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Veterinary research2023; 54(1); 33; doi: 10.1186/s13567-023-01160-2

Whole genome sequencing to study antimicrobial resistance and RTX virulence genes in equine Actinobacillus isolates.

Abstract: Actinobacillus equuli is mostly associated with disease in horses and is most widely known as the causative agent of sleepy foal disease. Even though existing phenotypic tools such as biochemical tests, 16S rRNA gene sequencing, and Matrix Assisted Laser Desorption Ionization Time of Flight Mass Spectrometry (MALDI-TOF MS) can be used to identify members of the Actinobacillus genus, these methods struggle to differentiate between certain species and do not allow strain, virulence, and antimicrobial susceptibility typing. Hence, we performed in-depth analysis of 24 equine Actinobacillus isolates using phenotypic identification and susceptibility testing on the one hand, and long-read nanopore whole genome sequencing on the other hand. This allowed to address strain divergence down to the whole genome single nucleotide polymorphism (SNP) level. While lowest resolution was observed for 16S rRNA gene classification, a new multi-locus sequence typing (MLST) scheme allowed proper classification up to the species level. Nevertheless, a SNP-level analysis was required to distinguish A. equuli subspecies equuli and haemolyticus. Our data provided first WGS data on Actinobacillus genomospecies 1, Actinobacillus genomospecies 2, and A. arthritidis, which allowed the identification of a new Actinobacillus genomospecies 1 field isolate. Also, in-depth characterization of RTX virulence genes provided information on the distribution, completeness, and potential complementary nature of the RTX gene operons within the Actinobacillus genus. Even though overall low prevalence of acquired resistance was observed, two plasmids were identified conferring resistance to penicillin-ampicillin-amoxicillin and chloramphenicol in one A. equuli strain. In conclusion our data delivered new insights in the use of long-read WGS in high resolution identification, virulence gene typing, and antimicrobial resistance (AMR) of equine Actinobacillus species.
© 2023. The Author(s).
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Publication Date: 2023-04-05 PubMed ID: 37020296PubMed Central: PMC10074821DOI: 10.1186/s13567-023-01160-2Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research used whole genome sequencing to deeply analyze Actinobacillus equuli, a bacteria commonly causing disease in horses, to better understand its resistance to antibiotics and its virulence genes. The study uncovers new insights on identification, virulence gene typing, and antimicrobial resistance of the bacteria.

Research Purpose and Approach

  • The study aimed to explore, with greater clarity and accuracy, the antimicrobial resistance and virulent characteristics of Actinobacillus equuli, a bacterium often associated with infections in horses. Traditional identification methods, while useful, have proven to be limited in differentiating between certain species and establishing virulence and antimicrobial susceptibility patterns.
  • To achieve this, the researchers carried out an extensive analysis of 24 equine Actinobacillus isolates. This analysis incorporated both phenotypic identification and susceptibility testing alongside long-read nanopore whole genome sequencing, permitting a thorough investigation down to single nucleotide polymorphisms.

Findings

  • The study discovered that the lowest resolution was found when employing 16S rRNA gene classification, whereas a new multi-locus sequence typing (MLST) scheme allowed for proper classification up to the species level. To distinguish between A. equuli subspecies equuli and haemolyticus, however, SNP-level analysis was necessary.
  • The first whole genome sequencing (WGS) data on Actinobacillus genomospecies 1, Actinobacillus genomospecies 2, and A. arthritidis was provided by the study, unveiling a new field isolate for Actinobacillus genomospecies 1.
  • The data also allowed robust characterization of RTX virulence genes – this provided further information on distribution, completeness, and the potential complementary nature of the RTX gene operons within the Actinobacillus genus.
  • Despite mostly low prevalence of acquired resistance, penicillin-ampicillin-amoxicillin and chloramphenicol resistance in one A. equuli strain were identified, facilitated by two different plasmids.

Conclusion

  • This research not only provided new insights into this bacterial genus, but also demonstrated the effectiveness of long-read whole genome sequencing in identifying, typing virulence genes, and determining antimicrobial resistance of equine Actinobacillus species. This can help develop better disease management in horses.

Cite This Article

APA
Vereecke N, Vandekerckhove A, Theuns S, Haesebrouck F, Boyen F. (2023). Whole genome sequencing to study antimicrobial resistance and RTX virulence genes in equine Actinobacillus isolates. Vet Res, 54(1), 33. https://doi.org/10.1186/s13567-023-01160-2

Publication

Veterinary research
ISSN: 1297-9716
NlmUniqueID: 9309551
Country: England
Language: English
Volume: 54
Issue: 1
Pages: 33
PII: 33

Researcher Affiliations

Vereecke, Nick
  • Department of Translational Physiology, Infectiology and Public Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820, Merelbeke, Belgium. nick.vereecke@ugent.be.
  • PathoSense BV, Lier, Belgium. nick.vereecke@ugent.be.
Vandekerckhove, Arlette
  • Department of Pathobiology, Pharmacology and Zoological Medicine, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820, Merelbeke, Belgium.
Theuns, Sebastiaan
  • PathoSense BV, Lier, Belgium.
Haesebrouck, Freddy
  • Department of Pathobiology, Pharmacology and Zoological Medicine, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820, Merelbeke, Belgium.
Boyen, Filip
  • Department of Pathobiology, Pharmacology and Zoological Medicine, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820, Merelbeke, Belgium.

MeSH Terms

  • Animals
  • Horses
  • Actinobacillus / genetics
  • Anti-Bacterial Agents
  • Multilocus Sequence Typing / veterinary
  • RNA, Ribosomal, 16S / genetics
  • Virulence
  • Drug Resistance, Bacterial
  • Whole Genome Sequencing / veterinary

Grant Funding

  • HBC.2020.2889 / Agentschap Innoveren en Ondernemen
  • AUGE/15/05 / Research Foundation-Flanders (FWO)

Conflict of Interest Statement

None of the authors of this paper has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of the paper. ST is co-founder and co-owner of PathoSense BV. NV is an employee at PathoSense BV.

References

This article includes 74 references
  1. Rycroft AN, Garside LH. Actinobacillus species and their role in animal disease.. Vet J 2000 Jan;159(1):18-36.
    doi: 10.1053/tvjl.1999.0403pubmed: 10640409google scholar: lookup
  2. Henderson B, Diaz M, Martins C, Kenney D, Baird JD, Arroyo LG. Valvular endocarditis in the horse: 20 cases (1993-2020).. Can Vet J 2020 Dec;61(12):1290-1294.
    pmc: PMC7659875pubmed: 33299245
  3. Christensen H, Bisgaard M, Angen O, Olsen JE. Final classification of Bisgaard taxon 9 as Actinobacillus arthritidis sp. nov. and recognition of a novel genomospecies for equine strains of Actinobacillus lignieresii.. Int J Syst Evol Microbiol 2002 Jul;52(Pt 4):1239-46.
    pubmed: 12148635doi: 10.1099/00207713-52-4-1239google scholar: lookup
  4. Donahue JM, Sells SF, Bolin DC. Classification of Actinobacillus spp isolates from horses involved in mare reproductive loss syndrome.. Am J Vet Res 2006 Aug;67(8):1426-32.
    doi: 10.2460/ajvr.67.8.1426pubmed: 16881857google scholar: lookup
  5. Kokotovic B, Angen Ø, Bisgaard M. Genetic diversity of Actinobacillus lignieresii isolates from different hosts.. Acta Vet Scand 2011 Feb 8;53(1):6.
    doi: 10.1186/1751-0147-53-6pmc: PMC3041693pubmed: 21303512google scholar: lookup
  6. Murakami M, Shimonishi Y, Hobo S, Niwa H, Ito H. First isolation of Actinobacillus genomospecies 2 in Japan.. J Vet Med Sci 2016 May 3;78(4):701-3.
    doi: 10.1292/jvms.15-0597pmc: PMC4873865pubmed: 26668165google scholar: lookup
  7. Matthews S, Dart AJ, Dowling BA, Hodgson JL, Hodgson DR. Peritonitis associated with Actinobacillus equuli in horses: 51 cases.. Aust Vet J 2001 Aug;79(8):536-9.
    doi: 10.1111/j.1751-0813.2001.tb10741.xpubmed: 11599812google scholar: lookup
  8. Pusterla N, Jones ME, Mohr FC, Higgins JK, Mapes S, Jang SS, Samitz EM, Byrne BA. Fatal pulmonary hemorrhage associated with RTX toxin producing Actinobacillus equuli subspecies haemolyticus infection in an adult horse.. J Vet Diagn Invest 2008 Jan;20(1):118-21.
    doi: 10.1177/104063870802000127pubmed: 18182526google scholar: lookup
  9. Layman QD, Rezabek GB, Ramachandran A, Love BC, Confer AW. A retrospective study of equine actinobacillosis cases: 1999-2011.. J Vet Diagn Invest 2014 May;26(3):365-375.
    doi: 10.1177/1040638714531766pubmed: 24742921google scholar: lookup
  10. Moyaert H, Decostere A, Baele M, Hermans K, Tavernier P, Chiers K, Haesebrouck F. An unusual Actinobacillus equuli strain isolated from a rabbit with Tyzzer's disease.. Vet Microbiol 2007 Sep 20;124(1-2):184-6.
    doi: 10.1016/j.vetmic.2007.04.013pubmed: 17482388google scholar: lookup
  11. Schröttner P, Schultz J, Rudolph W, Gunzer F, Thürmer A, Fitze G, Jacobs E. Actinobacillus equuli ssp. haemolyticus in a semi-occlusively treated horse bite wound in a 2-year-old girl.. Ger Med Sci 2013;11:Doc14.
    pmc: PMC3782719pubmed: 24068980doi: 10.3205/000182google scholar: lookup
  12. Ward CL, Wood JL, Houghton SB, Mumford JA, Chanter N. Actinobacillus and Pasteurella species isolated from horses with lower airway disease.. Vet Rec 1998 Sep 5;143(10):277-9.
    doi: 10.1136/vr.143.10.277pubmed: 9787421google scholar: lookup
  13. Christensen H, Bisgaard M, Olsen JE. Reclassification of equine isolates previously reported as Actinobacillus equuli, variants of A. equuli, Actinobacillus suis or Bisgaard taxon 11 and proposal of A. equuli subsp. equuli subsp. nov. and A. equuli subsp. haemolyticus subsp. nov.. Int J Syst Evol Microbiol 2002 Sep;52(Pt 5):1569-1576.
    pubmed: 12361259doi: 10.1099/00207713-52-5-1569google scholar: lookup
  14. Kuhnert P, Berthoud H, Straub R, Frey J. Host cell specific activity of RTX toxins from haemolytic Actinobacillus equuli and Actinobacillus suis.. Vet Microbiol 2003 Mar 20;92(1-2):161-7.
    doi: 10.1016/S0378-1135(02)00353-Xpubmed: 12488079google scholar: lookup
  15. Ensink JM, van Klingeren B, Houwers DJ, Klein WR, Vulto AG. In-vitro susceptibility to antimicrobial drugs of bacterial isolates from horses in The Netherlands.. Equine Vet J 1993 Jul;25(4):309-13.
    doi: 10.1111/j.2042-3306.1993.tb02969.xpubmed: 8354217google scholar: lookup
  16. Thomas E, Thomas V, Wilhelm C. Antibacterial activity of cefquinome against equine bacterial pathogens.. Vet Microbiol 2006 Jun 15;115(1-3):140-7.
    doi: 10.1016/j.vetmic.2005.12.019pubmed: 16455213google scholar: lookup
  17. Nielsen SS, Bicout DJ, Calistri P, Canali E, Drewe JA, Garin-Bastuji B, Gonzales Rojas JL, Gortazar Schmidt C, Herskin M, Michel V, Miranda Chueca MA, Padalino B, Pasquali P, Roberts HC, Sihvonen LH, Spoolder H, Stahl K, Velarde A, Viltrop A, Winckler C, Dewulf J, Guardabassi L, Hilbert F, Mader R, Baldinelli F, Alvarez J. Assessment of animal diseases caused by bacteria resistant to antimicrobials: Horses.. EFSA J 2021 Dec;19(12):e07112.
    pmc: PMC8703245pubmed: 34987627doi: 10.2903/j.efsa.2021.7112google scholar: lookup
  18. Michael GB, Bossé JT, Schwarz S. Antimicrobial Resistance in Pasteurellaceae of Veterinary Origin.. Microbiol Spectr 2018 May;6(3).
    doi: 10.1128/microbiolspec.ARBA-0022-2017pubmed: 29916344google scholar: lookup
  19. Bokma J, Vereecke N, De Bleecker K, Callens J, Ribbens S, Nauwynck H, Haesebrouck F, Theuns S, Boyen F, Pardon B. Phylogenomic analysis of Mycoplasma bovis from Belgian veal, dairy and beef herds.. Vet Res 2020 Sep 23;51(1):121.
    doi: 10.1186/s13567-020-00848-zpmc: PMC7510102pubmed: 32967727google scholar: lookup
  20. De Witte C, Vereecke N, Theuns S, De Ruyck C, Vercammen F, Bouts T, Boyen F, Nauwynck H, Haesebrouck F. Presence of Broad-Spectrum Beta-Lactamase-Producing Enterobacteriaceae in Zoo Mammals.. Microorganisms 2021 Apr 14;9(4).
    doi: 10.3390/microorganisms9040834pmc: PMC8070755pubmed: 33919869google scholar: lookup
  21. Cardenas-Alvarez MX, Restrepo-Montoya D, Bergholz TM. Genome-Wide Association Study of Listeria monocytogenes Isolates Causing Three Different Clinical Outcomes.. Microorganisms 2022 Sep 29;10(10).
    doi: 10.3390/microorganisms10101934pmc: PMC9610272pubmed: 36296210google scholar: lookup
  22. Brynildsrud O, Bohlin J, Scheffer L, Eldholm V. Rapid scoring of genes in microbial pan-genome-wide association studies with Scoary.. Genome Biol 2016 Nov 25;17(1):238.
    doi: 10.1186/s13059-016-1108-8pmc: PMC5124306pubmed: 27887642google scholar: lookup
  23. Ceric O, Tyson GH, Goodman LB, Mitchell PK, Zhang Y, Prarat M, Cui J, Peak L, Scaria J, Antony L, Thomas M, Nemser SM, Anderson R, Thachil AJ, Franklin-Guild RJ, Slavic D, Bommineni YR, Mohan S, Sanchez S, Wilkes R, Sahin O, Hendrix GK, Lubbers B, Reed D, Jenkins T, Roy A, Paulsen D, Mani R, Olsen K, Pace L, Pulido M, Jacob M, Webb BT, Dasgupta S, Patil A, Ramachandran A, Tewari D, Thirumalapura N, Kelly DJ, Rankin SC, Lawhon SD, Wu J, Burbick CR, Reimschuessel R. Enhancing the one health initiative by using whole genome sequencing to monitor antimicrobial resistance of animal pathogens: Vet-LIRN collaborative project with veterinary diagnostic laboratories in United States and Canada.. BMC Vet Res 2019 May 6;15(1):130.
    doi: 10.1186/s12917-019-1864-2pmc: PMC6501310pubmed: 31060608google scholar: lookup
  24. Marin C, Marco-Jiménez F, Martínez-Priego L, De Marco-Romero G, Soriano-Chirona V, Lorenzo-Rebenaque L, D'Auria G. Rapid Oxford Nanopore Technologies MinION Sequencing Workflow for Campylobacter jejuni Identification in Broilers on Site—A Proof-of-Concept Study.. Animals (Basel) 2022 Aug 13;12(16).
    doi: 10.3390/ani12162065pmc: PMC9405271pubmed: 36009653google scholar: lookup
  25. Chen L, Li H, Chen T, Yu L, Guo H, Chen Y, Chen M, Li Z, Wu Z, Wang X, Zhao J, Yan H, Wang X, Zhou L, Zhou J. Genome-wide DNA methylation and transcriptome changes in Mycobacterium tuberculosis with rifampicin and isoniazid resistance.. Int J Clin Exp Pathol 2018;11(6):3036-3045.
    pmc: PMC6958063pubmed: 31938429
  26. Dimitriu T. Evolution of horizontal transmission in antimicrobial resistance plasmids.. Microbiology (Reading) 2022 Jul;168(7).
    doi: 10.1099/mic.0.001214pubmed: 35849537google scholar: lookup
  27. Blair JM, Webber MA, Baylay AJ, Ogbolu DO, Piddock LJ. Molecular mechanisms of antibiotic resistance.. Nat Rev Microbiol 2015 Jan;13(1):42-51.
    doi: 10.1038/nrmicro3380pubmed: 25435309google scholar: lookup
  28. Boueroy P, Wongsurawat T, Jenjaroenpun P, Chopjitt P, Hatrongjit R, Jittapalapong S, Kerdsin A. Plasmidome in mcr-1 harboring carbapenem-resistant enterobacterales isolates from human in Thailand.. Sci Rep 2022 Nov 9;12(1):19051.
    doi: 10.1038/s41598-022-21836-7pmc: PMC9646850pubmed: 36351969google scholar: lookup
  29. Bossé JT, Durham AL, Rycroft AN, Kroll JS, Langford PR. New plasmid tools for genetic analysis of Actinobacillus pleuropneumoniae and other pasteurellaceae.. Appl Environ Microbiol 2009 Oct;75(19):6124-31.
    doi: 10.1128/AEM.00809-09pmc: PMC2753053pubmed: 19666733google scholar: lookup
  30. Matter D, Rossano A, Sieber S, Perreten V. Small multidrug resistance plasmids in Actinobacillus porcitonsillarum.. Plasmid 2008 Mar;59(2):144-52.
    doi: 10.1016/j.plasmid.2007.11.003pubmed: 18190962google scholar: lookup
  31. Quinn PJ, Carter ME, Markey BK, Carter GR. Clinical veterinary microbiology. London: Wolfe/Mosby; 1994.
  32. Montagnani C, Pecile P, Moriondo M, Petricci P, Becciani S, Chiappini E, Indolfi G, Rossolini GM, Azzari C, de Martino M, Galli L. First Human Case of Meningitis and Sepsis in a Child Caused by Actinobacillus suis or Actinobacillus equuli.. J Clin Microbiol 2015 Jun;53(6):1990-2.
    doi: 10.1128/JCM.00339-15pmc: PMC4432038pubmed: 25878346google scholar: lookup
  33. Christensen H, Bisgaard M. Revised definition of Actinobacillus sensu stricto isolated from animals. A review with special emphasis on diagnosis.. Vet Microbiol 2004 Mar 26;99(1):13-30.
    doi: 10.1016/j.vetmic.2003.12.002pubmed: 15019108google scholar: lookup
  34. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH, Phillippy AM. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation.. Genome Res 2017 May;27(5):722-736.
    doi: 10.1101/gr.215087.116pmc: PMC5411767pubmed: 28298431google scholar: lookup
  35. Li H. Minimap2: pairwise alignment for nucleotide sequences.. Bioinformatics 2018 Sep 15;34(18):3094-3100.
    doi: 10.1093/bioinformatics/bty191pmc: PMC6137996pubmed: 29750242google scholar: lookup
  36. Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments.. Genome Biol 2014 Mar 3;15(3):R46.
    doi: 10.1186/gb-2014-15-3-r46pmc: PMC4053813pubmed: 24580807google scholar: lookup
  37. Jolley KA, Bliss CM, Bennett JS, Bratcher HB, Brehony C, Colles FM, Wimalarathna H, Harrison OB, Sheppard SK, Cody AJ, Maiden MCJ. Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain.. Microbiology (Reading) 2012 Apr;158(Pt 4):1005-1015.
    doi: 10.1099/mic.0.055459-0pmc: PMC3492749pubmed: 22282518google scholar: lookup
  38. Mikheenko A, Prjibelski A, Saveliev V, Antipov D, Gurevich A. Versatile genome assembly evaluation with QUAST-LG.. Bioinformatics 2018 Jul 1;34(13):i142-i150.
    doi: 10.1093/bioinformatics/bty266pmc: PMC6022658pubmed: 29949969google scholar: lookup
  39. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes.. Genome Res 2015 Jul;25(7):1043-55.
    doi: 10.1101/gr.186072.114pmc: PMC4484387pubmed: 25977477google scholar: lookup
  40. Kaas RS, Leekitcharoenphon P, Aarestrup FM, Lund O. Solving the problem of comparing whole bacterial genomes across different sequencing platforms.. PLoS One 2014;9(8):e104984.
    doi: 10.1371/journal.pone.0104984pmc: PMC4128722pubmed: 25110940google scholar: lookup
  41. Nedergaard S, Jensen AB, Haubek D, Nørskov-Lauritsen N. Multilocus Sequence Typing of Aggregatibacter actinomycetemcomitans Competently Depicts the Population Structure of the Species.. Microbiol Spectr 2021 Dec 22;9(3):e0108521.
    doi: 10.1128/Spectrum.01085-21pmc: PMC8672891pubmed: 34908433google scholar: lookup
  42. Davies RL, MacCorquodale R, Reilly S. Characterisation of bovine strains of Pasteurella multocida and comparison with isolates of avian, ovine and porcine origin.. Vet Microbiol 2004 Apr 5;99(2):145-58.
    doi: 10.1016/j.vetmic.2003.11.013pubmed: 15019106google scholar: lookup
  43. Petersen A, Christensen H, Kodjo A, Weiser GC, Bisgaard M. Development of a multilocus sequence typing (MLST) scheme for Mannheimia haemolytica and assessment of the population structure of isolates obtained from cattle and sheep.. Infect Genet Evol 2009 Jul;9(4):626-32.
    doi: 10.1016/j.meegid.2009.03.009pubmed: 19460329google scholar: lookup
  44. Meats E, Feil EJ, Stringer S, Cody AJ, Goldstein R, Kroll JS, Popovic T, Spratt BG. Characterization of encapsulated and noncapsulated Haemophilus influenzae and determination of phylogenetic relationships by multilocus sequence typing.. J Clin Microbiol 2003 Apr;41(4):1623-36.
    doi: 10.1128/JCM.41.4.1623-1636.2003pmc: PMC153921pubmed: 12682154google scholar: lookup
  45. Mullins MA, Register KB, Brunelle BW, Aragon V, Galofré-Mila N, Bayles DO, Jolley KA. A curated public database for multilocus sequence typing (MLST) and analysis of Haemophilus parasuis based on an optimized typing scheme.. Vet Microbiol 2013 Mar 23;162(2-4):899-906.
    doi: 10.1016/j.vetmic.2012.11.019pubmed: 23218953google scholar: lookup
  46. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications.. Wellcome Open Res 2018;3:124.
    doi: 10.12688/wellcomeopenres.14826.1pmc: PMC6192448pubmed: 30345391google scholar: lookup
  47. Chernomor O, von Haeseler A, Minh BQ. Terrace Aware Data Structure for Phylogenomic Inference from Supermatrices.. Syst Biol 2016 Nov;65(6):997-1008.
    doi: 10.1093/sysbio/syw037pmc: PMC5066062pubmed: 27121966google scholar: lookup
  48. CLSI (2018) Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals - VET01 5th edit.
  49. Kronvall G. Normalized resistance interpretation as a tool for establishing epidemiological MIC susceptibility breakpoints.. J Clin Microbiol 2010 Dec;48(12):4445-52.
    doi: 10.1128/JCM.01101-10pmc: PMC3008453pubmed: 20926714google scholar: lookup
  50. Interpretation NR Normalized Resistance Interpretation (NRI). http://www.bioscand.se/nri/
  51. Abricate (Seemann T). https://github.com/tseemann/abricate
  52. Chen L, Zheng D, Liu B, Yang J, Jin Q. VFDB 2016: hierarchical and refined dataset for big data analysis--10 years on.. Nucleic Acids Res 2016 Jan 4;44(D1):D694-7.
    doi: 10.1093/nar/gkv1239pmc: PMC4702877pubmed: 26578559google scholar: lookup
  53. Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, Tsang KK, Lago BA, Dave BM, Pereira S, Sharma AN, Doshi S, Courtot M, Lo R, Williams LE, Frye JG, Elsayegh T, Sardar D, Westman EL, Pawlowski AC, Johnson TA, Brinkman FS, Wright GD, McArthur AG. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database.. Nucleic Acids Res 2017 Jan 4;45(D1):D566-D573.
    doi: 10.1093/nar/gkw1004pmc: PMC5210516pubmed: 27789705google scholar: lookup
  54. Seemann T. Prokka: rapid prokaryotic genome annotation.. Bioinformatics 2014 Jul 15;30(14):2068-9.
    doi: 10.1093/bioinformatics/btu153pubmed: 24642063google scholar: lookup
  55. Robertson J, Nash JHE. MOB-suite: software tools for clustering, reconstruction and typing of plasmids from draft assemblies.. Microb Genom 2018 Aug;4(8).
    pmc: PMC6159552pubmed: 30052170doi: 10.1099/mgen.0.000206google scholar: lookup
  56. Maul C, Suchowski M, Klose K, Antov V, Pfeffer M, Schwarz BA. [Detection of Actinobacillus equuli ssp. equuli in piglets with purulent polyarthritis and tendovaginitis].. Tierarztl Prax Ausg G Grosstiere Nutztiere 2020 Feb;48(1):51-58.
    doi: 10.1055/a-1067-3908pubmed: 32059237google scholar: lookup
  57. Fox GE, Wisotzkey JD, Jurtshuk P Jr. How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity.. Int J Syst Bacteriol 1992 Jan;42(1):166-70.
    doi: 10.1099/00207713-42-1-166pubmed: 1371061google scholar: lookup
  58. Blackall PJ, Bisgaard M, McKenzie RA. Characterisation of Australian isolates of Actinobacillus capsulatus, Actinobacillus equuli, Pasteurella caballi and Bisgaard Taxa 9 and 11.. Aust Vet J 1997 Jan;75(1):52-5.
    doi: 10.1111/j.1751-0813.1997.tb13831.xpubmed: 9034500google scholar: lookup
  59. Lentsch RH, Wagner JE. Isolation of Actinobacillus lignieresii and Actinobacillus equuli from laboratory rodents.. J Clin Microbiol 1980 Sep;12(3):351-4.
    doi: 10.1128/jcm.12.3.351-354.1980pmc: PMC273589pubmed: 7217333google scholar: lookup
  60. Ashhurst-Smith C, Norton R, Thoreau W, Peel MM. Actinobacillus equuli septicemia: an unusual zoonotic infection.. J Clin Microbiol 1998 Sep;36(9):2789-90.
    doi: 10.1128/JCM.36.9.2789-2790.1998pmc: PMC105212pubmed: 9705442google scholar: lookup
  61. Dousse F, Thomann A, Brodard I, Korczak BM, Schlatter Y, Kuhnert P, Miserez R, Frey J. Routine phenotypic identification of bacterial species of the family Pasteurellaceae isolated from animals.. J Vet Diagn Invest 2008 Nov;20(6):716-24.
    doi: 10.1177/104063870802000602pubmed: 18987220google scholar: lookup
  62. Kuhnert P, Bisgaard M, Korczak BM, Schwendener S, Christensen H, Frey J. Identification of animal Pasteurellaceae by MALDI-TOF mass spectrometry.. J Microbiol Methods 2012 Apr;89(1):1-7.
    doi: 10.1016/j.mimet.2012.02.001pubmed: 22343217google scholar: lookup
  63. Jin H, You L, Zhao F, Li S, Ma T, Kwok LY, Xu H, Sun Z. Hybrid, ultra-deep metagenomic sequencing enables genomic and functional characterization of low-abundance species in the human gut microbiome.. Gut Microbes 2022 Jan-Dec;14(1):2021790.
    doi: 10.1080/19490976.2021.2021790pmc: PMC8786330pubmed: 35067170google scholar: lookup
  64. Sereika M, Petriglieri F, Jensen TBN, Sannikov A, Hoppe M, Nielsen PH, Marshall IPG, Schramm A, Albertsen M. Closed genomes uncover a saltwater species of Candidatus Electronema and shed new light on the boundary between marine and freshwater cable bacteria.. ISME J 2023 Apr;17(4):561-569.
    doi: 10.1038/s41396-023-01372-6pmc: PMC10030654pubmed: 36697964google scholar: lookup
  65. Moss EL, Maghini DG, Bhatt AS. Complete, closed bacterial genomes from microbiomes using nanopore sequencing.. Nat Biotechnol 2020 Jun;38(6):701-707.
    doi: 10.1038/s41587-020-0422-6pmc: PMC7283042pubmed: 32042169google scholar: lookup
  66. Frey J. Virulence in Actinobacillus pleuropneumoniae and RTX toxins.. Trends Microbiol 1995 Jul;3(7):257-61.
    doi: 10.1016/S0966-842X(00)88939-8pubmed: 7551637google scholar: lookup
  67. Frey J, Bosse JT, Chang YF, Cullen JM, Fenwick B, Gerlach GF, Gygi D, Haesebrouck F, Inzana TJ, Jansen R. Actinobacillus pleuropneumoniae RTX-toxins: uniform designation of haemolysins, cytolysins, pleurotoxin and their genes.. J Gen Microbiol 1993 Aug;139(8):1723-8.
    doi: 10.1099/00221287-139-8-1723pubmed: 8409915google scholar: lookup
  68. Benavente C, Fuentealba I. Actinobacillus suis and Actinobacillus equuli, emergent pathogens of septic embolic nephritis, a new challenge for the swine industry. Arch Med Vet 2012;44:99–107.
    doi: 10.4067/S0301-732X2012000200002google scholar: lookup
  69. Linhartová I, Bumba L, Mašín J, Basler M, Osička R, Kamanová J, Procházková K, Adkins I, Hejnová-Holubová J, Sadílková L, Morová J, Sebo P. RTX proteins: a highly diverse family secreted by a common mechanism.. FEMS Microbiol Rev 2010 Nov;34(6):1076-112.
    doi: 10.1111/j.1574-6976.2010.00231.xpmc: PMC3034196pubmed: 20528947google scholar: lookup
  70. Berthoud H, Frey J, Kuhnert P. Characterization of Aqx and its operon: the hemolytic RTX determinant of Actinobacillus equuli.. Vet Microbiol 2002 Jun 20;87(2):159-74.
    doi: 10.1016/S0378-1135(02)00048-2pubmed: 12034544google scholar: lookup
  71. Frey J. RTX Toxins of Animal Pathogens and Their Role as Antigens in Vaccines and Diagnostics.. Toxins (Basel) 2019 Dec 10;11(12).
    doi: 10.3390/toxins11120719pmc: PMC6950323pubmed: 31835534google scholar: lookup
  72. CLSI (2018) Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals - VET08 4th edit.
  73. Scott Weese J. Antimicrobial resistance in companion animals.. Anim Health Res Rev 2008 Dec;9(2):169-76.
    doi: 10.1017/S1466252308001485pubmed: 18983722google scholar: lookup
  74. Chang YF, Ma DP, Bai HQ, Young R, Struck DK, Shin SJ, Lein DH. Characterization of plasmids with antimicrobial resistant genes in Pasteurella haemolytica A1.. DNA Seq 1992;3(2):89-97.
    pubmed: 1333838doi: 10.3109/10425179209034001google scholar: lookup

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