1887

Abstract

Eight genetically related, Gram-negative bacterial strains, isolated from clinical specimens between 2012 and 2016, were submitted to Laboratories for species identification. The lack of species- or genus-level matches in curated 16S rRNA gene databases prompted us to undertake the polyphasic characterization of these so far undescribed organisms. Six isolates available for additional testing were oxidase negative, catalase positive, pleomorphic, Gram-negative rods displaying temperature-dependent motility and producing yellow-pigmented colonies with three distinct morphotypes: medium-sized shiny, large mucoid and agar-pitting. Biochemical reactions and sugar fermentation patterns were most similar to members of the genus . Fatty acid profiles were highly similar across all six organisms, with the major components being: C; C cyclo; C 3-OH/iso-C I; C ω7; and C ω7/C ω6. Whole-genome comparisons and multi locus sequence analysis (using the coding genes , , and ) suggest that the strains here described constitute three individual species within a novel genus related to the family . We propose for this novel taxon the name gen. nov., referring to the presentation of multiple characteristics typical of distinct genera within a single organism. Four isolates are representative of a single species: sp. nov (2016-Iso1, 2016-Iso2, type strain 2016-Iso3=DSM 110101=ATCC TSD-180 and 2013-Iso5). The remaining two isolates constitute the novel species sp. nov. (type strain 2016-Iso4=DSM 110102=ATCC TSD-182) and sp. nov. (type strain 2015-Iso6=DSM 110100=ATCC TSD-181). Our work provides the first formal characterization of the genus and forms the basis to study its taxonomic diversity.

Funding
This study was supported by the:
  • ARUP Institute for Clinical and Experimental Pathology (US) (Award NA)
    • Principle Award Recipient: Alessandro Rossi
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004094
2020-03-06
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/70/4/2703.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004094&mimeType=html&fmt=ahah

References

  1. Petti CA. Detection and identification of microorganisms by gene amplification and sequencing. Clin Infect Dis 2007; 44:1108–1114 [View Article]
    [Google Scholar]
  2. Schlaberg R, Simmon KE, Fisher MA. A systematic approach for discovering novel, clinically relevant bacteria. Emerg Infect Dis 2012; 18:422–430 [View Article]
    [Google Scholar]
  3. Tindall BJ, Rosselló-Móra R, Busse H-J, Ludwig W, Kämpfer P. Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 2010; 60:249–266 [View Article]
    [Google Scholar]
  4. Sasser M. Bacterial identification by gas chromatography analysis of fatty acids methyl esters GC-FAME, MIDI internal document (Last Revised 2006). Technical note #101; 1990
    [Google Scholar]
  5. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article]
    [Google Scholar]
  6. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article]
    [Google Scholar]
  7. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. Ncbi prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article]
    [Google Scholar]
  8. Arndt D, Grant JR, Marcu A, Sajed T, Pon A et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 2016; 44:W16–W21 [View Article]
    [Google Scholar]
  9. Sedkova N, Tao L, Rouvière PE, Cheng Q. Diversity of carotenoid synthesis gene clusters from environmental Enterobacteriaceae strains. Appl Environ Microbiol 2005; 71:8141–8146 [View Article]
    [Google Scholar]
  10. Lehner A, Grimm M, Rattei T, Ruepp A, Frishman D et al. Cloning and characterization of Enterobacter sakazakii pigment genes and in situ spectroscopic analysis of the pigment. FEMS Microbiol Lett 2006; 265:244–248 [View Article]
    [Google Scholar]
  11. Zhang W, Hu X, Wang L, Wang X. Reconstruction of the carotenoid biosynthetic pathway of Cronobacter sakazakii BAA894 in Escherichia coli. PLoS One 2014; 9:e86739 [View Article]
    [Google Scholar]
  12. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article]
    [Google Scholar]
  13. Mlaga KD, Lotte R, Montaudié H, Rolain J-M, Ruimy R. 'Nissabacter archeti' gen. nov., sp. nov., a new member of Enterobacteriaceae family, isolated from human sample at Archet 2 Hospital, Nice, France. New Microbes New Infect 2017; 17:81–83 [View Article]
    [Google Scholar]
  14. Brady C, Cleenwerck I, Venter S, Coutinho T, De Vos P. Taxonomic evaluation of the genus Enterobacter based on multilocus sequence analysis (MLSA): proposal to reclassify E. nimipressuralis and E. amnigenus into Lelliottia gen. nov. as Lelliottia nimipressuralis comb. nov. and Lelliottia amnigena comb. nov., respectively, E. gergoviae and E. pyrinus into Pluralibacter gen. nov. as Pluralibacter gergoviae comb. nov. and Pluralibacter pyrinus comb. nov., respectively, E. cowanii, E. radicincitans, E. oryzae and E. arachidis into Kosakonia gen. nov. as Kosakonia cowanii comb. nov., Kosakonia radicincitans comb. nov., Kosakonia oryzae comb. nov. and Kosakonia arachidis comb. nov., respectively, and E. turicensis, E. helveticus and E. pulveris into Cronobacter as Cronobacter zurichensis nom. nov., Cronobacter helveticus comb. nov. and Cronobacter pulveris comb. nov., respectively, and emended description of the genera Enterobacter and Cronobacter. Syst Appl Microbiol 2013; 36:309–319 [View Article]
    [Google Scholar]
  15. Adeolu M, Alnajar S, Naushad S, S Gupta R. Genome-based phylogeny and taxonomy of the 'Enterobacteriales': proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol 2016; 66:5575–5599 [View Article]
    [Google Scholar]
  16. Hurst MRH, Beattie A, Altermann E, Moraga RM, Harper LA et al. The draft genome sequence of the Yersinia entomophaga entomopathogenic type strain MH96T. Toxins 2016; 8:143 11 05 2016 [View Article]
    [Google Scholar]
  17. Daligault HE, Davenport KW, Minogue TD, Bishop-Lilly KA, Broomall SM et al. Whole-Genome Yersinia sp. assemblies from 10 diverse strains. Genome Announc 2014; 2:e01055-14 23 10 2014 [View Article]
    [Google Scholar]
  18. Brady C, Hunter G, Kirk S, Arnold D, Denman S. Rahnella victoriana sp. nov., Rahnella bruchi sp. nov., Rahnella woolbedingensis sp. nov., classification of Rahnella genomospecies 2 and 3 as Rahnella variigena sp. nov. and Rahnella inusitata sp. nov., respectively and emended description of the genus Rahnella. Syst Appl Microbiol 2014; 37:545–552 [View Article]
    [Google Scholar]
  19. Brady CL, Cleenwerck I, Venter SN, Engelbeen K, De Vos P et al. Emended description of the genus Pantoea, description of four species from human clinical samples, Pantoea septica sp. nov., Pantoea eucrina sp. nov., Pantoea brenneri sp. nov. and Pantoea conspicua sp. nov., and transfer of Pectobacterium cypripedii (Hori 1911) Brenner et al. 1973 emend. Hauben et al. 1998 to the genus as Pantoea cypripedii comb. nov. Int J Syst Evol Microbiol 2010; 60:2430–2440 [View Article]
    [Google Scholar]
  20. Brady C, Cleenwerck I, Venter S, Vancanneyt M, Swings J et al. Phylogeny and identification of Pantoea species associated with plants, humans and the natural environment based on multilocus sequence analysis (MLSA). Syst Appl Microbiol 2008; 31:447–460 [View Article]
    [Google Scholar]
  21. Spröer C, Mendrock U, Swiderski J, Lang E, Stackebrandt E. The phylogenetic position of Serratia, Buttiauxella and some other genera of the family Enterobacteriaceae. Int J Syst Bacteriol 1999; 49 Pt 4:1433–1438 [View Article]
    [Google Scholar]
  22. Lang E, Schumann P, Knapp BA, Kumar R, Spröer C et al. Budvicia diplopodorum sp. nov. and emended description of the genus Budvicia. Int J Syst Evol Microbiol 2013; 63:260–267 [View Article]
    [Google Scholar]
  23. Fanjat N, Leclercq A, Joosten H, Robichon D. Comparison of the phenotyping methods ID 32E and Vitek 2 compact GN with 16S rRNA gene sequencing for the identification of Enterobacter sakazakii. J Clin Microbiol 2007; 45:2048–2050 [View Article]
    [Google Scholar]
  24. Stephan R, Lehner A, Tischler P, Rattei T. Complete genome sequence of Cronobacter turicensis LMG 23827, a food-borne pathogen causing deaths in neonates. J Bacteriol 2011; 193:309–310 [View Article]
    [Google Scholar]
  25. Yarza P, Spröer C, Swiderski J, Mrotzek N, Spring S et al. 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 2013; 36:69–73 [View Article]
    [Google Scholar]
  26. Boye K, Hansen DS. Sequencing of 16S rDNA of Klebsiella: taxonomic relations within the genus and to other Enterobacteriaceae. Int J Med Microbiol 2003; 292:495–503 [View Article]
    [Google Scholar]
  27. Kim W, Song M-O, Song W, Kim K-J, Chung S-I et al. Comparison of 16S rDNA analysis and rep-PCR genomic fingerprinting for molecular identification of Yersinia pseudotuberculosis. Antonie Van Leeuwenhoek 2003; 83:125–133 [View Article]
    [Google Scholar]
  28. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008; 36:W465–W469 [View Article]
    [Google Scholar]
  29. Edgar RC. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article]
    [Google Scholar]
  30. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000; 17:540–552 [View Article]
    [Google Scholar]
  31. Gascuel O. BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 1997; 14:685–695 [View Article]
    [Google Scholar]
  32. Chevenet F, Brun C, Bañuls A-L, Jacq B, Christen R. TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 2006; 7:439 [View Article]
    [Google Scholar]
  33. Chun J, Rainey FA. Integrating genomics into the taxonomy and systematics of the bacteria and archaea. Int J Syst Evol Microbiol 2014; 64:316–324 [View Article]
    [Google Scholar]
  34. Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 2017; 110:1281–1286 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004094
Loading
/content/journal/ijsem/10.1099/ijsem.0.004094
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

MOVIE

Supplementary material 3

MOVIE
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error