Skip to main content
Log in

Genomic and phylogenomic analysis of Fusobacteriaceae family and proposal to reclassify Fusobacterium naviforme Jungano 1909 into a novel genus as Zandiella naviformis gen. nov., comb. nov. and reclassification of Fusobacterium necrophorum subsp. funduliforme as later heterotypic synonym of Fusobacterium necrophorum subsp. necrophorum and Fusobacterium equinum as later heterotypic synonym of Fusobacterium gonidiaformans

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

The family Fusobacteriaceae is a large family within the phylum Fusobacteriota. The reclassification of F. naviforme as Zandiella naviformis gen. nov., comb. nov. is proposed because of the separate and distinct phylogenetic situation on the basis of the results of 16S rRNA gene sequence analysis, the genetic and genomic differences from all other species and subspecies in the Fusobacteriaceae family. The type strain is ATCC 25832; CCUG 50052; NCTC 13121. In phylogenetic trees drawn using complete genome sequences and 16S rRNA gene sequences, F. necrophorum subsp. funduliforme and F. equinum were clades together with F. necrophorum subsp. necrophorum and F. gonidiaformans, respectively. The average nucleotide identity, average amino acid identity, and digital DNA–DNA hybridization values between themes exceeded the cut-off values for species delineation. Based on these results, F. necrophorum subsp. funduliforme and F. equinum should be reclassified as later heterotypic synonyms of F. necrophorum subsp. necrophorum and F. gonidiaformans, respectively.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anonymous (1991) Int J Syst Bacteriol 41:456–8

  • Brazier JS (2006) Human infections with Fusobacterium necrophorum. Anaerobe 12(4):165–172

    Article  PubMed  Google Scholar 

  • Brook I (2007) Anaerobic infections: diagnosis and management. CRC Press, Lonon

    Book  Google Scholar 

  • Brook I, Frazier EH (1993) Anaerobic osteomyelitis and arthritis in a military hospital: a 10-year experience. Am J Med 94(1):21–28

    Article  CAS  PubMed  Google Scholar 

  • Brook I, Hausfeld JN (2011) Microbiology of acute and chronic maxillary sinusitis in smokers and nonsmokers. Annal Otol Rhinol Laryngol 120(11):707–712

    Article  Google Scholar 

  • Brune A, Evers S, Kaim G, Ludwig W, Schink B (2002) Ilyobacter insuetus sp. nov., a fermentative bacterium specialized in the degradation of hydroaromatic compounds. Int J Syst Evolut Microbiol 52(2):429–432

    Article  CAS  Google Scholar 

  • Carlier J-P, K’ouas G, Han XY (2007) Moryella indoligenes gen. nov., sp. nov., an anaerobic bacterium isolated from clinical specimens. Int J Syst Evolut Microbiol 57(4):725–729

    Article  CAS  Google Scholar 

  • Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS et al (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68(1):461–466

    Article  CAS  PubMed  Google Scholar 

  • Citron DM (2002) Update on the taxonomy and clinical aspects of the genus Fusobacterium. Clinic Infect Dis 35(Supplement_1):S22–S27

    Article  Google Scholar 

  • Collins M, Shah H (1986) Reclassification of Bacteroides termitidis Sebald (Holdeman and Moore) in a New Genus Sebaldella, as Sebaldella termitidis comb. nov. Int J Syst Evolut Microbiol 36(2):349–350

    Google Scholar 

  • Collins MD, Hoyles L, Törnqvist E, von Essen R, Falsen E (2001) Characterization of some strains from human clinical sources which resemble “Leptotrichia sanguinegens”: description of Sneathia sanguinegens sp. nov., gen. nov. Syst Appl Microbiol 24(3):358–361

    Article  CAS  PubMed  Google Scholar 

  • Dörner C, Schink B (1990) Clostridium homopropionicum sp. nov., a new strict anaerobe growing with 2-, 3-, or 4-hydroxybutyrate. Arch Microbiol 154:342–348

    Article  PubMed  Google Scholar 

  • Eisenberg T, Kämpfer P, Ewers C, Semmler T, Glaeser SP, Collins E et al (2016) Oceanivirga salmonicida gen. nov., sp. Nov., a member of the Leptotrichiaceae isolated from Atlantic salmon (Salmo salar). Int J Syst Evolut Microbiol 66(6):2429–2437

    Article  CAS  Google Scholar 

  • Eisenberg T, Glaeser SP, Ewers C, Semmler T, Drescher B, Kämpfer P (2016) Caviibacter abscessus gen. nov., sp. nov., a member of the family Leptotrichiaceae isolated from Guinea Pigs (Cavia porcellus). Int J Syst Evolut Microbiol 66(4):1652–1659

    Article  CAS  Google Scholar 

  • Eisenberg T, Glaeser SP, Blom J, Kämpfer P (2020) Proposal to reclassify Leptotrichia goodfellowii into a novel genus as Pseudoleptotrichia goodfellowii gen. nov., comb. nov. Int J Syst Evolut Microbiol 70(3):2084–2088

    Article  CAS  Google Scholar 

  • Eisenberg T, Glaeser SP, Blom J, Kämpfer P (2020) Proposal to reclassify Streptobacillus hongkongensis into a novel genus as Pseudostreptobacillus hongkongensis gen. nov., comb. nov. Int J Syst Evolut Microbiol 70(4):2366–2368

    Article  CAS  Google Scholar 

  • Euzeby J (2012) List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evolut Microbiol 62:1–4

    Article  Google Scholar 

  • Fanourgiakis P, Vekemans M, Georgala A, Daneau D, Vandermies A, Grenier P et al (2003) Febrile neutropenia and Fusobacterium bacteremia: clinical experience with 13 cases. Support Care Cancer 11:332–335

    Article  CAS  PubMed  Google Scholar 

  • Foster G, Ross H, Naylor R, Collins M, Ramos CP, Garayzabal FF et al (1995) Cetobacterium ceti gen. nov., sp. Nov., a new gram-negative obligate anaerobe from sea mammals. Lett Appl Microbiol 21(3):202–206

    Article  CAS  PubMed  Google Scholar 

  • García-López M, Meier-Kolthoff JP, Tindall BJ, Gronow S, Woyke T, Kyrpides NC et al (2019) Analysis of 1000 type-strain genomes improves taxonomic classification of Bacteroidetes. Front Microbiol 10:2083

    Article  PubMed  PubMed Central  Google Scholar 

  • Garrity GM, Holt JG (2001) The road map to the manual. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey's manual of systematic bacteriology, 2nd edn, vol 1. Springer, New York, pp 119–166

  • Gharbia SE, Shah HN (1991) Biochemical properties of Fusobacterium naviforme and phenotypically similar isolates. Lett Appl Microbiol 12(5):177–179

    Article  CAS  Google Scholar 

  • Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57(1):81–91

    Article  CAS  PubMed  Google Scholar 

  • Griffin AT, Christensen D (2014) Fusobacterium spondylodiscitis: case report and literature review. Diagn Microbiol Infect Dis 78(4):491–493

    Article  PubMed  Google Scholar 

  • https://lpsn.dsmz.de/genus/leptotrichia

  • Ingar O (2014) The family fusobacteriaceae. The prokaryotes 109–32

  • Jang SS, Hirsh DC (1994) Characterization, distribution, and microbiological associations of Fusobacterium spp. in clinical specimens of animal origin. J Clinic Microbiol 32(2):384–387

    Article  CAS  Google Scholar 

  • Janssen PH, Harfoot C (1990) Ilyobacter delafieldii sp. nov., a metabolically restricted anaerobic bacterium fermenting PHB. Arch Microbiol 154:253–259

    Article  CAS  Google Scholar 

  • Jeon Y-S, Chung H, Park S, Hur I, Lee J-H, Chun J (2005) jPHYDIT: a JAVA-based integrated environment for molecular phylogeny of ribosomal RNA sequences. Bioinformatics 21(14):3171–3173

    Article  CAS  PubMed  Google Scholar 

  • Justesen US, Skov MN, Knudsen E, Holt HM, Søgaard P, Justesen T (2010) 16S rRNA gene sequencing in routine identification of anaerobic bacteria isolated from blood cultures. J Clin Microbiol 48(3):946–948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim M, Oh H-S, Park S-C, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evolut Microbiol 64(Pt_2):346–351

    Article  CAS  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Konstantinidis KT, Tiedje JM (2005a) Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci 102(7):2567–2572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Konstantinidis KT, Tiedje JM (2005b) Towards a genome-based taxonomy for prokaryotes. J Bacteriol 187(18):6258–6264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kristensen LH, Prag J (2000) Human necrobacillosis, with emphasis on Lemierre’s syndrome. Clin Infect Dis 31(2):524–532

    Article  Google Scholar 

  • Lalucat J, Mulet M, Gomila M, García-Valdés E (2020) Genomics in bacterial taxonomy: impact on the genus Pseudomonas. Genes 11(2):139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Monnier A, Jamet A, Carbonnelle E, Barthod G, Moumile K, Lesage F et al (2008) Fusobacterium necrophorum middle ear infections in children and related complications: report of 25 cases and literature review. Pediatr Infect Dis J 27(7):613–617

    Article  PubMed  Google Scholar 

  • Levaditi C, Nicolau S, Poincloux P (1925) Sur le rôle étiologique de Streptobacillus moniliformis (nov. spec.) dans l’érythème polymorphe aigu septicémique. CR Acad Sci 180:1188–1190

    Google Scholar 

  • Ludwig W, Viver T, Westram R, Gago JF, Bustos-Caparros E, Knittel K et al (2021) Release LTP_12_2020, featuring a new ARB alignment and improved 16S rRNA tree for prokaryotic type strains. Syst Appl Microbiol 44(4):126218

    Article  PubMed  Google Scholar 

  • M K Über die fusospirillare Symbiose, die Gattung Fusobacterium (K.B. Lehmann) und Spirillum sputigenum. Zugleich ein Beitrag zur Bakteriologie der Mundhöhle. II. Mitteilung. Die Gattung Fusobacterium. Zentralblatt für Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene, Abteilung. 1922;89:4–22.

  • Medlar AJ, Törönen P, Holm L (2018) AAI-profiler: fast proteome-wide exploratory analysis reveals taxonomic identity, misclassification and contamination. Nucleic Acids Res 46(W1):W479–W485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meier-Kolthoff JP, Göker M (2019) TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 10(1):2182

    Article  PubMed  PubMed Central  Google Scholar 

  • Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:1–14

    Article  Google Scholar 

  • Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M (2022) TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res 50(D1):D801–D807

    Article  CAS  PubMed  Google Scholar 

  • Moore WECHL (1970) Fusobacterium. In: Cato EP, Cummins CS, Holdeman LV, Johnson JL, Moore WEC, Smibert RM, Smith LDS (eds) Outline of clinical methods in anaerobic bacteriology, 2nd revision. Blacksburg/Virginia, Virginia Polytechnic Institute—Anaerobe Laboratory, pp 45–51

    Google Scholar 

  • Mori T, Ebe T, Takahashi M, Isonuma H, Ikemoto H, Oguri T (1993) Lung abscess: analysis of 66 cases from 1979 to 1991. Intern Med 32(4):278–284

    Article  CAS  PubMed  Google Scholar 

  • Oren A, da Costa MS, Garrity GM, Rainey FA, Rossello-Mora R, Schink B, Sutcliffe I, Trujillo ME, Whitman WB (2015) Proposal to include the rank of phylum in the International Code of Nomenclature of Prokaryotes. Int J Syst Evol Microbiol 65:4284-4287

  • Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci 106(45):19126–19131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J (2016) JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32(6):929–931

    Article  CAS  PubMed  Google Scholar 

  • Roalkvam I, Bredy F, Baumberger T, Pedersen R-B, Steen IH (2015) Hypnocyclicus thermotrophus gen. nov., sp. nov. isolated from a microbial mat in a hydrothermal vent field. Int J Syst Evolut Microbiol 65(Pt12):4521–4525

    Article  CAS  Google Scholar 

  • Schink B (1984) Fermentation of tartrate enantiomers by anaerobic bacteria, and description of two new species of strict anaerobes, Ruminococcus pasteurii and Ilyobacter tartaricus. Arch Microbiol 139:409–414

    Article  CAS  Google Scholar 

  • Schink B, Pfennig N (1982) Propionigenium modestum gen. nov. sp. nov. a new strictly anaerobic, nonsporing bacterium growing on succinate. Arch Microbiol 133:209–216

    Article  CAS  Google Scholar 

  • Shimohata M, Naruse S, Kawasaki S, Watanabe Y, Koyama M, Ito Y et al (2012) Brain abscess due to fusobacterium necrophorum in a patient with convulsion and no signs of meningitis. Rinsho Shinkeigaku Clinic Neurol 52(6):429–432

    Article  Google Scholar 

  • Shinjo T, Fujisawa T, Mitsuoka T (1991) Proposal of two subspecies of Fusobacterium necrophorum (Flügge) Moore and Holdeman: Fusobacterium necrophorum subsp. necrophorum subsp. nov., nom. rev. (ex Flügge 1886), and Fusobacterium necrophorum subsp. funduliforme subsp. nov., nom. rev. (ex Hallé 1898). Int J Syst Evolut Microbiol 41(3):395–397

    CAS  Google Scholar 

  • Skerman VBD, McGowan V, Sneath PHA (1980) Approved lists of bacterial names. Int J Syst Bacteriol 30(1):225–230

    Article  Google Scholar 

  • Stackebrandt E (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155

    Google Scholar 

  • Stieb M, Schink B (1984) A new 3-hydroxybutyrate fermenting anaerobe, Ilyobacter polytropus, gen. nov. sp. nov., possessing various fermentation pathways. Arch Microbiol 140:139–146

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teeling H, Meyerdierks A, Bauer M, Amann R, Glöckner FO (2004) Application of tetranucleotide frequencies for the assignment of genomic fragments. Environ Microbiol 6(9):938–947

    Article  CAS  PubMed  Google Scholar 

  • Thompson CC, Chimetto L, Edwards RA, Swings J, Stackebrandt E, Thompson FL (2013) Microbial genomic taxonomy. BMC Genomics 14(1):1–8

    Article  Google Scholar 

  • Validation list no. 37 (1991) Validation of publication of new names and new combinations previously effectively published outside the IJSB. Int J Syst Bacteriol 41: 331

  • Yarza P, Spröer C, Swiderski J, Mrotzek N, Spring S, Tindall BJ et al (2013) Sequencing orphan species initiative (SOS): filling the gaps in the 16S rRNA gene sequence database for all species with validly published names. Syst Appl Microbiol 36(1):69–73

    Article  CAS  PubMed  Google Scholar 

  • Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H et al (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67(5):1613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J-S, Manno D, Hawari J (2009) Psychrilyobacter atlanticus gen. nov., sp. nov., a marine member of the phylum Fusobacteria that produces H2 and degrades nitramine explosives under low temperature conditions. Int J Syst Evolut Microbiol 59(3):491–497

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

Analysis of data and manuscript propertion

Corresponding author

Correspondence to Mehdi Fatahi-Bafghi.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fatahi-Bafghi, M. Genomic and phylogenomic analysis of Fusobacteriaceae family and proposal to reclassify Fusobacterium naviforme Jungano 1909 into a novel genus as Zandiella naviformis gen. nov., comb. nov. and reclassification of Fusobacterium necrophorum subsp. funduliforme as later heterotypic synonym of Fusobacterium necrophorum subsp. necrophorum and Fusobacterium equinum as later heterotypic synonym of Fusobacterium gonidiaformans. Antonie van Leeuwenhoek 117, 34 (2024). https://doi.org/10.1007/s10482-023-01921-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10482-023-01921-1

Keywords

Navigation