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Volume 73, Issue 10

gen. nov., sp. nov., and sp. nov., gen. nov.: novel bacteria from the family isolated from the female genital tract Open Access

Abstract

Four obligately anaerobic Gram-positive bacteria representing one novel genus and two novel species were isolated from the female genital tract. Both novel species, designated UPII 610-J and KA00274, and an additional isolate of each species were characterized utilizing biochemical, genotypic and phylogenetic analyses. All strains were non-motile and non-spore forming, asaccharolytic, non-cellulolytic and indole-negative coccobacilli. Fatty acid methyl ester analysis for UPII 610-J and KA00274 and additional isolates revealed C, C, Cω9c and Cω6,9c to be the major fatty acids for both species. UPII 610-J had a 16S rRNA gene sequence similarity of 99.4 % to an uncultured clone sequence (AY724740) designated as Bacterial Vaginosis Associated Bacterium 2 (BVAB2). KA00274 had a 16S rRNA gene sequence similarity of 96.5 % to UPII 610-J. Whole genomic DNA mol% G+C content was 42.2 and 39.3 % for UPII 610-JT and KA00274, respectively. Phylogenetic analyses indicate these isolates represent a novel genus and two novel species within the family. We propose the names gen. nov., sp. nov., for UPII 610-J representing the type strain of this species (=DSM 112989, =ATCC TSD-274) and gen. nov., sp. nov., for KA00274 representing the type strain of this species (=DSM 112988, =ATCC TSD-275).

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bacterial vaginosis , BVAB2 , genital tract , human vagina and Oscillospiraceae
Funding
This study was supported by the:
  • National Institutes of Health (Award U19 AI120249)
    • Principle Award Recipient: SharonL. Hillier
  • National Institutes of Health (Award R01 HG005816)
    • Principle Award Recipient: DavidN. Fredricks
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2023-10-03
2024-04-27
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References

  1. Johnson JL, Francis BS. Taxonomy of the Clostridia: ribosomal ribonucleic acid homologies among the species. J Gen Microbiol 1975; 88:229–244 [View Article] [PubMed]
     [Google Scholar]
  2. Collins MD, Lawson PA, Willems A, Cordoba JJ, Fernandez-Garayzabal J et al. The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 1994; 44:812–826 [View Article] [PubMed]
     [Google Scholar]
  3. Rainey FA et al. Family VIII: Ruminococcaceae fam. nov. In DeVos P, Garrity GM, Jones D, Krieg NR, Ludwig W et al. eds Bergey’s Manual of Systemic BacteriologyThe Firmicutes, 2nd. edn vol 3 New York: Springer; 2009 pp 1016–1043
     [Google Scholar]
  4. Yutin N, Galperin MY. A genomic update on clostridial phylogeny: gram-negative spore formers and other misplaced clostridia. Environ Microbiol 2013; 15:2631–2641 [View Article] [PubMed]
     [Google Scholar]
  5. Cruz-Morales P, Orellana CA, Moutafis G, Moonen G, Rincon G et al. Revisiting the evolution and taxonomy of Clostridia, a phylogenomic update. Genome Biol Evol 2019; 11:2035–2044 [View Article] [PubMed]
     [Google Scholar]
  6. Rainey FA. Family VIII. Ruminococcaceae fam. nov. In De Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W et al. eds Bergey’s Manual of Systematic Bacteriology, 2nd edn. vol 3 New York: Springer; p 1016
     [Google Scholar]
  7. Euzéby J. Validation list No.132. Int J Syst Evol Microbiol 2010; 60:469–472
     [Google Scholar]
  8. Zhang X, Tu B, Dai L-R, Lawson PA, Zheng Z-Z et al. Petroclostridium xylanilyticum gen. nov., sp. nov., a xylan-degrading bacterium isolated from an oilfield, and reclassification of clostridial cluster III members into four novel genera in a new Hungateiclostridiaceae fam. nov. Int J Syst Evol Microbiol 2018; 68:3197–3211 [View Article] [PubMed]
     [Google Scholar]
  9. Tindall BJ. The names Hungateiclostridium Zhang et al. 2018, Hungateiclostridium thermocellum (Viljoen et al. 1926) Zhang et al. 2018, Hungateiclostridium cellulolyticum (Patel et al. 1980) Zhang et al. 2018, Hungateiclostridium aldrichii (Yang et al. 1990) Zhang et al. 2018, Hungateiclostridium alkalicellulosi (Zhilina et al. 2006) Zhang et al. 2018, Hungateiclostridium clariflavum (Shiratori et al. 2009) Zhang et al. 2018, Hungateiclostridium straminisolvens (Kato et al. 2004) Zhang et al. 2018 and Hungateiclostridium saccincola (Koeck et al. 2016) Zhang et al. 2018 contravene Rule 51b of the International Code of Nomenclature of Prokaryotes and require replacement names in the genus Acetivibrio Patel et al. 1980. Int J Syst Evol Microbiol 2019; 69:3927–3932 [View Article]
     [Google Scholar]
  10. Fredricks DN, Fiedler TL, Marrazzo JM. Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med 2005; 353:1899–1911 [View Article] [PubMed]
     [Google Scholar]
  11. Fredricks DN, Fiedler TL, Thomas KK, Oakley BB, Marrazzo JM. Targeted PCR for detection of vaginal bacteria associated with bacterial vaginosis. J Clin Microbiol 2007; 45:3270–3276 [View Article] [PubMed]
     [Google Scholar]
  12. Fredricks DN, Fiedler TL, Thomas KK, Mitchell CM, Marrazzo JM. Changes in vaginal bacterial concentrations with intravaginal metronidazole therapy for bacterial vaginosis as assessed by quantitative PCR. J Clin Microbiol 2009; 47:721–726 [View Article] [PubMed]
     [Google Scholar]
  13. Marrazzo JM, Thomas KK, Fiedler TL, Ringwood K, Fredricks DN. Relationship of specific vaginal bacteria and bacterial vaginosis treatment failure in women who have sex with women. Ann Intern Med 2008; 149:20–28 [View Article] [PubMed]
     [Google Scholar]
  14. Marrazzo JM, Thomas KK, Fiedler TL, Ringwood K, Fredricks DN. Risks for acquisition of bacterial vaginosis among women who report sex with women: a cohort study. PLoS One 2010; 5:e11139 [View Article] [PubMed]
     [Google Scholar]
  15. Srinivasan S, Hoffman NG, Morgan MT, Matsen FA, Fiedler TL et al. Bacterial communities in women with bacterial vaginosis: high resolution phylogenetic analyses reveal relationships of microbiota to clinical criteria. PLoS One 2012; 7:e37818 [View Article] [PubMed]
     [Google Scholar]
  16. Fethers K, Twin J, Fairley CK, Fowkes FJI, Garland SM et al. Bacterial Vaginosis (BV) candidate bacteria: associations with BV and behavioural practices in sexually-experienced and inexperienced women. PLoS One 2012; 7:e30633 [View Article] [PubMed]
     [Google Scholar]
  17. Datcu R, Gesink D, Mulvad G, Montgomery-Andersen R, Rink E et al. Vaginal microbiome in women from Greenland assessed by microscopy and quantitative PCR. BMC Infect Dis 2013; 13:480 [View Article]
     [Google Scholar]
  18. Datcu R, Gesink D, Mulvad G, Montgomery-Andersen R, Rink E et al. Bacterial vaginosis diagnosed by analysis of first-void-urine specimens. J Clin Microbiol 2014; 52:218–225 [View Article]
     [Google Scholar]
  19. Hilbert DW, Smith WL, Paulish-Miller TE, Chadwick SG, Toner G et al. Utilization of molecular methods to identify prognostic markers for recurrent bacterial vaginosis. Diagn Microbiol Infect Dis 2016; 86:231–242 [View Article] [PubMed]
     [Google Scholar]
  20. Balle C, Lennard K, Dabee S, Barnabas SL, Jaumdally SZ et al. Endocervical and vaginal microbiota in South African adolescents with asymptomatic Chlamydia trachomatis infection. Sci Rep 2018; 8:11109 [View Article] [PubMed]
     [Google Scholar]
  21. Balkus JE, Srinivasan S, Anzala O, Kimani J, Andac C et al. Impact of periodic presumptive treatment for bacterial vaginosis on the vaginal microbiome among women participating in the preventing vaginal infections trial. J Infect Dis 2017; 215:723–731 [View Article] [PubMed]
     [Google Scholar]
  22. Carter KA, Balkus JE, Anzala O, Kimani J, Hoffman NG et al. Associations between vaginal bacteria and bacterial vaginosis signs and symptoms: a comparative study of Kenyan and American women. Front Cell Infect Microbiol 2022; 12:801770 [View Article] [PubMed]
     [Google Scholar]
  23. Cheng L, Norenhag J, Hu YOO, Brusselaers N, Fransson E et al. Vaginal microbiota and human papillomavirus infection among young Swedish women. NPJ Biofilms Microbiomes 2020; 6:39 [View Article] [PubMed]
     [Google Scholar]
  24. Nelson DB, Hanlon A, Hassan S, Britto J, Geifman-Holtzman O et al. Preterm labor and bacterial vaginosis-associated bacteria among urban women. J Perinat Med 2009; 37:130–134 [View Article] [PubMed]
     [Google Scholar]
  25. Haggerty CL, Ness RB, Totten PA, Farooq F, Tang G et al. Presence and concentrations of select bacterial vaginosis-associated bacteria are associated with increased risk of pelvic inflammatory disease. Sex Transm Dis 2020; 47:344–346 [View Article] [PubMed]
     [Google Scholar]
  26. Lannon SMR, Adams Waldorf KM, Fiedler T, Kapur RP, Agnew K et al. Parallel detection of lactobacillus and bacterial vaginosis-associated bacterial DNA in the chorioamnion and vagina of pregnant women at term. J Matern Fetal Neonatal Med 2019; 32:2702–2710 [View Article] [PubMed]
     [Google Scholar]
  27. Lennard K, Dabee S, Barnabas SL, Havyarimana E, Blakney A et al. Microbial composition predicts genital tract inflammation and persistent bacterial vaginosis in South African adolescent females. Infect Immun 2018; 86:e00410-17 [View Article] [PubMed]
     [Google Scholar]
  28. Madan RP, Carpenter C, Fiedler T, Kalyoussef S, McAndrew TC et al. Altered biomarkers of mucosal immunity and reduced vaginal Lactobacillus concentrations in sexually active female adolescents. PLoS One 2012; 7:e40415 [View Article] [PubMed]
     [Google Scholar]
  29. Tamarelle J, Ma B, Gajer P, Humphrys MS, Terplan M et al. Nonoptimal vaginal microbiota after azithromycin treatment for Chlamydia trachomatis infection. J Infect Dis 2020; 221:627–635 [View Article] [PubMed]
     [Google Scholar]
  30. Srinivasan S, Chambers LC, Tapia KA, Hoffman NG, Munch MM et al. Urethral microbiota in men: association of Haemophilus influenzae and Mycoplasma penetrans with nongonococcal urethritis. Clin Infect Dis 2021; 73:e1684–e1693 [View Article] [PubMed]
     [Google Scholar]
  31. Zinsli KA, Srinivasan S, Balkus JE, Chambers LC, Lowens MS et al. Bacterial vaginosis-associated bacteria in cisgender men who have sex with women: prevalence, association with non-gonococcal urethritis and natural history. Sex Transm Infect 2023; 99:317–323 [View Article] [PubMed]
     [Google Scholar]
  32. Damke E, Kurscheidt FA, Irie MMT, Gimenes F, Consolaro MEL. Male partners of infertile couples with seminal positivity for markers of bacterial vaginosis have impaired fertility. Am J Mens Health 2018; 12:2104–2115 [View Article] [PubMed]
     [Google Scholar]
  33. Coleman JS, Gaydos CA. Molecular diagnosis of bacterial vaginosis: an update. J Clin Microbiol 2018; 56:e00342-18 [View Article] [PubMed]
     [Google Scholar]
  34. Austin MN, Rabe LK, Srinivasan S, Fredricks DN, Wiesenfeld HC et al. Mageeibacillus indolicus gen. nov., sp. nov.: a novel bacterium isolated from the female genital tract. Anaerobe 2015; 32:37–42 [View Article] [PubMed]
     [Google Scholar]
  35. Austin MN, Srinivasan S, Fredricks DN, Wiesenfeld HC, Hillier SL. Mageeibacillus. In Whitman WB, Devos P, Dedysh S, Hedlund B, Kampfer P. eds Bergey’s Manual of Systematics of Archaea and Bacteria John Wiley & Sons, Inc; 2015 [View Article]
     [Google Scholar]
  36. Srinivasan S, Munch MM, Sizova MV, Fiedler TL, Kohler CM et al. More easily cultivated than identified: classical isolation with molecular identification of vaginal bacteria. J Infect Dis 2016; 214 Suppl 1:S21–8 [View Article] [PubMed]
     [Google Scholar]
  37. Srinivasan S, Beamer MA, Fiedler TL, Austin MN, Sizova MV et al. Megasphaera lornae sp. nov., Megasphaera hutchinsoni sp. nov., and Megasphaera vaginalis sp. nov.: novel bacteria isolated from the female genital tract. Int J Syst Evol Microbiol 2021; 71:
     [Google Scholar]
  38. Falsen E, Collins MD, Welinder-Olsson C, Song Y, Finegold SM et al. Fastidiosipila sanguinis gen. nov., sp. nov., a new Gram-positive, coccus-shaped organism from human blood. Int J Syst Evol Microbiol 2005; 55:853–858 [View Article] [PubMed]
     [Google Scholar]
  39. Summanen P, Baron EJ, Citron DM, Strong CA, Wexler HM et al. Wadsworth Anaerobic Bacteriology Manual, 5th. Belmont, CA: Star Publishing; 1993
     [Google Scholar]
  40. Stevens DL, Bryant AE, Carrol K et al. Clostridium. In Jorgensen JH, Pfaller MA, Carroll KC, Funke G, Landry ML et al. eds Manual of Clinical Microbiology, 11th edn. Washington, DC, USA: ASM Press;15 2015 pp 940–966
     [Google Scholar]
  41. Johnson MJ, Thatcher E, Cox ME. Techniques for controlling variability in gram staining of obligate anaerobes. J Clin Microbiol 1995; 33:755–758 [View Article] [PubMed]
     [Google Scholar]
  42. Samuel LP, Balada-Llasat J-M, Harrington A, Cavagnolo R. Multicenter assessment of gram stain error rates. J Clin Microbiol 2016; 54:1442–1447 [View Article] [PubMed]
     [Google Scholar]
  43. Halebian S, Harris B, Finegold SM, Rolfe RD. Rapid method that aids in distinguishing Gram-positive from Gram-negative anaerobic bacteria. J Clin Microbiol 1981; 13:444–448 [View Article] [PubMed]
     [Google Scholar]
  44. Kasana RC, Salwan R, Dhar H, Dutt S, Gulati A. A rapid and easy method for the detection of microbial cellulases on agar plates using gram’s iodine. Curr Microbiol 2008; 57:503–507 [View Article] [PubMed]
     [Google Scholar]
  45. Sasser M. Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids (Technical Note No.101) Newark, DE: Microbial ID Inc; 1990
     [Google Scholar]
  46. Culture Collection University of Gothenburg Revival of freeze-dried cultures 2020 https://ccug.se/ordering/revival
     [Google Scholar]
  47. Clinical Laboratory Standards Institute (CLSI) Methods for antimicrobial susceptibility testing of anaerobic bacteria. In CLSI Standard M11, 9th. edn Wayne, PA: Clinical and Laboratory Standards Institute; 2018
     [Google Scholar]
  48. Clinical Laboratory Standards Institute (CLSI) Performance standards for antimicrobial susceptibility testing. In CLSI Standard M100, 32nd. edn Clinical and Laboratory Standards Institute; 2022
     [Google Scholar]
  49. Centers for Disease Control and Prevention Sexually transmitted diseases treatment guidelines. Morbidity and Mortality Weekly Report 2015; 64:69–71
     [Google Scholar]
  50. Abd El Aziz MA, Sharifipour F, Abedi P, Jahanfar S, Judge HM. Secnidazole for treatment of bacterial vaginosis: a systematic review. BMC Womens Health 2019; 19:121 [View Article] [PubMed]
     [Google Scholar]
  51. Gajdács M, Spengler G, Urbán E. Identification and antimicrobial susceptibility testing of anaerobic bacteria: Rubik’s cube of clinical microbiology?. Antibiotics 2017; 6:25 [View Article] [PubMed]
     [Google Scholar]
  52. Flores Ramos S, Brugger SD, Escapa IF, Skeete CA, Cotton SL et al. Genomic stability and genetic defense systems in Dolosigranulum pigrum, a candidate beneficial bacterium from the human microbiome. mSystems 2021; 6:e0042521 [View Article] [PubMed]
     [Google Scholar]
  53. Hufnagel DE, Hufford MB, Seetharam AS. SequelTools: a suite of tools for working with PacBio sequel raw sequence data. BMC Bioinformatics 2020; 21:429 [View Article] [PubMed]
     [Google Scholar]
  54. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
     [Google Scholar]
  55. 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; 25:1043–1055 [View Article] [PubMed]
     [Google Scholar]
  56. Manni M, Berkeley MR, Seppey M, Zdobnov EM. BUSCO: assessing genomic data quality and beyond. Curr Protoc 2021; 1:e323 [View Article] [PubMed]
     [Google Scholar]
  57. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
     [Google Scholar]
  58. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 1993; 10:512–526 [View Article] [PubMed]
     [Google Scholar]
  59. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
     [Google Scholar]
  60. Wattam AR, Davis JJ, Assaf R, Boisvert S, Brettin T et al. Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Res 2017; 45:D535–D542 [View Article] [PubMed]
     [Google Scholar]
  61. 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]
  62. Meier-Kolthoff JP, Klenk H-P, Göker M. Taxonomic use of DNA G+C content and DNA-DNA hybridization in the genomic age. Int J Syst Evol Microbiol 2014; 64:352–356 [View Article] [PubMed]
     [Google Scholar]
  63. Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M. TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res 2022; 50:D801–D807 [View Article] [PubMed]
     [Google Scholar]
  64. Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Preprints 2016; 4:e1900v1: [View Article]
     [Google Scholar]
  65. Konstantinidis KT, Tiedje JM. Towards a genome-based taxonomy for prokaryotes. J Bacteriol 2005; 187:6258–6264 [View Article] [PubMed]
     [Google Scholar]
  66. Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci 2005; 102:2567–2572 [View Article] [PubMed]
     [Google Scholar]
  67. Chen S, Niu L, Zhang Y. Saccharofermentans acetigenes gen. nov., sp. nov., an anaerobic bacterium isolated from sludge treating brewery wastewater. Int J Syst Evol Microbiol 2010; 60:2735–2738 [View Article] [PubMed]
     [Google Scholar]
  68. van Gelder AH, Sousa DZ, Rijpstra WIC, Damsté JSS, Stams AJM et al. Ercella succinigenes gen. nov., sp. nov., an anaerobic succinate-producing bacterium. Int J Syst Evol Microbiol 2014; 64:2449–2454 [View Article] [PubMed]
     [Google Scholar]
  69. Shiratori H, Sasaya K, Ohiwa H, Ikeno H, Ayame S et al. Clostridium clariflavum sp. nov. and Clostridium caenicola sp. nov., moderately thermophilic, cellulose-/cellobiose-digesting bacteria isolated from methanogenic sludge. Int J Syst Evol Microbiol 2009; 59:1764–1770 [View Article] [PubMed]
     [Google Scholar]
  70. Nishiyama T, Ueki A, Kaku N, Ueki K. Clostridium sufflavum sp. nov., isolated from a methanogenic reactor treating cattle waste. Int J Syst Evol Microbiol 2009; 59:981–986 [View Article] [PubMed]
     [Google Scholar]
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Amygdalobacter indicium gen. nov., sp. nov., and Amygdalobacter nucleatus sp. nov., gen. nov.: novel bacteria from the family Oscillospiraceae isolated from the female genital tract
Int J Syst Evol Microbiol 73, 006017 (2023); https://doi.org/10.1099/ijsem.0.006017
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