Skip to main content
Top
Published in: Journal of Translational Medicine 1/2020

01-12-2020 | Denture | Research

Profiling the Salivary microbiome of the Qatari population

Authors: Selvasankar Murugesan, Sara Fahad Al Ahmad, Parul Singh, Marwa Saadaoui, Manoj Kumar, Souhaila Al Khodor

Published in: Journal of Translational Medicine | Issue 1/2020

Login to get access

Abstract

Background

The role of the human microbiome in human health and disease has been studied in various body sites. However, compared to the gut microbiome, where most of the research focus is, the salivary microbiome still bears a vast amount of information that needs to be revealed. This study aims to characterize the salivary microbiome composition in the Qatari population, and to explore specific microbial signatures that can be associated with various lifestyles and different oral conditions.

Materials and methods

We characterized the salivary microbiome of 997 Qatari adults using high-throughput sequencing of the V1–V3 region of the 16S rRNA gene.

Results

In this study, we have characterized the salivary microbiome of 997 Qatari participants. Our data show that Bacteroidetes, Firmicutes, Actinobacteria and Proteobacteria are the common phyla isolated from the saliva samples, with Bacteroidetes being the most predominant phylum. Bacteroidetes was also more predominant in males versus females in the study cohort, although differences in the microbial diversity were not statistically significant. We also show that, a lower diversity of the salivary microbiome is observed in the elderly participants, with Prevotella and Treponema being the most significant genera. In participants with oral conditions such as mouth ulcers, bleeding or painful gum, our data show that Prevotella and Capnocytophaga are the most dominant genera as compared to the controls. Similar patterns were observed in participants with various smoking habits as compared to the non-smoking participants. Our data show that Streptococcus and Neisseria are more dominant among denture users, as compared to the non-denture users. Our data also show that, abnormal oral conditions are associated with a reduced microbial diversity and microbial richness. Moreover, in this study we show that frequent coffee drinkers have higher microbial diversity compared to the non-drinkers, indicating that coffee may cause changes to the salivary microbiome. Furthermore, tea drinkers show higher microbial richness as compared to the non-tea drinkers.

Conclusion

This is the first study to assess the salivary microbiome in an Arab population, and one of the largest population-based studies aiming to the characterize the salivary microbiome composition and its association with age, oral health, denture use, smoking and coffee-tea consumption.
Appendix
Available only for authorised users
Literature
2.
go back to reference Liang D, Leung RK, Guan W, Au WW. Involvement of gut microbiome in human health and disease: brief overview, knowledge gaps and research opportunities. Gut Pathog. 2018;10:3.PubMedPubMedCentralCrossRef Liang D, Leung RK, Guan W, Au WW. Involvement of gut microbiome in human health and disease: brief overview, knowledge gaps and research opportunities. Gut Pathog. 2018;10:3.PubMedPubMedCentralCrossRef
3.
go back to reference Cao Y, Fanning S, Proos S, Jordan K, Srikumar S. A review on the applications of next generation sequencing technologies as applied to food-related microbiome studies. Front Microbiol. 1829;2017:8. Cao Y, Fanning S, Proos S, Jordan K, Srikumar S. A review on the applications of next generation sequencing technologies as applied to food-related microbiome studies. Front Microbiol. 1829;2017:8.
4.
go back to reference Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009;326:1694–7.PubMedPubMedCentralCrossRef Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009;326:1694–7.PubMedPubMedCentralCrossRef
5.
go back to reference Roblegg E, Coughran A, Sirjani D. Saliva: an all-rounder of our body. Eur J Pharm Biopharm. 2019;142:133–41.PubMedCrossRef Roblegg E, Coughran A, Sirjani D. Saliva: an all-rounder of our body. Eur J Pharm Biopharm. 2019;142:133–41.PubMedCrossRef
6.
go back to reference Humphrey SP, Williamson RT. A review of saliva: normal composition, flow, and function. J Prosthet Dent. 2001;85:162–9.PubMedCrossRef Humphrey SP, Williamson RT. A review of saliva: normal composition, flow, and function. J Prosthet Dent. 2001;85:162–9.PubMedCrossRef
8.
go back to reference Kaczor-Urbanowicz KE, Martin Carreras-Presas C, Aro K, Tu M, Garcia-Godoy F, Wong DT. Saliva diagnostics—current views and directions. Exp Biol Med (Maywood). 2017;242:459–72.CrossRef Kaczor-Urbanowicz KE, Martin Carreras-Presas C, Aro K, Tu M, Garcia-Godoy F, Wong DT. Saliva diagnostics—current views and directions. Exp Biol Med (Maywood). 2017;242:459–72.CrossRef
10.
go back to reference Kodukula K, Faller DV, Harpp DN, Kanara I, Pernokas J, Pernokas M, Powers WR, Soukos NS, Steliou K, Moos WH. Gut microbiota and salivary diagnostics: the mouth is salivating to tell us something. BioResearch open access. 2017;6:123–32.PubMedPubMedCentralCrossRef Kodukula K, Faller DV, Harpp DN, Kanara I, Pernokas J, Pernokas M, Powers WR, Soukos NS, Steliou K, Moos WH. Gut microbiota and salivary diagnostics: the mouth is salivating to tell us something. BioResearch open access. 2017;6:123–32.PubMedPubMedCentralCrossRef
11.
go back to reference Belstrøm D, Holmstrup P, Bardow A, Kokaras A, Fiehn N-E, Paster BJ. Temporal stability of the salivary microbiota in oral health. PLoS ONE. 2016;11:e0147472.PubMedPubMedCentralCrossRef Belstrøm D, Holmstrup P, Bardow A, Kokaras A, Fiehn N-E, Paster BJ. Temporal stability of the salivary microbiota in oral health. PLoS ONE. 2016;11:e0147472.PubMedPubMedCentralCrossRef
12.
go back to reference Cameron SJ, Huws SA, Hegarty MJ, Smith DP, Mur LA. The human salivary microbiome exhibits temporal stability in bacterial diversity. FEMS Microbiol Ecol. 2015;91:fiv091.PubMedCrossRef Cameron SJ, Huws SA, Hegarty MJ, Smith DP, Mur LA. The human salivary microbiome exhibits temporal stability in bacterial diversity. FEMS Microbiol Ecol. 2015;91:fiv091.PubMedCrossRef
13.
go back to reference Rasiah IA, Wong L, Anderson SA, Sissons CH. Variation in bacterial DGGE patterns from human saliva: over time, between individuals and in corresponding dental plaque microcosms. Arch Oral Biol. 2005;50:779–87.PubMedCrossRef Rasiah IA, Wong L, Anderson SA, Sissons CH. Variation in bacterial DGGE patterns from human saliva: over time, between individuals and in corresponding dental plaque microcosms. Arch Oral Biol. 2005;50:779–87.PubMedCrossRef
14.
go back to reference Stahringer SS, Clemente JC, Corley RP, Hewitt J, Knights D, Walters WA, Knight R, Krauter KS. Nurture trumps nature in a longitudinal survey of salivary bacterial communities in twins from early adolescence to early adulthood. Genome Res. 2012;22:2146–52.PubMedPubMedCentralCrossRef Stahringer SS, Clemente JC, Corley RP, Hewitt J, Knights D, Walters WA, Knight R, Krauter KS. Nurture trumps nature in a longitudinal survey of salivary bacterial communities in twins from early adolescence to early adulthood. Genome Res. 2012;22:2146–52.PubMedPubMedCentralCrossRef
15.
go back to reference Yamanaka W, Takeshita T, Shibata Y, Matsuo K, Eshima N, Yokoyama T, Yamashita Y. Compositional stability of a salivary bacterial population against supragingival microbiota shift following periodontal therapy. PLoS ONE. 2012;7:e42806.PubMedPubMedCentralCrossRef Yamanaka W, Takeshita T, Shibata Y, Matsuo K, Eshima N, Yokoyama T, Yamashita Y. Compositional stability of a salivary bacterial population against supragingival microbiota shift following periodontal therapy. PLoS ONE. 2012;7:e42806.PubMedPubMedCentralCrossRef
16.
go back to reference Zhou Y, Gao H, Mihindukulasuriya KA, La Rosa PS, Wylie KM, Vishnivetskaya T, Podar M, Warner B, Tarr PI, Nelson DE, et al. Biogeography of the ecosystems of the healthy human body. Genome Biol. 2013;14:R1.PubMedPubMedCentralCrossRef Zhou Y, Gao H, Mihindukulasuriya KA, La Rosa PS, Wylie KM, Vishnivetskaya T, Podar M, Warner B, Tarr PI, Nelson DE, et al. Biogeography of the ecosystems of the healthy human body. Genome Biol. 2013;14:R1.PubMedPubMedCentralCrossRef
17.
go back to reference Priya KY, Prathibha KM. Methods of collection of saliva-a review. Int J Oral Health Dent. 2017;3:149–53. Priya KY, Prathibha KM. Methods of collection of saliva-a review. Int J Oral Health Dent. 2017;3:149–53.
18.
go back to reference Lim Y, Totsika M, Morrison M, Punyadeera C. The saliva microbiome profiles are minimally affected by collection method or DNA extraction protocols. Sci Rep. 2017;7:8523.PubMedPubMedCentralCrossRef Lim Y, Totsika M, Morrison M, Punyadeera C. The saliva microbiome profiles are minimally affected by collection method or DNA extraction protocols. Sci Rep. 2017;7:8523.PubMedPubMedCentralCrossRef
19.
go back to reference Rosier BT, Marsh PD, Mira A. Resilience of the oral microbiota in health: mechanisms that prevent dysbiosis. J Dent Res. 2018;97:371–80.PubMedCrossRef Rosier BT, Marsh PD, Mira A. Resilience of the oral microbiota in health: mechanisms that prevent dysbiosis. J Dent Res. 2018;97:371–80.PubMedCrossRef
20.
go back to reference He J, Li Y, Cao Y, Xue J, Zhou X. The oral microbiome diversity and its relation to human diseases. Folia Microbiol (Praha). 2015;60:69–80.CrossRef He J, Li Y, Cao Y, Xue J, Zhou X. The oral microbiome diversity and its relation to human diseases. Folia Microbiol (Praha). 2015;60:69–80.CrossRef
21.
22.
23.
go back to reference Bik EM, Long CD, Armitage GC, Loomer P, Emerson J, Mongodin EF, Nelson KE, Gill SR, Fraser-Liggett CM, Relman DA. Bacterial diversity in the oral cavity of 10 healthy individuals. ISME J. 2010;4:962–74.PubMedCrossRef Bik EM, Long CD, Armitage GC, Loomer P, Emerson J, Mongodin EF, Nelson KE, Gill SR, Fraser-Liggett CM, Relman DA. Bacterial diversity in the oral cavity of 10 healthy individuals. ISME J. 2010;4:962–74.PubMedCrossRef
24.
go back to reference Segata N, Haake SK, Mannon P, Lemon KP, Waldron L, Gevers D, Huttenhower C, Izard J. Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol. 2012;13:R42.PubMedPubMedCentralCrossRef Segata N, Haake SK, Mannon P, Lemon KP, Waldron L, Gevers D, Huttenhower C, Izard J. Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol. 2012;13:R42.PubMedPubMedCentralCrossRef
25.
go back to reference Hall MW, Singh N, Ng KF, Lam DK, Goldberg MB, Tenenbaum HC, Neufeld JD. R GB, Senadheera DB: Inter-personal diversity and temporal dynamics of dental, tongue, and salivary microbiota in the healthy oral cavity. NPJ Biofilms Microbiomes. 2017;3:2.PubMedPubMedCentralCrossRef Hall MW, Singh N, Ng KF, Lam DK, Goldberg MB, Tenenbaum HC, Neufeld JD. R GB, Senadheera DB: Inter-personal diversity and temporal dynamics of dental, tongue, and salivary microbiota in the healthy oral cavity. NPJ Biofilms Microbiomes. 2017;3:2.PubMedPubMedCentralCrossRef
27.
go back to reference Rusthen S, Kristoffersen AK, Young A, Galtung HK, Petrovski BE, Palm O, Enersen M, Jensen JL. Dysbiotic salivary microbiota in dry mouth and primary Sjogren’s syndrome patients. PLoS ONE. 2019;14:e0218319.PubMedPubMedCentralCrossRef Rusthen S, Kristoffersen AK, Young A, Galtung HK, Petrovski BE, Palm O, Enersen M, Jensen JL. Dysbiotic salivary microbiota in dry mouth and primary Sjogren’s syndrome patients. PLoS ONE. 2019;14:e0218319.PubMedPubMedCentralCrossRef
28.
go back to reference Lira-Junior R, Akerman S, Klinge B, Bostrom EA, Gustafsson A. Salivary microbial profiles in relation to age, periodontal, and systemic diseases. PLoS ONE. 2018;13:e0189374.PubMedPubMedCentralCrossRef Lira-Junior R, Akerman S, Klinge B, Bostrom EA, Gustafsson A. Salivary microbial profiles in relation to age, periodontal, and systemic diseases. PLoS ONE. 2018;13:e0189374.PubMedPubMedCentralCrossRef
29.
go back to reference Krishnan K, Chen T, Paster BJ. A practical guide to the oral microbiome and its relation to health and disease. Oral Dis. 2017;23:276–86.PubMedCrossRef Krishnan K, Chen T, Paster BJ. A practical guide to the oral microbiome and its relation to health and disease. Oral Dis. 2017;23:276–86.PubMedCrossRef
30.
go back to reference Wu J, Peters BA, Dominianni C, Zhang Y, Pei Z, Yang L, Ma Y, Purdue MP, Jacobs EJ, Gapstur SM, et al. Cigarette smoking and the oral microbiome in a large study of American adults. ISME J. 2016;10:2435–46.PubMedPubMedCentralCrossRef Wu J, Peters BA, Dominianni C, Zhang Y, Pei Z, Yang L, Ma Y, Purdue MP, Jacobs EJ, Gapstur SM, et al. Cigarette smoking and the oral microbiome in a large study of American adults. ISME J. 2016;10:2435–46.PubMedPubMedCentralCrossRef
31.
go back to reference Rodríguez-Rabassa M, López P, Rodríguez-Santiago RE, Cases A, Felici M, Sánchez R, Yamamura Y, Rivera-Amill V. Cigarette smoking modulation of saliva microbial composition and cytokine levels. Int J Environ Res Public Health. 2018;15:2479.PubMedCentralCrossRef Rodríguez-Rabassa M, López P, Rodríguez-Santiago RE, Cases A, Felici M, Sánchez R, Yamamura Y, Rivera-Amill V. Cigarette smoking modulation of saliva microbial composition and cytokine levels. Int J Environ Res Public Health. 2018;15:2479.PubMedCentralCrossRef
33.
go back to reference Yasunaga H, Takeshita T, Shibata Y, Furuta M, Shimazaki Y, Akifusa S, Ninomiya T, Kiyohara Y, Takahashi I, Yamashita Y. Exploration of bacterial species associated with the salivary microbiome of individuals with a low susceptibility to dental caries. Clin Oral Investig. 2017;21:2399–406.PubMedCrossRef Yasunaga H, Takeshita T, Shibata Y, Furuta M, Shimazaki Y, Akifusa S, Ninomiya T, Kiyohara Y, Takahashi I, Yamashita Y. Exploration of bacterial species associated with the salivary microbiome of individuals with a low susceptibility to dental caries. Clin Oral Investig. 2017;21:2399–406.PubMedCrossRef
34.
go back to reference Belstrom D, Holmstrup P, Fiehn NE, Kirkby N, Kokaras A, Paster BJ, Bardow A. Salivary microbiota in individuals with different levels of caries experience. J Oral Microbiol. 2017;9:1270614.PubMedPubMedCentralCrossRef Belstrom D, Holmstrup P, Fiehn NE, Kirkby N, Kokaras A, Paster BJ, Bardow A. Salivary microbiota in individuals with different levels of caries experience. J Oral Microbiol. 2017;9:1270614.PubMedPubMedCentralCrossRef
35.
go back to reference Schoilew K, Ueffing H, Dalpke A, Wolff B, Frese C, Wolff D, Boutin S. Bacterial biofilm composition in healthy subjects with and without caries experience. J Oral Microbiol. 2019;11:1633194.PubMedPubMedCentralCrossRef Schoilew K, Ueffing H, Dalpke A, Wolff B, Frese C, Wolff D, Boutin S. Bacterial biofilm composition in healthy subjects with and without caries experience. J Oral Microbiol. 2019;11:1633194.PubMedPubMedCentralCrossRef
36.
go back to reference Ennibi OK, Claesson R, Akkaoui S, Reddahi S, Kwamin F, Haubek D, Johansson A. High salivary levels of JP2 genotype of Aggregatibacter actinomycetemcomitans is associated with clinical attachment loss in Moroccan adolescents. Clin Exp Dent Res. 2019;5:44–51.PubMedPubMedCentralCrossRef Ennibi OK, Claesson R, Akkaoui S, Reddahi S, Kwamin F, Haubek D, Johansson A. High salivary levels of JP2 genotype of Aggregatibacter actinomycetemcomitans is associated with clinical attachment loss in Moroccan adolescents. Clin Exp Dent Res. 2019;5:44–51.PubMedPubMedCentralCrossRef
37.
go back to reference Salminen A, Kopra KA, Hyvarinen K, Paju S, Mantyla P, Buhlin K, Nieminen MS, Sinisalo J, Pussinen PJ. Quantitative PCR analysis of salivary pathogen burden in periodontitis. Front Cell Infect Microbiol. 2015;5:69.PubMedPubMedCentralCrossRef Salminen A, Kopra KA, Hyvarinen K, Paju S, Mantyla P, Buhlin K, Nieminen MS, Sinisalo J, Pussinen PJ. Quantitative PCR analysis of salivary pathogen burden in periodontitis. Front Cell Infect Microbiol. 2015;5:69.PubMedPubMedCentralCrossRef
38.
go back to reference Khemwong T, Kobayashi H, Ikeda Y, Matsuura T, Sudo T, Kano C, Mikami R, Izumi Y. Fretibacterium sp. human oral taxon 360 is a novel biomarker for periodontitis screening in the Japanese population. PLoS ONE. 2019;14:e0218266.PubMedPubMedCentralCrossRef Khemwong T, Kobayashi H, Ikeda Y, Matsuura T, Sudo T, Kano C, Mikami R, Izumi Y. Fretibacterium sp. human oral taxon 360 is a novel biomarker for periodontitis screening in the Japanese population. PLoS ONE. 2019;14:e0218266.PubMedPubMedCentralCrossRef
39.
go back to reference Janem WF, Scannapieco FA, Sabharwal A, Tsompana M, Berman HA, Haase EM, Miecznikowski JC, Mastrandrea LD. Salivary inflammatory markers and microbiome in normoglycemic lean and obese children compared to obese children with type 2 diabetes. PLoS ONE. 2017;12:e0172647.PubMedPubMedCentralCrossRef Janem WF, Scannapieco FA, Sabharwal A, Tsompana M, Berman HA, Haase EM, Miecznikowski JC, Mastrandrea LD. Salivary inflammatory markers and microbiome in normoglycemic lean and obese children compared to obese children with type 2 diabetes. PLoS ONE. 2017;12:e0172647.PubMedPubMedCentralCrossRef
40.
go back to reference Acharya A, Chan Y, Kheur S, Jin LJ, Watt RM, Mattheos N. Salivary microbiome in non-oral disease: a summary of evidence and commentary. Arch Oral Biol. 2017;83:169–73.PubMedCrossRef Acharya A, Chan Y, Kheur S, Jin LJ, Watt RM, Mattheos N. Salivary microbiome in non-oral disease: a summary of evidence and commentary. Arch Oral Biol. 2017;83:169–73.PubMedCrossRef
41.
go back to reference Pereira PAB, Aho VTE, Paulin L, Pekkonen E, Auvinen P, Scheperjans F. Oral and nasal microbiota in Parkinson’s disease. Parkinsonism Related Disord. 2017;38:61–7.CrossRef Pereira PAB, Aho VTE, Paulin L, Pekkonen E, Auvinen P, Scheperjans F. Oral and nasal microbiota in Parkinson’s disease. Parkinsonism Related Disord. 2017;38:61–7.CrossRef
43.
go back to reference Zhang X, Zhang D, Jia H, Feng Q, Wang D, Liang D, Wu X, Li J, Tang L, Li Y, et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med. 2015;21:895.PubMedCrossRef Zhang X, Zhang D, Jia H, Feng Q, Wang D, Liang D, Wu X, Li J, Tang L, Li Y, et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med. 2015;21:895.PubMedCrossRef
44.
45.
go back to reference Sampaio-Maia B, Caldas IM, Pereira ML, Perez-Mongiovi D, Araujo R. The oral microbiome in health and its implication in oral and systemic diseases. Adv Appl Microbiol. 2016;97:171–210.PubMedCrossRef Sampaio-Maia B, Caldas IM, Pereira ML, Perez-Mongiovi D, Araujo R. The oral microbiome in health and its implication in oral and systemic diseases. Adv Appl Microbiol. 2016;97:171–210.PubMedCrossRef
46.
go back to reference Takeshita T, Kageyama S, Furuta M, Tsuboi H, Takeuchi K, Shibata Y, Shimazaki Y, Akifusa S, Ninomiya T, Kiyohara Y, Yamashita Y. Bacterial diversity in saliva and oral health-related conditions: the Hisayama Study. Sci Rep. 2016;6:22164.PubMedPubMedCentralCrossRef Takeshita T, Kageyama S, Furuta M, Tsuboi H, Takeuchi K, Shibata Y, Shimazaki Y, Akifusa S, Ninomiya T, Kiyohara Y, Yamashita Y. Bacterial diversity in saliva and oral health-related conditions: the Hisayama Study. Sci Rep. 2016;6:22164.PubMedPubMedCentralCrossRef
47.
go back to reference Vogtmann E, Chen J, Kibriya MG, Amir A, Shi J, Chen Y, Islam T, Eunes M, Ahmed A, Naher J, et al. Comparison of oral collection methods for studies of microbiota. Cancer Epidemiol Biomark Prev. 2019;28:137–43.CrossRef Vogtmann E, Chen J, Kibriya MG, Amir A, Shi J, Chen Y, Islam T, Eunes M, Ahmed A, Naher J, et al. Comparison of oral collection methods for studies of microbiota. Cancer Epidemiol Biomark Prev. 2019;28:137–43.CrossRef
48.
go back to reference Xun Z, Zhang Q, Xu T, Chen N, Chen F. Dysbiosis and ecotypes of the salivary microbiome associated with inflammatory bowel diseases and the assistance in diagnosis of diseases using oral bacterial profiles. Front Microbiol. 2018;9:1136.PubMedPubMedCentralCrossRef Xun Z, Zhang Q, Xu T, Chen N, Chen F. Dysbiosis and ecotypes of the salivary microbiome associated with inflammatory bowel diseases and the assistance in diagnosis of diseases using oral bacterial profiles. Front Microbiol. 2018;9:1136.PubMedPubMedCentralCrossRef
49.
go back to reference Shaw L, Ribeiro ALR, Levine AP, Pontikos N, Balloux F, Segal AW, Roberts AP, Smith AM. The human salivary microbiome is shaped by shared environment rather than genetics: evidence from a large family of closely related individuals. MBio. 2017;8:e01237-17.PubMedPubMedCentralCrossRef Shaw L, Ribeiro ALR, Levine AP, Pontikos N, Balloux F, Segal AW, Roberts AP, Smith AM. The human salivary microbiome is shaped by shared environment rather than genetics: evidence from a large family of closely related individuals. MBio. 2017;8:e01237-17.PubMedPubMedCentralCrossRef
50.
go back to reference Raju SC, Lagstrom S, Ellonen P, de Vos WM, Eriksson JG, Weiderpass E, Rounge TB. Gender-specific associations between saliva microbiota and body size. Front Microbiol. 2019;10:767.PubMedPubMedCentralCrossRef Raju SC, Lagstrom S, Ellonen P, de Vos WM, Eriksson JG, Weiderpass E, Rounge TB. Gender-specific associations between saliva microbiota and body size. Front Microbiol. 2019;10:767.PubMedPubMedCentralCrossRef
51.
go back to reference Cabral DJ, Wurster JI, Flokas ME, Alevizakos M, Zabat M, Korry BJ, Rowan AD, Sano WH, Andreatos N, Ducharme RB, et al. The salivary microbiome is consistent between subjects and resistant to impacts of short-term hospitalization. Sci Rep. 2017;7:11040.PubMedPubMedCentralCrossRef Cabral DJ, Wurster JI, Flokas ME, Alevizakos M, Zabat M, Korry BJ, Rowan AD, Sano WH, Andreatos N, Ducharme RB, et al. The salivary microbiome is consistent between subjects and resistant to impacts of short-term hospitalization. Sci Rep. 2017;7:11040.PubMedPubMedCentralCrossRef
52.
go back to reference Xu X, He J, Xue J, Wang Y, Li K, Zhang K, Guo Q, Liu X, Zhou Y, Cheng L, et al. Oral cavity contains distinct niches with dynamic microbial communities. Environ Microbiol. 2015;17:699–710.PubMedCrossRef Xu X, He J, Xue J, Wang Y, Li K, Zhang K, Guo Q, Liu X, Zhou Y, Cheng L, et al. Oral cavity contains distinct niches with dynamic microbial communities. Environ Microbiol. 2015;17:699–710.PubMedCrossRef
53.
go back to reference Percival RS, Challacombe SJ, Marsh PD. Age-related microbiological changes in the salivary and plaque microflora of healthy adults. J Med Microbiol. 1991;35:5–11.PubMedCrossRef Percival RS, Challacombe SJ, Marsh PD. Age-related microbiological changes in the salivary and plaque microflora of healthy adults. J Med Microbiol. 1991;35:5–11.PubMedCrossRef
54.
go back to reference Fransen F, van Beek AA, Borghuis T, Meijer B, Hugenholtz F, van der Gaast-de Jongh C, Savelkoul HF, de Jonge MI, Faas MM, Boekschoten MV, et al. The impact of gut microbiota on gender-specific differences in immunity. Front Immunol. 2017;8:754.PubMedPubMedCentralCrossRef Fransen F, van Beek AA, Borghuis T, Meijer B, Hugenholtz F, van der Gaast-de Jongh C, Savelkoul HF, de Jonge MI, Faas MM, Boekschoten MV, et al. The impact of gut microbiota on gender-specific differences in immunity. Front Immunol. 2017;8:754.PubMedPubMedCentralCrossRef
55.
go back to reference Haro C, Rangel-Zuniga OA, Alcala-Diaz JF, Gomez-Delgado F, Perez-Martinez P, Delgado-Lista J, Quintana-Navarro GM, Landa BB, Navas-Cortes JA, Tena-Sempere M, et al. Intestinal microbiota is influenced by gender and body mass index. PLoS ONE. 2016;11:e0154090.PubMedPubMedCentralCrossRef Haro C, Rangel-Zuniga OA, Alcala-Diaz JF, Gomez-Delgado F, Perez-Martinez P, Delgado-Lista J, Quintana-Navarro GM, Landa BB, Navas-Cortes JA, Tena-Sempere M, et al. Intestinal microbiota is influenced by gender and body mass index. PLoS ONE. 2016;11:e0154090.PubMedPubMedCentralCrossRef
56.
go back to reference Zaura E, Brandt BW, Mattos MJ, Buijs MJ, Caspers MP, Rashid MU, Weintraub A, Nord CE, Savell A, Hu Y, et al. Same exposure but two radically different responses to antibiotics: resilience of the salivary microbiome versus long-term microbial shifts in feces. MBio. 2015;6:e01693-01615.CrossRef Zaura E, Brandt BW, Mattos MJ, Buijs MJ, Caspers MP, Rashid MU, Weintraub A, Nord CE, Savell A, Hu Y, et al. Same exposure but two radically different responses to antibiotics: resilience of the salivary microbiome versus long-term microbial shifts in feces. MBio. 2015;6:e01693-01615.CrossRef
57.
go back to reference Takahashi N. Oral microbiome metabolism: from “Who Are They?” to “What Are They Doing?”. J Dent Res. 2015;94:1628–37.PubMedCrossRef Takahashi N. Oral microbiome metabolism: from “Who Are They?” to “What Are They Doing?”. J Dent Res. 2015;94:1628–37.PubMedCrossRef
58.
go back to reference Frandsen EV, Kjeldsen M, Kilian M. Inhibition of Prevotella and Capnocytophaga immunoglobulin A1 proteases by human serum. Clin Diagn Lab Immunol. 1997;4:458–64.PubMedPubMedCentralCrossRef Frandsen EV, Kjeldsen M, Kilian M. Inhibition of Prevotella and Capnocytophaga immunoglobulin A1 proteases by human serum. Clin Diagn Lab Immunol. 1997;4:458–64.PubMedPubMedCentralCrossRef
59.
go back to reference Affoo RH, Foley N, Garrick R, Siqueira WL, Martin RE. Meta-analysis of salivary flow rates in young and older adults. J Am Geriatr Soc. 2015;63:2142–51.PubMedCrossRef Affoo RH, Foley N, Garrick R, Siqueira WL, Martin RE. Meta-analysis of salivary flow rates in young and older adults. J Am Geriatr Soc. 2015;63:2142–51.PubMedCrossRef
60.
go back to reference Cruz-Almeida Y, Aguirre M, Sorenson H, Tighe P, Wallet SM, Riley JL 3rd. Age differences in salivary markers of inflammation in response to experimental pain: does venipuncture matter? J Pain Res. 2017;10:2365–72.PubMedPubMedCentralCrossRef Cruz-Almeida Y, Aguirre M, Sorenson H, Tighe P, Wallet SM, Riley JL 3rd. Age differences in salivary markers of inflammation in response to experimental pain: does venipuncture matter? J Pain Res. 2017;10:2365–72.PubMedPubMedCentralCrossRef
61.
go back to reference Jiang Q, Liu J, Chen L, Gan N, Yang D. The oral microbiome in the elderly with dental caries and health. Front Cell Infect Microbiol. 2018;8:442.PubMedCrossRef Jiang Q, Liu J, Chen L, Gan N, Yang D. The oral microbiome in the elderly with dental caries and health. Front Cell Infect Microbiol. 2018;8:442.PubMedCrossRef
62.
go back to reference Marchini L, Campos MS, Silva AM, Paulino LC, Nobrega FG. Bacterial diversity in aphthous ulcers. Oral Microbiol Immunol. 2007;22:225–31.PubMedCrossRef Marchini L, Campos MS, Silva AM, Paulino LC, Nobrega FG. Bacterial diversity in aphthous ulcers. Oral Microbiol Immunol. 2007;22:225–31.PubMedCrossRef
63.
go back to reference Lourenvarsigmao TGB, Spencer SJ, Alm EJ, Colombo APV. Defining the gut microbiota in individuals with periodontal diseases: an exploratory study. J Oral Microbiol. 2018;10:1487741.PubMedPubMedCentralCrossRef Lourenvarsigmao TGB, Spencer SJ, Alm EJ, Colombo APV. Defining the gut microbiota in individuals with periodontal diseases: an exploratory study. J Oral Microbiol. 2018;10:1487741.PubMedPubMedCentralCrossRef
64.
go back to reference Mashima I, Theodorea CF, Thaweboon B, Thaweboon S, Scannapieco FA, Nakazawa F. Exploring the salivary microbiome of children stratified by the oral hygiene index. PLoS ONE. 2017;12:e0185274.PubMedPubMedCentralCrossRef Mashima I, Theodorea CF, Thaweboon B, Thaweboon S, Scannapieco FA, Nakazawa F. Exploring the salivary microbiome of children stratified by the oral hygiene index. PLoS ONE. 2017;12:e0185274.PubMedPubMedCentralCrossRef
66.
go back to reference O’Donnell LE, Robertson D, Nile CJ, Cross LJ, Riggio M, Sherriff A, Bradshaw D, Lambert M, Malcolm J, Buijs MJ, et al. The oral microbiome of denture wearers is influenced by levels of natural dentition. PLoS ONE. 2015;10:e0137717.PubMedPubMedCentralCrossRef O’Donnell LE, Robertson D, Nile CJ, Cross LJ, Riggio M, Sherriff A, Bradshaw D, Lambert M, Malcolm J, Buijs MJ, et al. The oral microbiome of denture wearers is influenced by levels of natural dentition. PLoS ONE. 2015;10:e0137717.PubMedPubMedCentralCrossRef
67.
go back to reference Teles FR, Teles RP, Sachdeo A, Uzel NG, Song XQ, Torresyap G, Singh M, Papas A, Haffajee AD, Socransky SS. Comparison of microbial changes in early redeveloping biofilms on natural teeth and dentures. J Periodontol. 2012;83:1139–48.PubMedPubMedCentralCrossRef Teles FR, Teles RP, Sachdeo A, Uzel NG, Song XQ, Torresyap G, Singh M, Papas A, Haffajee AD, Socransky SS. Comparison of microbial changes in early redeveloping biofilms on natural teeth and dentures. J Periodontol. 2012;83:1139–48.PubMedPubMedCentralCrossRef
68.
go back to reference Brook I. The impact of smoking on oral and nasopharyngeal bacterial flora. J Dent Res. 2011;90:704–10.PubMedCrossRef Brook I. The impact of smoking on oral and nasopharyngeal bacterial flora. J Dent Res. 2011;90:704–10.PubMedCrossRef
69.
go back to reference Charlson ES, Chen J, Custers-Allen R, Bittinger K, Li H, Sinha R, Hwang J, Bushman FD, Collman RG. Disordered microbial communities in the upper respiratory tract of cigarette smokers. PLoS ONE. 2010;5:e15216.PubMedPubMedCentralCrossRef Charlson ES, Chen J, Custers-Allen R, Bittinger K, Li H, Sinha R, Hwang J, Bushman FD, Collman RG. Disordered microbial communities in the upper respiratory tract of cigarette smokers. PLoS ONE. 2010;5:e15216.PubMedPubMedCentralCrossRef
70.
go back to reference Berkowitz L, Schultz BM, Salazar GA, Pardo-Roa C, Sebastian VP, Alvarez-Lobos MM, Bueno SM. Impact of cigarette smoking on the gastrointestinal tract inflammation: opposing effects in Crohn’s disease and ulcerative colitis. Front Immunol. 2018;9:74.PubMedPubMedCentralCrossRef Berkowitz L, Schultz BM, Salazar GA, Pardo-Roa C, Sebastian VP, Alvarez-Lobos MM, Bueno SM. Impact of cigarette smoking on the gastrointestinal tract inflammation: opposing effects in Crohn’s disease and ulcerative colitis. Front Immunol. 2018;9:74.PubMedPubMedCentralCrossRef
71.
go back to reference Yu G, Phillips S, Gail MH, Goedert JJ, Humphrys MS, Ravel J, Ren Y, Caporaso NE. The effect of cigarette smoking on the oral and nasal microbiota. Microbiome. 2017;5:3.PubMedPubMedCentralCrossRef Yu G, Phillips S, Gail MH, Goedert JJ, Humphrys MS, Ravel J, Ren Y, Caporaso NE. The effect of cigarette smoking on the oral and nasal microbiota. Microbiome. 2017;5:3.PubMedPubMedCentralCrossRef
72.
go back to reference Grover N, Sharma J, Sengupta S, Singh S, Singh N, Kaur H. Long-term effect of tobacco on unstimulated salivary pH. J Oral Maxillofac Pathol. 2016;20:16–9.PubMedPubMedCentralCrossRef Grover N, Sharma J, Sengupta S, Singh S, Singh N, Kaur H. Long-term effect of tobacco on unstimulated salivary pH. J Oral Maxillofac Pathol. 2016;20:16–9.PubMedPubMedCentralCrossRef
73.
go back to reference Peters BA, McCullough ML, Purdue MP, Freedman ND, Um CY, Gapstur SM, Hayes RB, Ahn J. Association of coffee and tea intake with the oral microbiome: results from a large cross-sectional study. Cancer Epidemiol Biomark Prev. 2018;27:814–21.CrossRef Peters BA, McCullough ML, Purdue MP, Freedman ND, Um CY, Gapstur SM, Hayes RB, Ahn J. Association of coffee and tea intake with the oral microbiome: results from a large cross-sectional study. Cancer Epidemiol Biomark Prev. 2018;27:814–21.CrossRef
75.
go back to reference Loftfield E, Shiels MS, Graubard BI, Katki HA, Chaturvedi AK, Trabert B, Pinto LA, Kemp TJ, Shebl FM, Mayne ST, et al. Associations of coffee drinking with systemic immune and inflammatory markers. Cancer Epidemiol Biomark Prev. 2015;24:1052–60.CrossRef Loftfield E, Shiels MS, Graubard BI, Katki HA, Chaturvedi AK, Trabert B, Pinto LA, Kemp TJ, Shebl FM, Mayne ST, et al. Associations of coffee drinking with systemic immune and inflammatory markers. Cancer Epidemiol Biomark Prev. 2015;24:1052–60.CrossRef
76.
go back to reference Signoretto C, Bianchi F, Burlacchini G, Sivieri F, Spratt D, Canepari P. Drinking habits are associated with changes in the dental plaque microbial community. J Clin Microbiol. 2010;48:347–56.PubMedCrossRef Signoretto C, Bianchi F, Burlacchini G, Sivieri F, Spratt D, Canepari P. Drinking habits are associated with changes in the dental plaque microbial community. J Clin Microbiol. 2010;48:347–56.PubMedCrossRef
77.
go back to reference Signoretto C, Burlacchini G, Bianchi F, Cavalleri G, Canepari P. Differences in microbiological composition of saliva and dental plaque in subjects with different drinking habits. N Microbiol. 2006;29:293–302. Signoretto C, Burlacchini G, Bianchi F, Cavalleri G, Canepari P. Differences in microbiological composition of saliva and dental plaque in subjects with different drinking habits. N Microbiol. 2006;29:293–302.
78.
go back to reference Palmer RJ Jr. Composition and development of oral bacterial communities. Periodontol. 2000;2014(64):20–39. Palmer RJ Jr. Composition and development of oral bacterial communities. Periodontol. 2000;2014(64):20–39.
80.
go back to reference Su T, Liu R, Lee A, Long Y, Du L, Lai S, Chen X, Wang L, Si J, Owyang C, Chen S. Altered intestinal microbiota with increased abundance of prevotella is associated with high risk of diarrhea-predominant irritable bowel syndrome. Gastroenterol Res Pract. 2018;2018:6961783.PubMedPubMedCentral Su T, Liu R, Lee A, Long Y, Du L, Lai S, Chen X, Wang L, Si J, Owyang C, Chen S. Altered intestinal microbiota with increased abundance of prevotella is associated with high risk of diarrhea-predominant irritable bowel syndrome. Gastroenterol Res Pract. 2018;2018:6961783.PubMedPubMedCentral
81.
go back to reference Leite AZ, Rodrigues NC, Gonzaga MI, Paiolo JCC, de Souza CA, Stefanutto NAV, Omori WP, Pinheiro DG, Brisotti JL, Matheucci Junior E, et al. Detection of increased plasma interleukin-6 levels and prevalence of Prevotella copri and Bacteroides vulgatus in the feces of type 2 diabetes patients. Front Immunol. 2017;8:1107.PubMedPubMedCentralCrossRef Leite AZ, Rodrigues NC, Gonzaga MI, Paiolo JCC, de Souza CA, Stefanutto NAV, Omori WP, Pinheiro DG, Brisotti JL, Matheucci Junior E, et al. Detection of increased plasma interleukin-6 levels and prevalence of Prevotella copri and Bacteroides vulgatus in the feces of type 2 diabetes patients. Front Immunol. 2017;8:1107.PubMedPubMedCentralCrossRef
82.
go back to reference De Filippis F, Vannini L, La Storia A, Laghi L, Piombino P, Stellato G, Serrazanetti DI, Gozzi G, Turroni S, Ferrocino I, et al. The same microbiota and a potentially discriminant metabolome in the saliva of omnivore, ovo-lacto-vegetarian and Vegan individuals. PLoS ONE. 2014;9:e112373.PubMedPubMedCentralCrossRef De Filippis F, Vannini L, La Storia A, Laghi L, Piombino P, Stellato G, Serrazanetti DI, Gozzi G, Turroni S, Ferrocino I, et al. The same microbiota and a potentially discriminant metabolome in the saliva of omnivore, ovo-lacto-vegetarian and Vegan individuals. PLoS ONE. 2014;9:e112373.PubMedPubMedCentralCrossRef
83.
go back to reference Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, Huttenhower C. Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol. 2012;8:e1002606.PubMedPubMedCentralCrossRef Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, Huttenhower C. Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol. 2012;8:e1002606.PubMedPubMedCentralCrossRef
84.
go back to reference Takeshita T, Nakano Y, Kumagai T, Yasui M, Kamio N, Shibata Y, Shiota S, Yamashita Y. The ecological proportion of indigenous bacterial populations in saliva is correlated with oral health status. ISME J. 2009;3:65–78.PubMedCrossRef Takeshita T, Nakano Y, Kumagai T, Yasui M, Kamio N, Shibata Y, Shiota S, Yamashita Y. The ecological proportion of indigenous bacterial populations in saliva is correlated with oral health status. ISME J. 2009;3:65–78.PubMedCrossRef
85.
go back to reference Shahi SK, Freedman SN, Murra AC, Zarei K, Sompallae R, Gibson-Corley KN, Karandikar NJ, Murray JA, Mangalam AK. Prevotella histicola, a human gut commensal, is as potent as COPAXONE(R) in an animal model of multiple sclerosis. Front Immunol. 2019;10:462.PubMedPubMedCentralCrossRef Shahi SK, Freedman SN, Murra AC, Zarei K, Sompallae R, Gibson-Corley KN, Karandikar NJ, Murray JA, Mangalam AK. Prevotella histicola, a human gut commensal, is as potent as COPAXONE(R) in an animal model of multiple sclerosis. Front Immunol. 2019;10:462.PubMedPubMedCentralCrossRef
86.
go back to reference Kovatcheva-Datchary P, Nilsson A, Akrami R, Lee YS, De Vadder F, Arora T, Hallen A, Martens E, Bjorck I, Backhed F. Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of prevotella. Cell Metab. 2015;22:971–82.PubMedCrossRef Kovatcheva-Datchary P, Nilsson A, Akrami R, Lee YS, De Vadder F, Arora T, Hallen A, Martens E, Bjorck I, Backhed F. Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of prevotella. Cell Metab. 2015;22:971–82.PubMedCrossRef
87.
go back to reference Zheng W, Tsompana M, Ruscitto A, Sharma A, Genco R, Sun Y, Buck MJ. An accurate and efficient experimental approach for characterization of the complex oral microbiota. Microbiome. 2015;3:48.PubMedPubMedCentralCrossRef Zheng W, Tsompana M, Ruscitto A, Sharma A, Genco R, Sun Y, Buck MJ. An accurate and efficient experimental approach for characterization of the complex oral microbiota. Microbiome. 2015;3:48.PubMedPubMedCentralCrossRef
88.
go back to reference Mattei V, Murugesan S, Al Hashmi M, Mathew R, James N, Singh P, Kumar M, Lakshmanan AP, Terranegra A, Al Khodor S, Tomei S. Evaluation of methods for the extraction of microbial DNA from vaginal swabs used for microbiome studies. Front Cell Infect Microbiol. 2019;9:197.PubMedPubMedCentralCrossRef Mattei V, Murugesan S, Al Hashmi M, Mathew R, James N, Singh P, Kumar M, Lakshmanan AP, Terranegra A, Al Khodor S, Tomei S. Evaluation of methods for the extraction of microbial DNA from vaginal swabs used for microbiome studies. Front Cell Infect Microbiol. 2019;9:197.PubMedPubMedCentralCrossRef
89.
go back to reference Andrews S. FastQC: a quality control tool for high throughput sequence data; 2010. Andrews S. FastQC: a quality control tool for high throughput sequence data; 2010.
90.
go back to reference Zhang J, Kobert K, Flouri T, Stamatakis A. PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics. 2014;30:614–20.PubMedCrossRef Zhang J, Kobert K, Flouri T, Stamatakis A. PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics. 2014;30:614–20.PubMedCrossRef
92.
go back to reference Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.PubMedPubMedCentralCrossRef Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.PubMedPubMedCentralCrossRef
93.
go back to reference Escapa IF, Chen T, Huang Y, Gajare P, Dewhirst FE, Lemon KP. New insights into human nostril microbiome from the expanded human oral microbiome database (eHOMD): a resource for the microbiome of the human aerodigestive tract. Systems. 2018;3:e00187-00118. Escapa IF, Chen T, Huang Y, Gajare P, Dewhirst FE, Lemon KP. New insights into human nostril microbiome from the expanded human oral microbiome database (eHOMD): a resource for the microbiome of the human aerodigestive tract. Systems. 2018;3:e00187-00118.
94.
go back to reference Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.PubMedPubMedCentralCrossRef Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.PubMedPubMedCentralCrossRef
95.
96.
go back to reference Lozupone CA, Hamady M, Kelley ST, Knight R. Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol. 2007;73:1576–85.PubMedPubMedCentralCrossRef Lozupone CA, Hamady M, Kelley ST, Knight R. Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol. 2007;73:1576–85.PubMedPubMedCentralCrossRef
Metadata
Title
Profiling the Salivary microbiome of the Qatari population
Authors
Selvasankar Murugesan
Sara Fahad Al Ahmad
Parul Singh
Marwa Saadaoui
Manoj Kumar
Souhaila Al Khodor
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2020
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-020-02291-2

Other articles of this Issue 1/2020

Journal of Translational Medicine 1/2020 Go to the issue