1887

Abstract

is a fastidious facultative intracellular bacterial pathogen that causes ‘piscine francisellosis’, a serious disease affecting both marine and fresh water farmed and wild fish worldwide. Currently two subspecies are recognized, i.e. subsp. and subsp. . In the present study, the taxonomy of was revisited using a polyphasic approach, including whole genome derived parameters such as digital DNA–DNA hybridization, whole genome average nucleotide identity (wg-ANIm), whole genome phylogenetic analysis, whole genome G+C content, metabolic fingerprinting and chemotaxonomic analyses. The results indicated that isolates belonging to subsp. represent a phenotypically and genetically homogenous taxon, clearly distinguishable from subsp. that fulfils requirements for separate species status. We propose, therefore, elevation of subsp. to the species rank as sp. nov. with the type strain remaining as Ehime-1 (DSM 21254=LMG 24544). Furthermore, we identified sufficient phenotypic and genetic differences between subsp. recovered from diseased farmed Atlantic salmon in Chile and those isolated from wild and farmed Atlantic cod in Northern Europe to warrant proposal of the Chilean as a novel subspecies, i.e. subsp. subsp. nov. with strain PQ1106 (CECT 9798=NCTC14375) as the type strain. Finally, we emend the description of by including further metabolic information and the description of atypical strains.

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2020-03-11
2020-06-02
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References

  1. Boscaro V, Vannini C, Fokin SI, Verni F, Petroni G. Characterization of "Candidatus Nebulobacter yamunensis" from the cytoplasm of Euplotes aediculatus (Ciliophora, Spirotrichea) and emended description of the family Francisellaceae . Syst Appl Microbiol 2012; 35:432–440 [CrossRef]
    [Google Scholar]
  2. Brevik OJ, Ottem KF, Kamaishi T, Watanabe K, Nylund A. Francisella halioticida sp. nov., a pathogen of farmed giant abalone (Haliotis gigantea) in Japan. J Appl Microbiol 2011; 111:1044–1056 [CrossRef]
    [Google Scholar]
  3. Challacombe JF, Petersen JM, Gallegos-Graves LV, Hodge D, Pillai S et al. Whole-genome relationships among Francisella bacteria of diverse origins define new species and provide specific regions for detection. Appl Environ Microbiol 2017; 83:e2589–e2516 [CrossRef]
    [Google Scholar]
  4. Euzeby J. Notification of changes in taxonomic opinion previously published outside the IJSEM. Int J Syst Evol Microbiol 2013; 63:8–9
    [Google Scholar]
  5. Huber B, Escudero R, Busse H-J, Seibold E, Scholz HC et al. Description of Francisella hispaniensis sp. nov., isolated from human blood, reclassification of Francisella novicida (Larson et al. 1955) Olsufiev et al. 1959 as Francisella tularensis subsp. novicida comb. nov. and emended description of the genus Francisella . Int J Syst Evol Microbiol 2010; 60:1887–1896 [CrossRef]
    [Google Scholar]
  6. Larson MA, Nalbantoglu U, Sayood K, Zentz EB, Cer RZ et al. Reclassification of Wolbachia persica as Francisella persica comb. nov. and emended description of the family Francisellaceae . Int J Syst Evol Microbiol 2016; 66:1200–1205 [CrossRef]
    [Google Scholar]
  7. Liu L, Salam N, Jiao J-Y, E S-M, Chen C et al. Cysteiniphilum litorale gen. nov., sp. nov., isolated from coastal seawater. Int J Syst Evol Microbiol 2017; 67:2178–2183 [CrossRef]
    [Google Scholar]
  8. PH Q, Li Y, Salam N, Chen SY, Liu L et al. Allofrancisella inopinata gen. nov., sp. nov. and Allofrancisella frigidaquae sp. nov., isolated from water-cooling systems, and transfer of Francisella guangzhouensis Qu, et al. 2013 to the new genus as Allofrancisella guangzhouensis comb. nov. Int J Syst Evol Microbiol 2016:4832–4838
    [Google Scholar]
  9. Sjödin A, Öhrman C, Bäckman S, Lärkeryd A, Granberg M et al. Complete genome sequence of Francisella endociliophora strain FSC1006, isolated from a laboratory culture of the marine ciliate Euplotes raikovi . Genome Announc 2014; 2:e01227–14 [CrossRef]
    [Google Scholar]
  10. Soto E, Griffin MJ, Morales JA, Calvo EB, de Alexandre Sebastião F et al. Francisella marina sp. nov., etiologic agent of systemic disease in cultured spotted rose snapper (Lutjanus guttatus) in Central America. Appl Environ Microbiol 2018AEM-00144
    [Google Scholar]
  11. Vallesi A, Sjödin A, Petrelli D, Luporini P, Taddei AR et al. A New Species of the γ-Proteobacterium Francisella, F. adeliensis sp. nov., Endocytobiont in an Antarctic Marine Ciliate and Potential Evolutionary Forerunner of Pathogenic Species. Microb Ecol 20181–10
    [Google Scholar]
  12. Xiao M, Salam N, Liu L, Jiao J-Y, Zheng M-L et al. Fastidiosibacter lacustris gen. nov., sp. nov., isolated from a lake water sample, and proposal of Fastidiosibacteraceae fam. nov. within the order Thiotrichales . Int J Syst Evol Microbiol 2018; 68:347–352 [CrossRef]
    [Google Scholar]
  13. Zheng ML, Jiao JY, Dong L, Han MX, LH L et al. Pseudofrancisella aestuarii gen. nov., sp. nov., a novel member of the family Francisellaceae isolated from estuarine seawater. Antonie van Leeuwenhoek 2018
    [Google Scholar]
  14. Busse H-J, Scholz HC, Escudero R, Anda P, Kämpfer P et al. Objections to the transfer of Francisella novicida to the subspecies rank of Francisella tularensis – response to Johansson et al. Int J Syst Evol Microbiol 2010; 60:1718–1720 [CrossRef]
    [Google Scholar]
  15. Johansson A, Celli J, Conlan W, Elkins KL, Forsman M et al. Objections to the transfer of Francisella novicida to the subspecies rank of Francisella tularensis . Int J Syst Evol Microbiol 2010; 60:1717–1718 [CrossRef]
    [Google Scholar]
  16. Kingry LC, Petersen JM. Comparative review of Francisella tularensis and Francisella novicida. Frontiers in cellular and infection microbiology. Front Cell Infect Microbiol 2014; 4:35
    [Google Scholar]
  17. Larsson P, Elfsmark D, Svensson K, Wikström P, Forsman M et al. Molecular evolutionary consequences of niche restriction in Francisella tularensis, a facultative intracellular pathogen. PLoS Pathog 2009; 5:e1000472 [CrossRef]
    [Google Scholar]
  18. Matz LM, Kamdar KY, Holder ME, Metcalf GA, Weissenberger GM et al. Challenges of Francisella classification exemplified by an atypical clinical isolate. Diagn Microbiol Infect Dis 2018; 90:241–247 [CrossRef]
    [Google Scholar]
  19. Mikalsen J, Olsen AB, Tengs T, Colquhoun DJ. Francisella philomiragia subsp. noatunensis subsp. nov., isolated from farmed Atlantic cod (Gadus morhua L.). Int J Syst Evol Microbiol 2007; 57:1960–1965 [CrossRef]
    [Google Scholar]
  20. Ottem KF, Nylund A, Karlsbakk E, Friis-Møller A, Krossøy B et al. New species in the genus Francisella (Gammaproteobacteria; Francisellaceae); Francisella piscicida sp. nov. isolated from cod (Gadus morhua). Arch Microbiol 2007; 188:547–550 [CrossRef]
    [Google Scholar]
  21. Schrallhammer M, Schweikert M, Vallesi A, Verni F, Petroni G. Detection of a novel subspecies of Francisella noatunensis as endosymbiont of the ciliate Euplotes raikovi . Microb Ecol 2011; 61:455–464 [CrossRef]
    [Google Scholar]
  22. Colquhoun DJ, Duodu S. Francisella infections in farmed and wild aquatic organisms. Vet Res 2011; 42:47–62 [CrossRef]
    [Google Scholar]
  23. Ottem KF, Nylund A, Karlsbakk E, Friis-Møller A, Kamaishi T. Elevation of Francisella philomiragia subsp. noatunensis Mikalsen et al. (2007) to Francisella noatunensis comb. nov. [syn. Francisella piscicida Ottem et al. (2008) syn. nov.] and characterization of Francisella noatunensis subsp. orientalis subsp. nov., two important fish pathogens . J Appl Microbiol 2009; 106:1231–1243 [CrossRef]
    [Google Scholar]
  24. Ramírez-Paredes JG, Thompson KD, Metselaar M, Shahin K, Soto E et al. A Polyphasic Approach for Phenotypic and Genetic Characterization of the Fastidious Aquatic Pathogen Francisella noatunensis subsp. orientalis . Front Microbiol 2017; 8:2324 [CrossRef]
    [Google Scholar]
  25. Ramirez-Paredes JG, Larsson P, Wehner S, Bekaert M, Öhrman C et al. Draft Genome Sequence of Francisella noatunensis subsp. orientalis STIR-GUS-F2f7, a Highly Virulent Strain Recovered from Diseased Red Nile Tilapia Farmed in Europe. 2017. Genome Announc 5:e01555–16
    [Google Scholar]
  26. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [CrossRef]
    [Google Scholar]
  27. Suzuki MT, Giovannoni SJ. Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl Environ Microbiol 1996; 62:625–630 [CrossRef]
    [Google Scholar]
  28. Stothard P. The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 2000; 28:1102–1104 [CrossRef]
    [Google Scholar]
  29. Edgar RC. Muscle: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004; 5:113 [CrossRef]
    [Google Scholar]
  30. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30:2725–2729 [CrossRef]
    [Google Scholar]
  31. Nei M, Kumar S. Molecular Evolution and Phylogenetics 9780195135855, ISBN. New York USA: Oxford University Press; 2000
    [Google Scholar]
  32. Hasegawa M, Kishino H, Yano T-aki. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 1985; 22:160–174 [CrossRef]
    [Google Scholar]
  33. Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119 [CrossRef]
    [Google Scholar]
  34. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJM et al. ABySS: a parallel assembler for short read sequence data. Genome Res 2009; 19:1117–1123 [CrossRef]
    [Google Scholar]
  35. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 2004; 14:1394–1403 [CrossRef]
    [Google Scholar]
  36. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 2009; 106:19126–19131 [CrossRef]
    [Google Scholar]
  37. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M et al. Versatile and open software for comparing large genomes. Genome Biol 2004; 5:R12 [CrossRef]
    [Google Scholar]
  38. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [CrossRef]
    [Google Scholar]
  39. Tindall BJ. Lipid composition of Halobacterium lacusprofundi . FEMS Microbiol Lett 1990a; 66:199–202 [CrossRef]
    [Google Scholar]
  40. Tindall BJ. A comparative study of the lipid composition of Halobacterium saccharovorum from various sources. Syst Appl Microbiol 1990b; 13:128–130 [CrossRef]
    [Google Scholar]
  41. Altenburgera P, Kämpferb P, Makristathisc A, Lubitza W, Bussea H-J. Classification of bacteria isolated from a medieval wall painting. J Biotechnol 1996; 47:39–52 [CrossRef]
    [Google Scholar]
  42. Busse J, Auling G. Polyamine pattern as a chemotaxonomic marker within the Proteobacteria . Syst Appl Microbiol 1988; 11:1–8 [CrossRef]
    [Google Scholar]
  43. Busse H-J, Bunka S, Hensel A, Lubitz W. Discrimination of members of the family Pasteurellaceae based on polyamine patterns. Int J Syst Evol Microbiol 1997; 47:698–708 [CrossRef]
    [Google Scholar]
  44. Stolz A, Busse H-J, Kämpfer P. Pseudomonas knackmussii sp. nov. Int J Syst Evol Microbiol 2007; 57:572–576 [CrossRef]
    [Google Scholar]
  45. Wayne LG, Moore WEC, Stackebrandt E, Kandler O, Colwell RR et al. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Evol Microbiol 1987; 37:463–464 [CrossRef]
    [Google Scholar]
  46. Rosselló-Mora R, Amann R. The species concept for prokaryotes. FEMS Microbiol Rev 2001; 25:39–67 [CrossRef]
    [Google Scholar]
  47. Parte AC. LPSN—list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 2014; 42:D613–D616 [CrossRef]
    [Google Scholar]
  48. Stackebrandt E, Goebel BM. Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Evol Microbiol 1994; 44:846–849 [CrossRef]
    [Google Scholar]
  49. Stackebrandt E, Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiology Today 2006; 33:152–155
    [Google Scholar]
  50. Kim M, Oh H-S, Park S-C, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [CrossRef]
    [Google Scholar]
  51. Tindall BJ, Busse H-J, Ludwig W, Rosselló-Móra R, Kämpfer P. Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 2010; 60:249–266 [CrossRef]
    [Google Scholar]
  52. Hollis DG, Weaver RE, Steigerwalt AG, Wenger JD, Moss CW et al. Francisella philomiragia comb. nov. (formerly Yersinia philomiragia) and Francisella tularensis biogroup novicida (formerly Francisella novicida) associated with human disease. J Clin Microbiol 1989; 27:1601–1608 [CrossRef]
    [Google Scholar]
  53. Mikalsen J, Colquhoun DJ. Francisella asiatica sp. nov. isolated from farmed tilapia (Oreochromis sp.) and elevation of Francisella philomiragia subsp. noatunensis to species rank as Francisella noatunensis comb. nov., sp. nov . Int J Syst Evol Microbiol 2009 [CrossRef]
    [Google Scholar]
  54. Ottem KF. Francisella noatunensis taxonomy and ecology Bergen, Norway: PhD Thesis, University of Bergen; 2011
    [Google Scholar]
  55. Ramasamy D, Mishra AK, Lagier J-C, Padhmanabhan R, Rossi M et al. A polyphasic strategy incorporating genomic data for the taxonomic description of novel bacterial species. Int J Syst Evol Microbiol 2014; 64:384–391 [CrossRef]
    [Google Scholar]
  56. Ciufo S, Kannan S, Sharma S, Badretdin A, Clark K et al. Using average nucleotide identity to improve taxonomic assignments in prokaryotic genomes at the NCBI. Int J Syst Evol Microbiol 2018; 68:2386–2392 [CrossRef]
    [Google Scholar]
  57. Dietrich EA, Kingry LC, Kugeler KJ, Levy C, Yaglom H et al. Francisella opportunistica sp. nov., isolated from human blood and cerebrospinal fluid. Int J Syst Evol Microbiol 2019; 70: 20 Dec 2019 [CrossRef]
    [Google Scholar]
  58. PH Q, Chen SY, Scholz HC, Busse HJ, Gu Q et al. Francisella guangzhouensis sp. nov., isolated from air-conditioning systems. Int J Syst Evol Microbiol 2013; 63:3628–3635
    [Google Scholar]
  59. Parker CT, Tindall BJ, Garrity GM. International Code of Nomenclature of bacteria, bacteriological Code (2008 revision). Int J Syst Evol Microbiol 2016; 66:
    [Google Scholar]
  60. Oren A, Garrity G. Proposal to emend rules 50a and 50b of the International Code of Nomenclature of prokaryotes. Int J Syst Evol Microbiol 2018; 68:3371–3376 [CrossRef]
    [Google Scholar]
  61. Birkbeck TH, Bordevik M, Frøystad MK, Baklien Å. Identification of Francisella sp. from Atlantic salmon, Salmo salar L., in Chile. J Fish Dis 2007; 30:505–507 [CrossRef]
    [Google Scholar]
  62. Birkbeck TH. Chapter 1.4 Francisellosis. In Avendaño-Herrera R. editor Enfermedades infecciosas del cultivo de salmonidos en Chile y el mundo, First Edition. Puerto Varas: Nivas-Chile; 2011 pp 115–130
    [Google Scholar]
  63. Bohle H, Tapia E, Martínez A, Rozas M, Figueroa A et al. Francisella philomiragia, a bacteria associated with high mortalities in Atlantic salmon (Salmo salar) cage farmed in Llanquihue lake. Arch Med Vet 2009; 41:237–244
    [Google Scholar]
  64. Cvitanich J, Gárate O, Silva C, Andrade M, Figueroa C et al. Isolation of a new rickettsia-like organism from Atlantic salmon in Chile. FHS/AFS newsletter 1995; 23:1–3
    [Google Scholar]
  65. Enríquez R, Monras M, Ceballos A, Igor C. First isolation of RLO (rickettsia-like organism) from Galaxias maculatus (puye). Arch Med Vet 1998; 30:233–234
    [Google Scholar]
  66. Oyarzún R, Vargas-Lagos C, Martínez D, Muñoz JLP, Dantagnan LP et al. The effects of intraperitoneal administration of Francisella noatunensis subsp. noatunensis on hepatic intermediary metabolism and indicators of stress in Patagonian blennie Eleginops maclovinus . Comp Biochem Physiol B Biochem Mol Biol 2019; 230:48–56 [CrossRef]
    [Google Scholar]
  67. Vargas-Lagos C, Martínez D, Oyarzún R, Avendaño-Herrera R, Yáñez AJ et al. High doses of Francisella noatunensis induces an immune response in Eleginops maclovinus . Fish Shellfish Immunol 2019; 90:1–11 [CrossRef]
    [Google Scholar]
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