Selenonomas noxia

MICR3004 Microbial Genomics Semester 2 2016, The University of Queensland

Classification

Higher order taxa

Bacteria – Terrabacteria group - Firmicutes – Negativicutes – Selenomonadales – Selenomonadaceae – Selenomonas ^[1]

Species

Species: “Selenomonas noxia” Type strain: ATCC 43541=JCM 8546=VPI D9B-5 ^[2]

Description and significance

“Selenomonas noxia” (“S. noxia”) is one of five “Selenomonas” species that Moore et al. first characterised in 1987 ^[3]. “S. noxia” fits the general Selenomonad description- motile, crescent-shaped, nonsporeforming gram-negative rods ^{[3] [4] [5] [6]}. It is morphologically distinguishable from other “Selenomonas” species by its relatively smaller cells (1.1 um diameter by 1.1–3.2 um length) ^[3]. It was first characterised from cultured isolates of the gingival crevice of periodontitis and gingivitis patients. “S. noxia” grow in anaerobic culture, showing abundant growth on peptone-yeast extract media with glucose, mannose, sorbitol, or sorbose ^[3]. “S. noxia” have one or more central-to-pole flagella originating from the concave cell side ^{[3] [6]}.

In a healthy oral microbiome, “S. noxia” occurrence strongly correlates with numerous other species: “Actinomyces gerencseriae”, “A. oris”, “A. johnsonii”, “S. sputigena”, “S. artemides”, “Streptococcus sanguinis”, “S. oralis”, “Fusobacterium nucleatum” and “Veillonella parvula”. These bacteria appear to contribute similar functions, with 98% overlap in encoded functions from a 60% overlap in genes. In the functional specialization present, “S. noxia” is one of six rare taxa within the oral microbiome that contribute genes for motility and chemotaxis ^[7].

“S. noxia” is important to study due to its consistent association with periodontal disease. It is thought to be a putative periodontal pathogen ^{[4] [6] [8] [9]}. Periodontitis is a highly prevalent diseasese, and much remains unclear about the mechanisms of its pathogenesis ^[7]. Elucidation of the exact role “S. noxia” plays in periodontitis initiation and progression, and the mechanism by this occurs, could inform new disease prevention and treatment methods.

Genome structure

The “S. noxia” type strain ATCC 4351 genome has been characterised by whole genome shotgun sequencing. With a size of 2.05499 Mb and GC content of 55.80%, the genome contains 1,983 distinct genes encoding for 1,876 proteins. No plasmids have been detected ^[10].

Cell structure and metabolism

Cell wall

Negativicutes class members, including “S. noxia”, are distinct from other firmicutes in staining Gram-negative. They have typical gram-negative envelope composition: inner phospholipid leaflet, periplasmic space with a thin peptidoglycan layer, outer lipopolysaccharide leaflet. Significant amounts of the polyamine putrescine have been detected in “S. noxia” peptidoglycan ^[11].

Motility

“S. noxia” achieve tumbling motility via a flagella tuft attached to the cell curvature ^{[3] [6]}.

Biofilm formation

“S. noxia” are part dental plaque, a structurally and functionally organized biofilm. Teles et al. found that S. noxia are one of the last species to colonise, increasing significantly in mean proportion after seven days without oral hygiene ^[12].

Metabolic functions

“S. noxia” are saccharolytic obligate anaerobes, meaning they metabolise sugars to produce energy without oxygen ^[8]. “S. noxia” typically ferment glucose and fructose to produce acetic and lactic acids, and major amounts of propionic acid ^{[3] [6] [8]}. They are distinct from other known “Selenomonas” species by an inability to ferment sucrose ^[3]. Moore et al. found that 27% of strains can respire via oxidative phosphorylation ^[3]. These strains have a partial electron transport chain of complexes I and II, and a bd terminal reductase. Nitrate is the terminal electron acceptor ^[13].

“S. noxia” are hydrogen-forming bacteria, with hydrogen detected in culture ^[3]. H2 production occurs in anaerobes as a means to reoxidize NADH, which can become overly reduced in fermenters. “S. noxia” encode for several hydrogen production pathways ^[14].

Ecology

“S. noxia” are strict anaerobes, located in the gingival crevice, and subgingival plaque adjacent to periodontal lesions ^[3]. They can act as both commensals and pathogens.

“S. noxia” appear to interact relatively little with other oral bacterial species. Five major bacterial complexes are consistently detected in subgingival plaque. “S. noxia” are an outlier, participating in no complexes ^{[15] [16]}. Isolates aggregate with the narrowest range of partners observed to date compared with Actinomyces, Bacteroides, Capnocytophaga, Haemophilus, Streptococcus and Veillonella species. Importantly, “S. noxia” do aggregate with Fusobacteria ^[16]. “Fusobacterium nucleatum” provides a physical tether for late colonisers and oral pathogens such as “S. noxia” to adhere to dental plaque ^[17].

Pathology

Periodontitis

Hundreds of microbes have insofar been identified within the gingival crevice and periodontal pocket. While little literature exists on “S. noxia” pathogenicity, it is one of the few species that appear to contribute significantly to periodontitis establishment and progression ^[4].

Periodontitis is a highly prevalent infectious disease. Tooth-supporting tissues become inflamed and periodontal pockets form, with the ultimate result of alveolar bone and periodontal attachment loss ^[18]. Disease develops with a shift in the subgingival microbiome away from a health-compatible state ^[7]. A trend toward anaerobes is typical ^[19]. Disease progresses via complex interactions between dental biofilms and the host’s immune system ^[18].

Moore et al.’s early studies suggested “S. noxia” were associated with periodontitis. The epithet ‘noxia’ refers to their harmful nature. Data revealed “S. noxia” increased from 0.9% to 5.9% in periodontal plaque from healthy to disease-active sites ^[3]. Many studies have since confirmed this finding ^{[9] [19] [20] [21] [22]}. Data cannot yet conclusively relate “S. noxia” to periodontitis etiology. Nonetheless, considerable literature supports this hypothesis ^{[4] [5] [6] [9] [21]}. Tanner et al. found that active-disease patients were distinguished by higher “S. noxia” mean proportions ^[21]. Association studies demonstrated no combination of species shows a stronger relationship with recent attachment loss than that of “S. noxia” by itself ^[20]. This suggests “S. noxia” may be involved with general aggressive periodontitis (GAP), a more destructive disease form. Supporting this, “S. noxia” have been detected in GAP lesions ^[4] and research shows “Selenomonas” phylotypes are typical and abundant members of GAP subgingival biofilm that contribute to structural organisation ^[22].

Gingival tissue is highly susceptible to lipopolysaccharide (LPS) endotoxins ^[6]. Among other bacterial products, LPS can trigger host inflammatory cascades. It stimulates cytokine production, which promotes destructive metalloproteinase matrix release of from host tissues ^[18]. “S. noxia” LPS possesses endotoxic properties stronger than that of “Escherichia coli” LPS ^[6], suggesting “S. noxia” LPS contributes to periodontal disease progression.

Halitosis

“S. noxia” have been implicated in halitosis. They produce volatile sulphur compounds, responsible for the bad breath associated with halitosis ^[23].

Obesity

Research suggests “S. noxia” may be involved obesity development. “S. noxia” at levels >1.05% of the total bacterial population can predict obesity with a sensitivity of 98% and specificity of 80% ^[5]. More research is needed to elucidate the exact relationship between oral bacteria and obesity.

Application to biotechnology

Biotechnologically relevant compound production

“S. noxia” produce propionate via fermentation ^[3]. Propionate and its derivatives are Food and Drug Administration approved “Generally Recognised As Safe” food additives. They are widely used as antimicrobial and anti-inflammatory agents, herbicides, food preservatives and artificial flavours ^[24]. Propionate mass production currently occurs largely by chemical synthesis. Interest in microbial production techniques is however growing in response to the environmental issues of conventional synthesis ^[24]. “S. noxia” could thus play a role in future propionate production.

“S. noxia” are hydrogen-forming bacteria ^[3]. Hydrogen is a biogas, which could provide a viable, clean alternative to fossil fuels. It has a high calorific value, is efficient, and can be used in fuel cells ^[25].

==Current research==

Smoking and the oral microbiome

Smoking negatively affects the subgingival microbiome in both periodontal health and disease by supporting pathogen-rich community formation. Interestingly, Tsigarida et al. recently identified that “S. noxia” is a part of the non-smoker core microbiome. Relative abundance was significantly higher in healthy non-smokers than healthy smokers ^[36].

Cyclic dinucleotides

Bacteria can sense and respond to their environment via secondary messenger molecules. Cyclic dinucleotides appear to be significant biofilm establishment and growth regulators. “S. noxia” produce detectable levels of cyclic dinucleotides ^[27]. Cyclic dinucleotide regulation interference could present an effective approach to fighting infectious diseases, including periodontitis sustained by “S. noxia”.

References

1. [1]

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3. Moore, L., Johnson, J., and Moore, W. (1987). “Selenomonas noxia” sp. nov., “Selenomonas flueggei” sp. nov., “Selenomonas infelix” sp. nov., “Selenomonas dianae” sp. nov., and “Selenomonas artemides” sp. nov., from the human gingival crevice. Int J Syst Evol Microbiol 37: 271-280.

4. Cruz, P., Mehretu, A., Buttner, M., Trice, T., and Howard, K. (2015). Development of a polymerase chain reaction assay for the rapid detection of the oral pathogenic bacterium, “Selenomonas noxia”. BMC Oral Health25: 95.

5. Goodson, J., Groppo, D., Halem, S., and Carpino, E. (2009). Is Obesity an Oral Bacterial Disease? Journal of Dental Research, 88: 519-523.

6. Kurimoto, T., Tachibana, C., Suzuki, M., and Watanabe, T. (1986). Biological and chemical characterization of lipopolysaccharide from “Selenomonas” spp. in human periodontal pockets. Infect Immun 51: 969–971.

7. Dabdoub, S. M., Ganesan, S. M., and Kumar, P. S. (2016). Comparative metagenomics reveals taxonomically idiosyncratic yet functionally congruent communities in periodontitis. Sci Rep 6: 38993.

8. Maiden, M., Tanner, A., and Moore, W. (1992). Identification of “Selenomonas” species by whole‐genomic DNA probes, sodium dodecyl sulfate‐polyacrylamide gel electrophoresis, biochemical tests and cellular fatty acid analysis. Mol Oral Microbiol 7: 7-13.

9. Colombo, A. P. V., Boches, S. K., Cotton, S. L., Goodson, J. M., Kent, R., Haffajee, A. D., Socransky, S. S., Hasturk, H., Dyke, T. E. V., and Paster, B. J. (2009). Comparisons of Subgingival Microbial Profiles of Refractory Periodontitis, Severe Periodontitis and Periodontal Health using the Human Oral Microbe Identification Microarray (HOMIM). J Periodontol 80: 1421-1432.

10. [3]

11. [https://www.jstage.jst.go.jp/article/jgam/48/3/48_3_177/_article Hamana, K., Saito, T., Okada, M., Sakamoto, A., and Hosoya, R. (2002). Covalently linked polyamines in the cell wall peptidoglycan of “Selenomonas”, “Anaeromusa”, “Dendrosporobacter”, “Acidaminococcus” and “Anaerovibrio” belonging to the “Sporomusa” subbranch. J Gen Appl Microbiol, 48: 177-80.]

12. Teles, F. R., Teles, R. P., Sachdeo, A., Uzel, N. G., Song, X. Q., Torresyap, G., Singh, M., Papas, A., Haffajee, A.D., and Socransky, S. S. (2012). Comparison of microbial changes in early re-developing biofilms on natural teeth and dentures. J Periodontol 83: 1139–1148.

13. [4]

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15. Tanner, A. C. R. (2015). Anaerobic culture to detect periodontal and caries pathogens. J Oral Biosci 57: 18–26.

16. Kolenbrander, P. E., Andersen, R. N., and Moore, L. V. (1989). Coaggregation of “Fusobacterium nucleatum”, “Selenomonas flueggei”, “Selenomonas infelix”, “Selenomonas noxia”, and “Selenomonas sputigena” with strains from 11 genera of oral bacteria. Infect Immun 57: 3194–3203.

17. Abreu, N. A., and Taga, M. E. (2016). Decoding molecular interactions in microbial communities. FEMS Microbiol Rev 40: 648–663.

18. Ossola, C., Surkin, A., Pugnaloni, P., Mohn, N., Elverdin, A., and Fernandez-Solari, C. (2012). Long-term treatment with methanandamide attenuates LPS-induced periodontitis in rats. Inflamm Res 61: 941-948.

19. Correa, J., Saraiva, A., Queiroz, C., Madeira, M., Duarte, P., Teixeira, M., Souza, D. G., and Silva, T. A. (2016). Arthritis-induced alveolar bone loss is associated with changes in the composition of oral microbiota. Anaerobe 39: 91-96.

20. Tanner, A., Bouldin, H., and Maiden, D. (1989). Newly delineated periodontal pathogens with special reference to “selenomonas” species. Infection 17: 182-187.

21. Tanner, A., Maiden, M., Macuch, P., Murray, L., and Kent, R. (1998). Microbiota of health, gingivitis, and initial periodontitis. J Clin Periodontol 25: 85-98.

22. Schueller, K., Riva, A., Pfeiffer, S., Berry, D., and Somoza, V. (2017). Members of the Oral Microbiota Are Associated with IL-8 Release by Gingival Epithelial Cells in Healthy Individuals. Front Microbiol 8: 416.

23. Ren, W., Zhang, Q., Liu, X., Zheng, S., Ma, L., Chen, F., Xu, T., and Xu, B. (2016). Supragingival plaque microbial community analysis of children with halitosis. J Microbiol Biotechnol 26: 2141-2147.

24. Eş, I., Khaneghah, A., Hashemi, M., and Koubaa, S. (2017). Current advances in biological production of propionic acid. Biotechnol Lett 39: 635-645.

25. Jia, X., Xi, B.-D., Li, M.-X., Yang, Y., and Wang, Y. (2017). Metaproteomics analysis of the functional insights into microbial communities of combined hydrogen and methane production by anaerobic fermentation from reed straw. PLoS ONE 12: e0183158.

26. Tsigarida, A. A., Dabdoub, S. M., Nagaraja, H. N., & Kumar, P. S. (2015). The Influence of Smoking on the Peri-Implant Microbiome. J Dent Res 94:1202–1217.

27. [https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5478684/ Gürsoy, U. K., Gürsoy, M., Könönen, E., and Sintim, H. O. (2017). Cyclic Dinucleotides in Oral Bacteria and in Oral Biofilms. Front Cell Infect Microbiol 7: 273.}

This page is written by Margot Bligh for the MICR3004 course, Semester 2, 2017