foods. J Food Prot 65: 575-582. doi: 10.4315/0362-028X-65.3.575
    [3] Janda JM, Abbott SL (2010) The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin Microbiol Rev 23: 35-73. doi: 10.1128/CMR.00039-09
    [4] McLellan SL, Fisher JC, Newton RJ (2015) The microbiome of urban waters. Int Microbiol 18: 141-149.
    [5] Cai L, Ju F, Zhang T (2014) Tracking human sewage microbiome in a municipal wastewater treatment plant. Appl Microbiol Biot 98: 3317-3326. doi: 10.1007/s00253-013-5402-z
    [6] Fisher JC, Eren AM, Green HC, et al. (2015) Comparison of sewage and animal faecal microbiomes using oligotyping reveals potential human faecal indicators in multiple taxonomic groups. Appl Environ Microbiol 81: 7023-7033. doi: 10.1128/AEM.01524-15
    [7] Bourque DL, Vinetz JM (2018) Illnesses associated with freshwater recreation during international travel. Curr Infect Dis Rep 20: 19. doi: 10.1007/s11908-018-0623-z
    [8] Schuetz AN (2019) Emerging agents of gastroenteritis: Aeromonas, Plesiomonas, and the diarrheagenic pathotypes of Escherichia coliSemin Diag n Pathol 36: 187-192. doi: 10.1053/j.semdp.2019.04.012
    [9] Parker JL, Shaw JG (2011) Aeromonas spp. clinical microbiology and disease. J Infect 62: 109-118. doi: 10.1016/j.jinf.2010.12.003
    [10] Tena D, Aspiroz C, Figueras MJ, et al.Surgical site infection due to Aeromonas species: report of nine cases and literature review. Scand J Infect Dis 41: 164-170. doi: 10.1080/00365540802660492
    [11] Bhowmick UD, Bhattacharjee S (2018) Bacteriological, clinical and virulence aspects of Aeromonas-associated diseases in humans. Pol J Microbiol 67: 137-149. doi: 10.21307/pjm-2018-020
    [12] Villari P, Crispino M, Montuori P, et al. (2000) Prevalence and molecular characterization of Aeromonas spp. in ready-to-eat foods in Italy. J Food Prot 63: 1754-1757. doi: 10.4315/0362-028X-63.12.1754
    [13] Chacón MR, Castro-Escarpulli G, Soler L, et al. (2002) A DNA probe specific for Aeromonas colonies. Diagn Microbiol Infect Dis 44: 221-225. doi: 10.1016/S0732-8893(02)00455-8
    [14] Nwaiwu O (2019) The glycerophospholipid-cholesterol acyltransferase gene (gcat) is present in other species of Aeromonas and is not specific to Aeromonas hydrophilaInt J Infect Dis 83: 167-168. doi: 10.1016/j.ijid.2019.03.013
    [15] Hoel S, Vadstein O, Jakobsen AN (2019) The Significance of mesophilic Aeromonas spp. in minimally processed ready-to-eat seafood. Microorganisms 7: 91. doi: 10.3390/microorganisms7030091
    [16] Tanwar J, Das S, Fatima Z, et al. (2014) Multidrug resistance: An emerging crisis. Interdiscip Perspec Infect Dis 2014: 541340. doi: 10.1155/2014/541340
    [17] WHO (World Health Organization) (2015) Global action plan on antimicrobial resistance.Available from: https://apps.who.int/iris/bitstream/handle/10665/193736/9789241509763_eng.pdf?sequence=1&isAllowed=y (Accessed 18 September 2019).
    [18] Dolejska M, Papagiannitsis CC (2018) Plasmid-mediated resistance is going wild. Plasmid 99: 99-111. doi: 10.1016/j.plasmid.2018.09.010
    [19] Deng YT, Wu YL, Tan AP, et al. (2014) Analysis of antimicrobial resistance genes in Aeromonas spp. isolated from cultured freshwater animals in China. Microb Drug Resist 20: 350-356. doi: 10.1089/mdr.2013.0068
    [20] Nwaiwu O, Nwachukwu MI (2016) Detection and molecular identification of persistent water vessel colonizing bacteria in a table water factory in Nigeria. Br Microbiol Res J 13: 1-12. doi: 10.9734/BMRJ/2016/24378
    [21] Stratev D, Odeyemi OA (2016) Antimicrobial resistance of Aeromonas hydrophila isolated from different food sources: A mini-review. J Infect Public Health 9: 535-544. doi: 10.1016/j.jiph.2015.10.006
    [22] Ramadan H, Ibrahim N, Samir M, et al. (2018) Aeromonas hydrophila from marketed mullet (Mugil cephalus) in Egypt: PCR characterization of β-lactam resistance and virulence genes. J Appl Microbiol 124: 1629-1637. doi: 10.1111/jam.13734
    [23] Alcalde-Rico M, Hernando-Amado S, Blanco P, et al. (2016) Multidrug Efflux Pumps at the crossroad between antibiotic resistance and bacterial virulence. Front Microbiol 7: 1483. doi: 10.3389/fmicb.2016.01483
    [24] Li X-Z, Plésiat P, Nikaido H (2015) The challenge of efflux-mediated antibiotic resistance in Gram-negative bacteria. Clin Microbiol Rev 28: 337-418. doi: 10.1128/CMR.00117-14
    [25] Webber MA, Piddock LJV (2003) The importance of efflux pumps in bacterial antibiotic resistance. J Antimicrob Chemother 51: 9-11. doi: 10.1093/jac/dkg050
    [26] Gillings MR (2014) Integrons: past, present, and future. Microbiol Mol Biol Rev 78: 257-277. doi: 10.1128/MMBR.00056-13
    [27] Amos GCA, Ploumakis S, Zhang L, et al. (2018) The widespread dissemination of integrons throughout bacterial communities in a riverine system. ISME J 12: 681-691. doi: 10.1038/s41396-017-0030-8
    [28] Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299-304. doi: 10.1038/35012500
    [29] Werner A (2014) Horizontal gene transfer among bacteria and its role in biological evolution. Life (Basel) 4: 217-224.
    [30] Burmeister AR (2015) Horizontal gene transfer. Evol Med Public Health 2015: 193-194. doi: 10.1093/emph/eov018
    [31] Zhou Y, Yu L, Nan Z, et al. (2019) Taxonomy, virulence genes and antimicrobial resistance of Aeromonas isolated from extra-intestinal and intestinal infections. BMC Infect Dis 19: 158. doi: 10.1186/s12879-019-3766-0
    [32] Scarano C, Piras F, Virdis S, et al. (2018) Antibiotic resistance of Aeromonas spp. strains isolated from Sparus aurata reared in Italian mariculture farms. Int J Food Microbiol 284: 91-97. doi: 10.1016/j.ijfoodmicro.2018.07.033
    [33] Li F, Wang W, Zhu Z, et al. (2015) Distribution, virulence-associated genes and antimicrobial resistance of Aeromonas isolates from diarrheal patients and water, China. J Infect 70: 600-608. doi: 10.1016/j.jinf.2014.11.004
    [34] NCBINational Center for Biotechnology Information. Genome Information by Organism.Available from: https://www.ncbi.nlm.nih.gov/genome/browse/#!/overview/.
    [35] Zankari E, Hasman H, Cosentino S, et al. (2012) Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67: 2640-2644. doi: 10.1093/jac/dks261
    [36] Zankari E, Hasman H, Kaas RS, et al. (2013) Genotyping using whole-genome sequencing is a realistic alternative to surveillance based on phenotypic antimicrobial susceptibility testing. J Antimicrob Chemother 68: 771-777. doi: 10.1093/jac/dks496
    [37] Binda E, Marinelli F, Marcone GL (2014) Old and New glycopeptide antibiotics: Action and resistance. Antibiotics (Basel) 3: 572-594. doi: 10.3390/antibiotics3040572
    [38] Krumperman PH (1983) Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Appl Environ Microbiol 46: 165-170. doi: 10.1128/AEM.46.1.165-170.1983
    [39] Davis R, Brown PD (2016) Multiple antibiotic resistance index, fitness and virulence potential in respiratory Pseudomonas aeruginosa from Jamaica. J Med Microbiol 65: 261-271. doi: 10.1099/jmm.0.000229
    [40] Magiorakos AP, Srinivasan A, Carey RB, et al. (2012) Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18: 268-281. doi: 10.1111/j.1469-0691.2011.03570.x
    [41] Clausen PT, Zankari E, Aarestrup FMBenchmarking of methods for identification of antimicrobial resistance genes in bacterial whole genome data. J Antimicrob Chemother 71: 2484-2488. doi: 10.1093/jac/dkw184
    [42] Clausen PTLC, Aarestrup FM, Lund O (2018) Rapid and precise alignment of raw reads against redundant databases with KMA. BMC Bioinformatics 19: 307. doi: 10.1186/s12859-018-2336-6
    [43] Center for Genomic Epidemiology ResFinderFG 1.0 database.Available from: https://cge.cbs.dtu.dk/services/ResFinderFG/.
    [44] XLSTAT: The leading data analysis and statistical solution for Microsoft Excel®.Available from: https://www.xlstat.com/en/.
    [45] Zhang Z, Schwartz S, Wagner L, et al. (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7: 203-214. doi: 10.1089/10665270050081478
    [46] Kumar S, Stecher G, Li M, et al. (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35: 1547-1549. doi: 10.1093/molbev/msy096
    [47] Tamura K, Nei M, Kumar S, (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101: 11030-11035. doi: 10.1073/pnas.0404206101
    [48] Nishida H (2012) Evolution of genome base composition and genome size in bacteria. Front Microbiol 3: 420. doi: 10.3389/fmicb.2012.00420
    [49] Sørensen SJ, Bailey M, Hansen LH, et al. (2005) Studying plasmid horizontal transfer in situ: a critical review. Nat Rev Micro 3: 700-710. doi: 10.1038/nrmicro1232
    [50] Romiguier J, Roux C (2017) Analytical biases associated with GC-content in molecular evolution. Front Genet 8: 16. doi: 10.3389/fgene.2017.00016
    [51] Musto H, Naya H, Zavala A, et al. (2006) Genomic GC level, optimal growth temperature, and genome size in prokaryotes. Biochem Biophys Res Commun 347: 1-3. doi: 10.1016/j.bbrc.2006.06.054
    [52] Agashe D, Shankar N (2014) The evolution of bacterial DNA base composition. J Exp Zool B Mol Dev Evol 322: 517-528. doi: 10.1002/jez.b.22565
    [53] Li X-Q, Du D (2014) Variation, evolution, and correlation analysis of C+G content and genome or chromosome size in different kingdoms and phyla. PLoS One 9: e88339. doi: 10.1371/journal.pone.0088339
    [54] Shintani M, Sanchez ZK, Kimbara K (2015) Genomics of microbial plasmids: classification and identification based on replication and transfer systems and host taxonomy. Front Microbiol 6: 242. doi: 10.3389/fmicb.2015.00242
    [55] Reichenberger ER, Rosen G, Hershberg U (2015) Prokaryotic nucleotide composition is shaped by both phylogeny and the environment. Genome Biol Evol 7: 1380-1389. doi: 10.1093/gbe/evv063
    [56] Raghava GPS, Searle SMJ, Audley PC, et al. (2003) OXBench: A benchmark for evaluation of protein multiple sequence alignment accuracy. BMC Bioinformatics 4: 47. doi: 10.1186/1471-2105-4-47
    [57] Martí-Renom MA, Stuart AC, Fiser A, et al. (2000) Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct 29: 291-325. doi: 10.1146/annurev.biophys.29.1.291
    [58] Sköld OResistance to trimethoprim and sulfonamides. Vet Res 32: 261-273. doi: 10.1051/vetres:2001123
    [59] Domínguez M, Miranda CD, Fuentes O, et al. (2019) Occurrence of transferable integrons and sul and dfr genes among sulfonamide-and/or trimethoprim-resistant bacteria isolated from Chilean salmonid farms. Front Microbiol 10: 748. doi: 10.3389/fmicb.2019.00748
    [60] Adelowo OO, Helbig T, Knecht C, et al. (2018) High abundances of class 1 integrase and sulfonamide resistance genes, and characterisation of class 1 integron gene cassettes in four urban wetlands in Nigeria. PLoS One 13: e0208269. doi: 10.1371/journal.pone.0208269
    [61] Quiroga MP, Andres P, Petroni A, et al. (2007) Complex class 1 integrons with diverse variable regions, including aac(6′)-Ib-cr, and a novel allele, qnrB10, associated with ISCR1 in clinical enterobacterial isolates from Argentina. Antimicrob Agents Chemother 51: 4466-4470. doi: 10.1128/AAC.00726-07
    [62] Ma J, Zeng Z, Chen Z, et al. (2009) High prevalence of plasmid-mediated quinolone resistance determinants qnr, aac(6′)-Ib-cr, and qepA among ceftiofur-resistant Enterobacteriaceae isolates from companion and food-producing animals. Antimicrob Agents Chemother 53: 519-524. doi: 10.1128/AAC.00886-08
    [63] Yigit H, Queenan AM, Anderson GJ, et al. (2001) Novel carbapenem-hydrolyzing beta-lactamase, KPC-1, from a carbapenem-resistant strain of Klebsiella pneumoniaeAntimicrob Agents Chemother 45: 1151-1161. doi: 10.1128/AAC.45.4.1151-1161.2001
    [64] Mathys DA, Mollenkopf DF, Feicht SM (2019) Carbapenemase-producing Enterobacteriaceae and Aeromonas spp. present in wastewater treatment plant effluent and nearby surface waters in the US. PLoS One 14.
    [65] Bush K, Jacoby GA (2010) Updated functional classification of β-Lactamases. Antimicrob Agents Chemother 54: 969-976. doi: 10.1128/AAC.01009-09
    [66] Son R, Rusul G, Sahilah AM, et al. (1997) Antibiotic resistance and plasmid profile of Aeromonas hydrophila isolates from cultured fish, Telapia (Telapia mossambica). Lett Appl Microbiol 24: 479-482. doi: 10.1046/j.1472-765X.1997.00156.x
    [67] Aoki T, Takahashi A (1987) Class D tetracycline resistance determinants of R plasmids from the fish pathogens Aeromonas hydrophila, Edwardsiella tarda, and Pasteurella piscicidaAntimicrob Agents Chemother 31: 1278-1280. doi: 10.1128/AAC.31.8.1278
    [68] Zhang R, Ichijo T, Huang YL, et al. (2012) High prevalence of qnr and aac(6′)-Ib-cr genes in both water-borne environmental bacteria and clinical isolates of Citrobacter freundii in China. Microbes Environ 27: 158-163. doi: 10.1264/jsme2.ME11308
    [69] Tuo H, Yang Y, Tao X, et al. (2018) The Prevalence of colistin resistant strains and antibiotic resistance gene profiles in Funan river, China. Front Microbiol 9: 3094. doi: 10.3389/fmicb.2018.03094
    [70] Attéré SA, Vincent AT, Trudel MV, et al. (2015) Diversity and homogeneity among small plasmids of Aeromonas salmonicida subsp. salmonicida linked with geographical origin. Front Microbiol 6: 1274. doi: 10.3389/fmicb.2015.01274
    [71] Massicotte MA, Vincent AT, Schneider A, et al. (2019) One Aeromonas salmonicida subsp. salmonicida isolate with a pAsa5 variant bearing antibiotic resistance and a pRAS3 variant making a link with a swine pathogen. Sci Total Environ 690: 313-320. doi: 10.1016/j.scitotenv.2019.06.456
    [72] Wein T, Hülter NF, Mizrahi I, et al. (2019) Emergence of plasmid stability under non-selective conditions maintains antibiotic resistance. Nat Commun 10: 1-13. doi: 10.1038/s41467-019-10600-7
    [73] Sultan I, Rahman S, Jan AT, et al. (2018) Antibiotics, resistome and resistance mechanisms: A bacterial perspective. Front Microbiol 9: 2066. doi: 10.3389/fmicb.2018.02066
    [74] Del Castillo CS, Hikima J, Jang HB, et al. (2013) Comparative sequence analysis of a multidrug-resistant plasmid from Aeromonas hydrophilaAntimicrob Agents Chemother 57: 120-129. doi: 10.1128/AAC.01239-12
    [75] Nikaido H (2009) Multidrug resistance in bacteria. Annu Rev Biochem 78: 119-146. doi: 10.1146/annurev.biochem.78.082907.145923
    [76] Sun J, Deng Z, Yan A (2014) Bacterial multidrug efflux pumps: Mechanisms, physiology and pharmacological exploitation. Biochem Biophys Res Commun 453: 254-267. doi: 10.1016/j.bbrc.2014.05.090
    [77] Libisch B, Giske CG, Kovács B, et al. (2008) Identification of the first VIM metallo-β-lactamase-producing multiresistant Aeromonas hydrophila strain. J Clin Microbiol 46: 1878-1880. doi: 10.1128/JCM.00047-08
    [78] European Antimicrobial Resistance Surveillance Network (EARS-Net)Surveillance of antimicrobial resistance in Europe.Annual report, 2016. Available from: https://www.ecdc.europa.eu/sites/portal/files/documents/AMR-surveillance-Europe-2016.pdf.
    [79] Al-Tawfiq JA, Laxminarayan R, Mendelson M (2017) How should we respond to the emergence of plasmid-mediated colistin resistance in humans and animals? Int J Infect Dis 54: 77-84. doi: 10.1016/j.ijid.2016.11.415
    [80] Caniaux I, Van Belkum A, Zambardi G, et al. (2017) MCR: modern colistin resistance. Eur J Clin Microbiol Infect Dis 36: 415-420. doi: 10.1007/s10096-016-2846-y
    [81] Basak S, Singh P, Rajurkar M (2016) Multidrug-Resistant and extensively drug resistant bacteria: A Study. J Pathog 2016: 4065603. doi: 10.1155/2016/4065603
    [82] Liu YY, Wang Y, Walsh TR, et al. (2016) Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 16: 161-168. doi: 10.1016/S1473-3099(15)00424-7
    [83] Neerincx PB, Leunissen JA (2005) Evolution of web services in bioinformatics. Brief Bioinform 6: 178-188. doi: 10.1093/bib/6.2.178
    [84] Behzadi P, Ranjbar R (2019) DNA microarray technology and bioinformatic web services. Acta Microbiol Immunol Hung 66: 19-30. doi: 10.1556/030.65.2018.028
    [85] Nwaiwu O (2018) Data on evolutionary relationships of Aeromonas hydrophila and Serratia proteamaculans that attach to water tanks. Data in Brief 16: 10-14. doi: 10.1016/j.dib.2017.10.073
    [86] Carnelli A, Mauri F, Demarta A (2017) Characterization of genetic determinants involved in antibiotic resistance in Aeromonas spp. and fecal coliforms isolated from different aquatic environments. Res Microbiol 168: 461-471. doi: 10.1016/j.resmic.2017.02.006
    [87] Jagoda SSSD, Honein K, Arulkanthan A, et al. (2017) Genome sequencing and annotation of Aeromonas veronii strain Ae52, a multidrug-resistant isolate from septicaemic gold fish (Carassius auratus) in Sri Lanka. Genom Data 11: 46-48. doi: 10.1016/j.gdata.2016.11.011
    [88] Hamner S, Brown BL, Hasan NA, et al. (2019) Metagenomic profiling of microbial pathogens in the little Bighorn river, Montana. Int J Environ Res Public Health 16: 1079. doi: 10.3390/ijerph16071097
    [89] Lan R, Reeves PR (2000) Intraspecies variation in bacterial genomes: the need for a species genome concept. Trends Microbiol 8: 396-401. doi: 10.1016/S0966-842X(00)01791-1
    [90] Kılıç S, Erill I (2016) Assessment of transfer methods for comparative genomics of regulatory networks in bacteria. BMC Bioinformatics 8: 277. doi: 10.1186/s12859-016-1113-7
    [91] Bogusz M, Whelan S (2017) Phylogenetic tree estimation with and without alignment: New distance methods and benchmarking. Syst Biol 66: 218-231.
    [92] Zielezinski A, Vinga S, Almeida J, et al. (2017) Alignment-free sequence comparison: benefits, applications, and tools. Genome Biol 18: 186. doi: 10.1186/s13059-017-1319-7
    [93] Bernard G, Chan CX, Chan YB, et al. (2019) Alignment-free inference of hierarchical and reticulate phylogenomic relationships. Brief Bioinform 20: 426-435. doi: 10.1093/bib/bbx067
    [94] Han JE, Kim JH, Choresca CH, et al. (2012) First description of ColE-type plasmid in Aeromonas spp. carrying quinolone resistance (qnrS2) gene. Lett Appl Microbiol 55: 290-294. doi: 10.1111/j.1472-765X.2012.03293.x
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