Skip to content
1887

Abstract

Data on the genomics of species other than (POTG), particularly within pulmonary environments, are scarce. In this study, we conducted whole-genome sequencing on pulmonary isolates of POTG, specifically (=3), (=1) and (=2), from people with cystic fibrosis. These genomic analyses were complemented with antimicrobial susceptibility tests for these strains. We compared the genomic sequences of these pulmonary isolates with those of previously characterized species. Our study revealed a distinct clade differentiation between non-pigmented and pigmented species. Unlike , the pulmonary POTG strains lacked known virulence genes, with the exception of a putative haemolysin gene. Regarding antibiotic resistance, notable resistances were limited to vancomycin in and clindamycin in . These findings support the hypothesis that POTG species may predominantly behave as commensals in the lung environment rather than as pathogens.

Funding
This study was supported by the:
  • Association Vaincre la Mucoviscidose (Award RC20170501971)
    • Principal Award Recipient: GENEVIEVEHERY-ARNAUD
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001411
2025-06-13
2026-03-16

Metrics

Loading full text...

Full text loading...

/deliver/fulltext/mgen/11/6/mgen001411.html?itemId=/content/journal/mgen/10.1099/mgen.0.001411&mimeType=html&fmt=ahah

References

  1. Carmody LA, Caverly LJ, Foster BK, Rogers MAM, Kalikin LM et al. Fluctuations in airway bacterial communities associated with clinical states and disease stages in cystic fibrosis. PLoS One 2018; 13:e0194060 [View Article] [PubMed]
    [Google Scholar]
  2. Muhlebach MS, Hatch JE, Einarsson GG, McGrath SJ, Gilipin DF et al. Anaerobic bacteria cultured from cystic fibrosis airways correlate to milder disease: a multisite study. Eur Respir J 2018; 52:1800242 [View Article] [PubMed]
    [Google Scholar]
  3. Zemanick ET, Harris JK, Wagner BD, Robertson CE, Sagel SD et al. Inflammation and airway microbiota during cystic fibrosis pulmonary exacerbations. PLoS One 2013; 8:e62917 [View Article] [PubMed]
    [Google Scholar]
  4. Charlson ES, Bittinger K, Haas AR, Fitzgerald AS, Frank I et al. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med 2011; 184:957–963 [View Article] [PubMed]
    [Google Scholar]
  5. Erb-Downward JR, Thompson DL, Han MK, Freeman CM, McCloskey L et al. Analysis of the lung microbiome in the “healthy” smoker and in COPD. PLoS One 2011; 6:e16384 [View Article] [PubMed]
    [Google Scholar]
  6. Whelan FJ, Waddell B, Syed SA, Shekarriz S, Rabin HR et al. Culture-enriched metagenomic sequencing enables in-depth profiling of the cystic fibrosis lung microbiota. Nat Microbiol 2020; 5:379–390 [View Article] [PubMed]
    [Google Scholar]
  7. Dickson RP, Erb-Downward JR, Freeman CM, McCloskey L, Falkowski NR et al. Bacterial topography of the healthy human lower respiratory tract. mBio 2017; 8: [View Article] [PubMed]
    [Google Scholar]
  8. Lee SY, Mac Aogáin M, Fam KD, Chia KL, Binte Mohamed Ali NA et al. Airway microbiome composition correlates with lung function and arterial stiffness in an age-dependent manner. PLoS One 2019; 14:e0225636 [View Article] [PubMed]
    [Google Scholar]
  9. Weinberg F, Dickson RP, Nagrath D, Ramnath N. The lung microbiome: a central mediator of host inflammation and metabolism in lung cancer patients?. Cancers 2020; 13: [View Article] [PubMed]
    [Google Scholar]
  10. Chen J, Li T, Ye C, Zhong J, Huang J-D et al. The lung microbiome: a new frontier for lung and brain disease. Int J Mol Sci 2023; 24:2170 [View Article]
    [Google Scholar]
  11. Beck JM, Young VB, Huffnagle GB. The microbiome of the lung. Transl Res 2012; 160:258–266 [View Article] [PubMed]
    [Google Scholar]
  12. Morris A, Beck JM, Schloss PD, Campbell TB, Crothers K et al. Comparison of the respiratory microbiome in healthy nonsmokers and smokers. Am J Respir Crit Care Med 2013; 187:1067–1075 [View Article] [PubMed]
    [Google Scholar]
  13. Park H, Shin JW, Park SG, Kim W. Microbial communities in the upper respiratory tract of patients with asthma and chronic obstructive pulmonary disease. PLoS One 2014; 9:e109710 [View Article]
    [Google Scholar]
  14. Lim MY, Yoon HS, Rho M, Sung J, Song Y-M et al. Analysis of the association between host genetics, smoking, and sputum microbiota in healthy humans. Sci Rep 2016; 6:23745 [View Article] [PubMed]
    [Google Scholar]
  15. Bassis CM, Erb-Downward JR, Dickson RP, Freeman CM, Schmidt TM et al. Analysis of the upper respiratory tract microbiotas as the source of the lung and gastric microbiotas in healthy individuals. mBio 2015; 6:e00037 [View Article]
    [Google Scholar]
  16. Guilloux CA, Lamoureux C, Beauruelle C, Héry-Arnaud G. Porphyromonas: A neglected potential key genus in human microbiomes. Anaerobe 2021; 68:102230 [View Article] [PubMed]
    [Google Scholar]
  17. Lamoureux C, Guilloux C-A, Beauruelle C, Gouriou S, Ramel S et al. An observational study of anaerobic bacteria in cystic fibrosis lung using culture dependant and independent approaches. Sci Rep 2021; 11:6845 [View Article] [PubMed]
    [Google Scholar]
  18. Abusleme L, Dupuy AK, Dutzan N, Silva N, Burleson JA et al. The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. ISME J 2013; 7:1016–1025 [View Article] [PubMed]
    [Google Scholar]
  19. 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] [PubMed]
    [Google Scholar]
  20. Murray PR, Washington JA. Microscopic and baceriologic analysis of expectorated sputum. Mayo Clin Proc 1975; 50:339–344 [PubMed]
    [Google Scholar]
  21. Wick RR, Judd LM, Gorrie CL, Holt KE. Completing bacterial genome assemblies with multiplex MinION sequencing. Microb Genom 2017; 3:e000132 [View Article] [PubMed]
    [Google Scholar]
  22. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  23. Vallenet D, Calteau A, Dubois M, Amours P, Bazin A et al. MicroScope: an integrated platform for the annotation and exploration of microbial gene functions through genomic, pangenomic and metabolic comparative analysis. Nucleic Acids Res 2020; 48:D579–D589 [View Article] [PubMed]
    [Google Scholar]
  24. Antipov D, Raiko M, Lapidus A, Pevzner PA. Metaviral SPAdes: assembly of viruses from metagenomic data. Bioinformatics 2020; 36:4126–4129 [View Article] [PubMed]
    [Google Scholar]
  25. Guo J, Bolduc B, Zayed AA, Varsani A, Dominguez-Huerta G et al. VirSorter2: a multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses. Microbiome 2021; 9:37 [View Article] [PubMed]
    [Google Scholar]
  26. Microbiologie SFd Anaérobies. CA-SFM / EUCAST. Société Française de Microbiologie ed 2022. pp 128–131
  27. Summanen P, Porphyromonas FS. Bergey’s Manual of Systematics of Archaea and Bacteria. Kindle ed 2015 pp 1–14 [View Article]
    [Google Scholar]
  28. Konstantinidis KT, Tiedje JM. Towards a genome-based taxonomy for prokaryotes. J Bacteriol 2005; 187:6258–6264 [View Article] [PubMed]
    [Google Scholar]
  29. Konstantinidis KT, Ramette A, Tiedje JM. The bacterial species definition in the genomic era. Philos Trans R Soc Lond B Biol Sci 2006; 361:1929–1940 [View Article] [PubMed]
    [Google Scholar]
  30. Mendez KN, Hoare A, Soto C, Bugueño I, Olivera M et al. Variability in genomic and virulent properties of Porphyromonas gingivalis strains isolated from healthy and severe chronic periodontitis individuals. Front Cell Infect Microbiol 2019; 9:246 [View Article] [PubMed]
    [Google Scholar]
  31. Hajishengallis G. Periodontitis: from microbial immune subversion to systemic inflammation. Nat Rev Immunol 2015; 15:30–44 [View Article] [PubMed]
    [Google Scholar]
  32. Payungporn S, Arirachakaran P, Poomipak W, Praianantathavorn K, Charalampakis G et al. Identification of bacteria associated with a periodontal disease in Thai patients based on next-generation sequencing. Jundishapur J Microbiol 2017; 10: [View Article]
    [Google Scholar]
  33. Yang HW, Huang YF, Chou MY. Occurrence of Porphyromonas gingivalis and Tannerella forsythensis in periodontally diseased and healthy subjects. J Periodontol 2004; 75:1077–1083 [View Article] [PubMed]
    [Google Scholar]
  34. Liu Y, Yuan X, Chen K, Zhou F, Yang H et al. Clinical significance and prognostic value of Porphyromonas gingivalis infection in lung cancer. Transl Oncol 2021; 14:100972 [View Article] [PubMed]
    [Google Scholar]
  35. Scher JU, Abramson SB. Periodontal disease, Porphyromonas gingivalis, and rheumatoid arthritis: what triggers autoimmunity and clinical disease?. Arthritis Res Ther 2013; 15:122 [View Article] [PubMed]
    [Google Scholar]
  36. Dominy SS, Lynch C, Ermini F, Benedyk M, Marczyk A et al. Porphyromonas gingivalis in Alzheimer’s disease brains: evidence for disease causation and treatment with small-molecule inhibitors. Sci Adv 2019; 5:eaau3333 [View Article] [PubMed]
    [Google Scholar]
  37. Pattaroni C, Watzenboeck ML, Schneidegger S, Kieser S, Wong NC et al. Early-life formation of the microbial and immunological environment of the human airways. Cell Host Microbe 2018; 24:857–865 [View Article] [PubMed]
    [Google Scholar]
  38. Crielaard W, Zaura E, Schuller AA, Huse SM, Montijn RC et al. Exploring the oral microbiota of children at various developmental stages of their dentition in the relation to their oral health. BMC Med Genom 2011; 4:22 [View Article] [PubMed]
    [Google Scholar]
  39. Könönen E, Väisänen M-L, Finegold SM, Heine R, Jousimies-Somer H. Cellular fatty acid analysis and enzyme profiles of Porphyromonas catoniae—a frequent colonizer of the oral cavity in children. Anaerobe 1996; 2:329–335 [View Article]
    [Google Scholar]
  40. Yasunaga H, Takeshita T, Shibata Y, Furuta M, Shimazaki Y et al. Exploration of bacterial species associated with the salivary microbiome of individuals with a low susceptibility to dental caries. Clin Oral Investig 2017; 21:2399–2406 [View Article] [PubMed]
    [Google Scholar]
  41. Keravec M, Mounier J, Guilloux CA, Fangous MS, Mondot S et al. Porphyromonas catoniae is associated with stable lung function and absence of Pseudomonas aeruginosa colonization in cystic fibrosis patients. BMJ Open Respir Res 2019; 6:e000374 [View Article]
    [Google Scholar]
  42. Martinez FJ, Erb-Downward JR, Huffnagle GB. Significance of the microbiome in chronic obstructive pulmonary disease. Annals ATS 2013; 10:S170–S179 [View Article] [PubMed]
    [Google Scholar]
  43. O’Flynn C, Deusch O, Darling AE, Eisen JA, Wallis C et al. Comparative genomics of the genus Porphyromonas identifies adaptations for heme synthesis within the prevalent canine oral species Porphyromonas cangingivalis. Genome Biol Evol 2015; 7:3397–3413 [View Article] [PubMed]
    [Google Scholar]
  44. Romero V, Fert-Bober J, Nigrovic PA, Darrah E, Haque UJ et al. Immune-mediated pore-forming pathways induce cellular hypercitrullination and generate citrullinated autoantigens in rheumatoid arthritis. Sci Transl Med 2013; 5:209ra150 [View Article] [PubMed]
    [Google Scholar]
  45. Gómez-Bañuelos E, Mukherjee A, Darrah E, Andrade F. Rheumatoid arthritis-associated mechanisms of Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans. J Clin Med 2019; 8:1309 [View Article] [PubMed]
    [Google Scholar]
  46. Nemoto TK, Ohara-Nemoto Y. Exopeptidases and gingipains in Porphyromonas gingivalis as prerequisites for its amino acid metabolism. Jpn Dent Sci Rev 2016; 52:22–29 [View Article] [PubMed]
    [Google Scholar]
  47. Aldridge KE, Ashcraft D, Cambre K, Pierson CL, Jenkins SG et al. Multicenter survey of the changing in vitro antimicrobial susceptibilities of clinical isolates of Bacteroides fragilis group, Prevotella, Fusobacterium, Porphyromonas, and Peptostreptococcus species. Antimicrob Agents Chemother 2001; 45:1238–1243 [View Article] [PubMed]
    [Google Scholar]
  48. Finegold SM, Vaisanen M-L, Rautio M, Eerola E, Summanen P et al. Porphyromonas uenonis sp. nov., a pathogen for humans distinct from P. asaccharolytica and P. endodontalis. J Clin Microbiol 2004; 42:5298–5301 [View Article] [PubMed]
    [Google Scholar]
  49. 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]
/content/journal/mgen/10.1099/mgen.0.001411
Loading
/content/journal/mgen/10.1099/mgen.0.001411
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
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