1887

Abstract

A Gram-stain-negative or -positive, strictly anaerobic, non-spore-forming and pleomorphic bacterium (designated 14-104) was isolated from the saliva sample of a patient with oral squamous cell carcinoma. It was an acid-tolerant neutralophilic mesophile, growing at between 20 and 40 °C (with optimum growth at 30 °C) and pH between pH 3.0 and 7.0 (with optimum growth at pH 6.0–7.0). It contained anteiso-C and C as the major fatty acids. The genome size of strain 14-104 was 2.98 Mbp, and the G+C content was 39.6 mol%. It shared <87 % 16S rRNA sequence similarity, <71 % orthologous average nucleotide identity, <76 % average amino acid identity and <68 %% of conserved proteins with its closest relative, CCUG 55929. Reconstruction of phylogenetic and phylogenomic trees revealed that strain 14-104 and CCUG 55929 were clustered as a distinct clade without any other terminal node. The phylogenetic and phylogenomic analyses along with physiological and chemotaxonomic data indicated that strain 14-104 represents a novel species in the genus , for which the name sp. nov. is proposed. The type strain is 14-104 (=BCRC 81305= NBRC 115041).

Funding
This study was supported by the:
  • Ministry of Science and Technology, Taiwan (Award 108-2221-E-006 -160 -MY3)
    • Principle Award Recipient: Jer-HorngWu
  • Ministry of Science and Technology, Taiwan (Award 108-2321-B-006-010)
    • Principle Award Recipient: Li-WhaWu
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.005703
2023-02-06
2024-12-06
Loading full text...

Full text loading...

References

  1. Zafar H, Saier MH. Gut bacteroides species in health and disease. Gut Microbes 2021; 13:1–20 [View Article]
    [Google Scholar]
  2. Al Masalma M, Raoult D, Roux V. Phocaeicola abscessus gen. nov., sp. nov., an anaerobic bacterium isolated from a human brain abscess sample. Int J Syst Evol Microbiol 2009; 59:2232–2237 [View Article]
    [Google Scholar]
  3. García-López M, Meier-Kolthoff JP, Tindall BJ, Gronow S, Woyke T et al. Analysis of 1,000 type-strain genomes improves taxonomic classification of Bacteroidetes. Front Microbiol 2019; 10:2083 [View Article]
    [Google Scholar]
  4. Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M. List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 2020; 70:5607–5612 [View Article] [PubMed]
    [Google Scholar]
  5. Kitahara M, Sakamoto M, Ike M, Sakata S, Benno Y. Bacteroides plebeius sp. nov. and Bacteroides coprocola sp. nov., isolated from human faeces. Int J Syst Evol Microbiol 2005; 55:2143–2147 [View Article] [PubMed]
    [Google Scholar]
  6. Hayashi H, Shibata K, Bakir MA, Sakamoto M, Tomita S et al. Bacteroides coprophilus sp. nov., isolated from human faeces. Int J Syst Evol Microbiol 2007; 57:1323–1326 [View Article] [PubMed]
    [Google Scholar]
  7. Bakir MA, Sakamoto M, Kitahara M, Matsumoto M, Benno Y. Bacteroides dorei sp. nov., isolated from human faeces. Int J Syst Evol Microbiol 2006; 56:1639–1643 [View Article] [PubMed]
    [Google Scholar]
  8. Eggerth AH, Gagnon BH. The bacteroides of human feces. J Bacteriol 1933; 25:389–413 [View Article]
    [Google Scholar]
  9. Hitch TCA, Riedel T, Oren A, Overmann J, Lawley TD et al. Automated analysis of genomic sequences facilitates high-throughput and comprehensive description of bacteria. ISME COMMUN 2021; 1: [View Article]
    [Google Scholar]
  10. Kitahara M, Tsuchida S, Kawasumi K, Amao H, Sakamoto M et al. Bacteroides chinchillae sp. nov. and Bacteroides rodentium sp. nov., isolated from chinchilla (Chinchilla lanigera) faeces. Int J Syst Evol Microbiol 2011; 61:877–881 [View Article]
    [Google Scholar]
  11. Choi JY, Choi S-H, Park J-E, Kim J-S, Lee J et al. Phocaeicola faecicola sp. nov., isolated from porcine faeces. Int J Syst Evol Microbiol 2021; 71: [View Article] [PubMed]
    [Google Scholar]
  12. Lan PTN, Sakamoto M, Sakata S, Benno Y. Bacteroides barnesiae sp. nov., Bacteroides salanitronis sp. nov. and Bacteroides gallinarum sp. nov., isolated from chicken caecum. Int J Syst Evol Microbiol 2006; 56:2853–2859 [View Article] [PubMed]
    [Google Scholar]
  13. Clavel T, Saalfrank A, Charrier C, Haller D. Isolation of bacteria from mouse caecal samples and description of Bacteroides sartorii sp. nov. Arch Microbiol 2010; 192:427–435 [View Article] [PubMed]
    [Google Scholar]
  14. Fenner L, Roux V, Mallet MN, Raoult D. Bacteroides massiliensis sp. nov., isolated from blood culture of a newborn. Int J Syst Evol Microbiol 2005; 55:1335–1337 [View Article] [PubMed]
    [Google Scholar]
  15. Ueki A, Abe K, Ohtaki Y, Kaku N, Watanabe K et al. Bacteroides paurosaccharolyticus sp. nov., isolated from a methanogenic reactor treating waste from cattle farms. Int J Syst Evol Microbiol 2011; 61:448–453 [View Article] [PubMed]
    [Google Scholar]
  16. Yoshida N, Emoto T, Yamashita T, Watanabe H, Hayashi T et al. Bacteroides vulgatus and Bacteroides dorei reduce gut microbial lipopolysaccharide production and inhibit atherosclerosis. Circulation 2018; 138:2486–2498 [View Article]
    [Google Scholar]
  17. Yuan S, Shen J. Bacteroides vulgatus diminishes colonic microbiota dysbiosis ameliorating lumbar bone loss in ovariectomized mice. Bone 2021; 142:115710 [View Article]
    [Google Scholar]
  18. Feng Q, Liang S, Jia H, Stadlmayr A, Tang L et al. Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat Commun 2015; 6:6528 [View Article]
    [Google Scholar]
  19. Lundmark A, Hu YOO, Huss M, Johannsen G, Andersson AF et al. Identification of salivary microbiota and its association with host inflammatory mediators in periodontitis. Front Cell Infect Microbiol 2019; 9:216 [View Article]
    [Google Scholar]
  20. Camelo-Castillo AJ, Mira A, Pico A, Nibali L, Henderson B et al. Subgingival microbiota in health compared to periodontitis and the influence of smoking. Front Microbiol 2015; 6:119 [View Article]
    [Google Scholar]
  21. Chen C, Hemme C, Beleno J, Shi ZJ, Ning D et al. Oral microbiota of periodontal health and disease and their changes after nonsurgical periodontal therapy. ISME J 2018; 12:1210–1224 [View Article] [PubMed]
    [Google Scholar]
  22. Wang L, Yin G, Guo Y, Zhao Y, Zhao M et al. Variations in oral microbiota composition are associated with a risk of throat cancer. Front Cell Infect Microbiol 2019; 9:205 [View Article]
    [Google Scholar]
  23. Herreros-Pomares A, Llorens C, Soriano B, Zhang F, Gallach S et al. Oral microbiome in proliferative Verrucous leukoplakia exhibits loss of diversity and enrichment of pathogens. Oral Oncol 2021; 120:105404 [View Article] [PubMed]
    [Google Scholar]
  24. Chen JW, Wu JH, Chiang WF, Chen YL, Wu WS et al. Taxonomic and functional dysregulation in salivary microbiomes during oral carcinogenesis. Front Cell Infect Microbiol 2021; 11:663068 [View Article]
    [Google Scholar]
  25. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  26. 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]
  27. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article]
    [Google Scholar]
  28. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
    [Google Scholar]
  29. Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 2019; 47:D309–D314 [View Article]
    [Google Scholar]
  30. Galperin MY, Mekhedov SL, Puigbo P, Smirnov S, Wolf YI et al. Genomic determinants of sporulation in Bacilli and Clostridia: towards the minimal set of sporulation-specific genes. Environ Microbiol 2012; 14:2870–2890 [View Article]
    [Google Scholar]
  31. Swoboda JG, Campbell J, Meredith TC, Walker S. Wall teichoic acid function, biosynthesis, and inhibition. Chembiochem 2010; 11:35–45 [View Article] [PubMed]
    [Google Scholar]
  32. Liu B, Zheng D, Jin Q, Chen L, Yang J. VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res 2019; 47:D687–D692 [View Article] [PubMed]
    [Google Scholar]
  33. Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 2020; 48:D517–D525 [View Article] [PubMed]
    [Google Scholar]
  34. Eijkelkamp BA, McDevitt CA, Kitten T. Manganese uptake and streptococcal virulence. Biometals 2015; 28:491–508 [View Article] [PubMed]
    [Google Scholar]
  35. van der Ploeg JR, Giertsen E, Lüdin B, Mörgeli C, Zinkernagel AS et al. Quantitative detection of Porphyromonas gingivalis fimA genotypes in dental plaque. FEMS Microbiol Lett 2004; 232:31–37 [View Article] [PubMed]
    [Google Scholar]
  36. Cosentino S, Voldby Larsen M, Møller Aarestrup F, Lund O. PathogenFinder–distinguishing friend from foe using bacterial whole genome sequence data. PLoS One 2013; 8:e77302 [View Article]
    [Google Scholar]
  37. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004; 5:113 [View Article] [PubMed]
    [Google Scholar]
  38. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009; 25:1972–1973 [View Article] [PubMed]
    [Google Scholar]
  39. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 2020; 37:1530–1534 [View Article]
    [Google Scholar]
  40. Abadi S, Azouri D, Pupko T, Mayrose I. Model selection may not be a mandatory step for phylogeny reconstruction. Nat Commun 2019; 10:934 [View Article]
    [Google Scholar]
  41. Minh BQ, Nguyen MAT, von Haeseler A. Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 2013; 30:1188–1195 [View Article] [PubMed]
    [Google Scholar]
  42. Eaton DAR, Matschiner M. Toytree: a minimalist tree visualization and manipulation library for Python. Methods Ecol Evol 2020; 11:187–191 [View Article]
    [Google Scholar]
  43. Irisawa T, Saputra S, Kitahara M, Sakamoto M. Sulistiani et al. Bacteroides caecicola sp. nov. and Bacteroides gallinaceum sp. nov., isolated from the caecum of an Indonesian chicken. Int J Syst Evol Microbiol 2016; 66:1431–1437 [View Article]
    [Google Scholar]
  44. Saputra S, Irisawa T, Sakamoto M, Kitahara M. Sulistiani et al. Bacteroides caecigallinarum sp. nov., isolated from caecum of an Indonesian chicken. Int J Syst Evol Microbiol 2015; 65:4341–4346 [View Article]
    [Google Scholar]
  45. Lee MD. GToTree: a user-friendly workflow for phylogenomics. Bioinformatics 2019; 35:4162–4164 [View Article] [PubMed]
    [Google Scholar]
  46. Eddy SR. Accelerated profile HMM searches. PLoS Comput Biol 2011; 7:10 [View Article]
    [Google Scholar]
  47. 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 [View Article] [PubMed]
    [Google Scholar]
  48. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 2017; 14:587–589 [View Article] [PubMed]
    [Google Scholar]
  49. Chernomor O, von Haeseler A, Minh BQ. Terrace aware data structure for phylogenomic inference from supermatrices. Syst Biol 2016; 65:997–1008 [View Article]
    [Google Scholar]
  50. 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 [View Article] [PubMed]
    [Google Scholar]
  51. Lee I, Ouk Kim Y, Park SC, Chun J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103 [View Article]
    [Google Scholar]
  52. Kim D, Park S, Chun J. Introducing EzAAI: a pipeline for high throughput calculations of prokaryotic average amino acid identity. J Microbiol 2021; 59:476–480 [View Article] [PubMed]
    [Google Scholar]
  53. Qin Q-L, Xie B-B, Zhang X-Y, Chen X-L, Zhou B-C et al. A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 2014; 196:2210–2215 [View Article] [PubMed]
    [Google Scholar]
  54. 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] [PubMed]
    [Google Scholar]
  55. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article] [PubMed]
    [Google Scholar]
  56. Barco RA, Garrity GM, Scott JJ, Amend JP, Nealson KH et al. A genus definition for bacteria and archaea based on a standard genome relatedness index. mBio 2020; 11: [View Article]
    [Google Scholar]
  57. Konstantinidis KT, Rosselló-Móra R, Amann R. Uncultivated microbes in need of their own taxonomy. ISME J 2017; 11:2399–2406 [View Article] [PubMed]
    [Google Scholar]
  58. Bewick V, Cheek L, Ball J. Statistics review 13: receiver operating characteristic curves. Crit Care 2004; 8:508–512 [View Article] [PubMed]
    [Google Scholar]
  59. Aliyu H, Lebre P, Blom J, Cowan D, De Maayer P. Phylogenomic re-assessment of the thermophilic genus Geobacillus. Syst Appl Microbiol 2016; 39:527–533 [View Article] [PubMed]
    [Google Scholar]
  60. Xu Z, Masuda Y, Hayakawa C, Ushijima N, Kawano K et al. Description of three novel members in the family Geobacteraceae, Oryzomonas japonicum gen. nov., sp. nov., Oryzomonas sagensis sp. nov., and Oryzomonas ruber sp. nov. Microorganisms 2020; 8:634 [View Article]
    [Google Scholar]
  61. Li Y, Xue H, Sang SQ, Lin CL, Wang XZ. Phylogenetic analysis of family Neisseriaceae based on genome sequences and description of Populibacter corticis gen. nov., sp. nov., a member of the family Neisseriaceae, isolated from symptomatic bark of Populus × euramericana canker. PLoS One 2017; 12:e0174506 [View Article]
    [Google Scholar]
  62. Ma T, Xue H, Piao C, Liu C, Yang M et al. Reclassification of 11 members of the family Rhodobacteraceae at genus and species levels and proposal of Pseudogemmobacter hezensis sp. nov. Front Microbiol 2022; 13:849695 [View Article]
    [Google Scholar]
  63. Wirth JS, Whitman WB. Phylogenomic analyses of a clade within the Roseobacter group suggest taxonomic reassignments of species of the genera Aestuariivita, Citreicella, Loktanella, Nautella, Pelagibaca, Ruegeria, Thalassobius, Thiobacimonas and Tropicibacter, and the proposal of six novel genera. Int J Syst Evol Microbiol 2018; 68:2393–2411 [View Article] [PubMed]
    [Google Scholar]
  64. Shin Y, Park S-J, Paek J, Kim J-S, Rhee M-S et al. Bacteroides koreensis sp. nov. and Bacteroides kribbi sp. nov., two new members of the genus Bacteroides. Int J Syst Evol Microbiol 2017; 67:4352–4357 [View Article] [PubMed]
    [Google Scholar]
  65. Smith AC, Hussey MA. Gram stain protocols. Am Soc Microbiol 2005; 1:14
    [Google Scholar]
  66. Tripathi N, Sapra A. Gram staining. In Statpearls Treasure Island FL: StatPearls Publishing; 2021
    [Google Scholar]
  67. Sutcliffe IC. A phylum level perspective on bacterial cell envelope architecture. Trends Microbiol 2010; 18:464–470 [View Article] [PubMed]
    [Google Scholar]
  68. Meriläinen L, Herranen A, Schwarzbach A, Gilbert L. Morphological and biochemical features of Borrelia burgdorferi pleomorphic forms. Microbiology 2015; 161:516–527 [View Article]
    [Google Scholar]
  69. Kell AJ, Stewart G, Ryan S, Peytavi R, Boissinot M et al. Vancomycin-modified nanoparticles for efficient targeting and preconcentration of Gram-positive and Gram-negative bacteria. ACS Nano 2008; 2:1777–1788 [View Article] [PubMed]
    [Google Scholar]
  70. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 1990; 20:16
    [Google Scholar]
  71. Hahnke RL, Meier-Kolthoff JP, García-López M, Mukherjee S, Huntemann M et al. Genome-based taxonomic classification of Bacteroidetes. Front Microbiol 2016; 7:2003 [View Article]
    [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.005703
Loading
/content/journal/ijsem/10.1099/ijsem.0.005703
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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