Salivary mycobiome dysbiosis and its potential impact on bacteriome shifts and host immunity in oral lichen planus
Abstract
The biodiversity of the mycobiome, an important component of the oral microbial community, and the roles of fungal–bacterial and fungal–immune system interactions in the pathogenesis of oral lichen planus (OLP) remain largely uncharacterized. In this study, we sequenced the salivary mycobiome and bacteriome associated with OLP. First, we described the dysbiosis of the microbiome in OLP patients, which exhibits lower levels of fungi and higher levels of bacteria. Significantly higher abundances of the fungi Candida and Aspergillus in patients with reticular OLP and of Alternaria and Sclerotiniaceae_unidentified in patients with erosive OLP were observed compared to the healthy controls. Aspergillus was identified as an “OLP-associated” fungus because of its detection at a higher frequency than in the healthy controls. Second, the co-occurrence patterns of the salivary mycobiome–bacteriome demonstrated negative associations between specific fungal and bacterial taxa identified in the healthy controls, which diminished in the reticular OLP group and even became positive in the erosive OLP group. Moreover, the oral cavities of OLP patients were colonized by dysbiotic oral flora with lower ecological network complexity and decreased fungal–Firmicutes and increased fungal–Bacteroidetes sub-networks. Third, several keystone fungal genera (Bovista, Erysiphe, Psathyrella, etc.) demonstrated significant correlations with clinical scores and IL-17 levels.more »
- Authors:
-
- Sichuan Univ., Chengdu (China). West China Hospital of Stomatology, National Clinical Research Center for Oral Diseases, State Key Lab. of Oral Diseases
- Shandong Univ., Qingdao (China). Inst. of Marine Science and Technology; Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics
- Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics
- The Forsyth Inst., Cambridge, MA (United States)
- Sichuan Univ., Chengdu (China). West China School of Basic Medical and Forensic Medicine
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Key Research and Development Program of China; National Natural Science Foundation of China (NNSFC)
- OSTI Identifier:
- 1582043
- Grant/Contract Number:
- AC02-05CH11231; 81771085; 81430011; 81600858; 81600874; 16ZD021
- Resource Type:
- Accepted Manuscript
- Journal Name:
- International Journal of Oral Science
- Additional Journal Information:
- Journal Volume: 11; Journal Issue: 2; Journal ID: ISSN 1674-2818
- Publisher:
- Springer Nature
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Li, Yan, Wang, Kun, Zhang, Bo, Tu, Qichao, Yao, Yufei, Cui, Bomiao, Ren, Biao, He, Jinzhi, Shen, Xin, Van Nostrand, Joy D., Zhou, Jizhong, Shi, Wenyuan, Xiao, Liying, Lu, Changqing, and Zhou, Xuedong. Salivary mycobiome dysbiosis and its potential impact on bacteriome shifts and host immunity in oral lichen planus. United States: N. p., 2019.
Web. doi:10.1038/s41368-019-0045-2.
Li, Yan, Wang, Kun, Zhang, Bo, Tu, Qichao, Yao, Yufei, Cui, Bomiao, Ren, Biao, He, Jinzhi, Shen, Xin, Van Nostrand, Joy D., Zhou, Jizhong, Shi, Wenyuan, Xiao, Liying, Lu, Changqing, & Zhou, Xuedong. Salivary mycobiome dysbiosis and its potential impact on bacteriome shifts and host immunity in oral lichen planus. United States. doi:https://doi.org/10.1038/s41368-019-0045-2
Li, Yan, Wang, Kun, Zhang, Bo, Tu, Qichao, Yao, Yufei, Cui, Bomiao, Ren, Biao, He, Jinzhi, Shen, Xin, Van Nostrand, Joy D., Zhou, Jizhong, Shi, Wenyuan, Xiao, Liying, Lu, Changqing, and Zhou, Xuedong. Tue .
"Salivary mycobiome dysbiosis and its potential impact on bacteriome shifts and host immunity in oral lichen planus". United States. doi:https://doi.org/10.1038/s41368-019-0045-2. https://www.osti.gov/servlets/purl/1582043.
@article{osti_1582043,
title = {Salivary mycobiome dysbiosis and its potential impact on bacteriome shifts and host immunity in oral lichen planus},
author = {Li, Yan and Wang, Kun and Zhang, Bo and Tu, Qichao and Yao, Yufei and Cui, Bomiao and Ren, Biao and He, Jinzhi and Shen, Xin and Van Nostrand, Joy D. and Zhou, Jizhong and Shi, Wenyuan and Xiao, Liying and Lu, Changqing and Zhou, Xuedong},
abstractNote = {The biodiversity of the mycobiome, an important component of the oral microbial community, and the roles of fungal–bacterial and fungal–immune system interactions in the pathogenesis of oral lichen planus (OLP) remain largely uncharacterized. In this study, we sequenced the salivary mycobiome and bacteriome associated with OLP. First, we described the dysbiosis of the microbiome in OLP patients, which exhibits lower levels of fungi and higher levels of bacteria. Significantly higher abundances of the fungi Candida and Aspergillus in patients with reticular OLP and of Alternaria and Sclerotiniaceae_unidentified in patients with erosive OLP were observed compared to the healthy controls. Aspergillus was identified as an “OLP-associated” fungus because of its detection at a higher frequency than in the healthy controls. Second, the co-occurrence patterns of the salivary mycobiome–bacteriome demonstrated negative associations between specific fungal and bacterial taxa identified in the healthy controls, which diminished in the reticular OLP group and even became positive in the erosive OLP group. Moreover, the oral cavities of OLP patients were colonized by dysbiotic oral flora with lower ecological network complexity and decreased fungal–Firmicutes and increased fungal–Bacteroidetes sub-networks. Third, several keystone fungal genera (Bovista, Erysiphe, Psathyrella, etc.) demonstrated significant correlations with clinical scores and IL-17 levels. Thus, we established that fungal dysbiosis is associated with the aggravation of OLP. Fungal dysbiosis could alter the salivary bacteriome or may reflect a direct effect of host immunity, which participates in OLP pathogenesis.},
doi = {10.1038/s41368-019-0045-2},
journal = {International Journal of Oral Science},
number = 2,
volume = 11,
place = {United States},
year = {2019},
month = {7}
}
Web of Science
Works referenced in this record:
Characterization of the Oral Fungal Microbiome (Mycobiome) in Healthy Individuals
journal, January 2010
- Ghannoum, Mahmoud A.; Jurevic, Richard J.; Mukherjee, Pranab K.
- PLoS Pathogens, Vol. 6, Issue 1
Btrim: A fast, lightweight adapter and quality trimming program for next-generation sequencing technologies
journal, August 2011
- Kong, Yong
- Genomics, Vol. 98, Issue 2
Oral lichen planus: An update on etiology, pathogenesis, clinical presentation, diagnosis and management
journal, January 2015
- Gupta, Sonia; Jawanda, ManveenKaur
- Indian Journal of Dermatology, Vol. 60, Issue 3
Medically important bacterial–fungal interactions
journal, March 2010
- Peleg, Anton Y.; Hogan, Deborah A.; Mylonakis, Eleftherios
- Nature Reviews Microbiology, Vol. 8, Issue 5
Immunological Consequences of Intestinal Fungal Dysbiosis
journal, June 2016
- Wheeler, Matthew L.; Limon, Jose J.; Bar, Agnieszka S.
- Cell Host & Microbe, Vol. 19, Issue 6
Scoring system for monitoring oral lichenoid lesions: A preliminary study
journal, June 2005
- Piboonniyom, Siribang-on; Treister, Nathaniel; Pitiphat, Waranuch
- Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology, Vol. 99, Issue 6
Aspergillus in endodontic infection near the maxillary sinus
journal, September 2015
- Gomes, Cinthya Cristina; Pinto, Larissa Christina Costa; Victor, Fernanda Loretti
- Brazilian Journal of Otorhinolaryngology, Vol. 81, Issue 5
Evaluating the Impact of DNA Extraction Method on the Representation of Human Oral Bacterial and Fungal Communities
journal, January 2017
- Vesty, Anna; Biswas, Kristi; Taylor, Michael W.
- PLOS ONE, Vol. 12, Issue 1
attract: A Method for Identifying Core Pathways That Define Cellular Phenotypes
journal, October 2011
- Mar, Jessica C.; Matigian, Nicholas A.; Quackenbush, John
- PLoS ONE, Vol. 6, Issue 10
Richness and diversity of mammalian fungal communities shape innate and adaptive immunity in health and disease: Highlights
journal, October 2014
- Rizzetto, Lisa; De Filippo, Carlotta; Cavalieri, Duccio
- European Journal of Immunology, Vol. 44, Issue 11
Invasive forms of Candida and Aspergillus in sputum samples of pulmonary tuberculosis patients attending the tuberculosis reference laboratory in Ghaemshahr, Northern Iran: An analysis of samples collected during the past 10years
journal, December 2016
- Jabbari amiri, Mohammad Reza; Aghili, Seyed Reza; Shokohi, Tahereh
- International Journal of Mycobacteriology, Vol. 5
Dysbiosis of oral buccal mucosa microbiota in patients with oral lichen planus
journal, March 2017
- He, Y.; Gong, D.; Shi, C.
- Oral Diseases, Vol. 23, Issue 5
Ecological network analysis: network construction
journal, October 2007
- Fath, Brian D.; Scharler, Ursula M.; Ulanowicz, Robert E.
- Ecological Modelling, Vol. 208, Issue 1
The mycobiota: interactions between commensal fungi and the host immune system
journal, May 2014
- Underhill, David M.; Iliev, Iliyan D.
- Nature Reviews Immunology, Vol. 14, Issue 6
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007
- Wang, Q.; Garrity, G. M.; Tiedje, J. M.
- Applied and Environmental Microbiology, Vol. 73, Issue 16
Production of carcinogenic acetaldehyde by Candida albicans from patients with potentially malignant oral mucosal disorders
journal, August 2012
- Gainza-Cirauqui, M. L.; Nieminen, M. T.; Novak Frazer, L.
- Journal of Oral Pathology & Medicine, Vol. 42, Issue 3
Carriage rate and virulence attributes of oral Candida albicans isolates from patients with oral lichen planus: a study in an ethnic Chinese cohort
journal, March 2009
- Zeng, Xin; Hou, Xiaohui; Wang, Zhi
- Mycoses, Vol. 52, Issue 2
Detection and identification of non-Candida albicans species in human oral lichen planus: Non-Candida albicans in oral lichen planus
journal, December 2010
- Masaki, Mika; Sato, Takuichi; Sugawara, Yumiko
- Microbiology and Immunology, Vol. 55, Issue 1
Shaping the oral mycobiota: interactions of opportunistic fungi with oral bacteria and the host
journal, August 2015
- Xu, H.; Dongari-Bagtzoglou, A.
- Current Opinion in Microbiology, Vol. 26
Aspergillus fumigatus in the cystic fibrosis lung: pros and cons of azole therapy
journal, January 2016
- Burgel, Pierre Régis; Paugam, André; Hubert, Dominique
- Infection and Drug Resistance, Vol. Volume 9
Mining the oral mycobiome: Methods, components, and meaning
journal, September 2016
- Diaz, Patricia I.; Hong, Bo-Young; Dupuy, Amanda K.
- Virulence, Vol. 8, Issue 3
Topographic diversity of fungal and bacterial communities in human skin
journal, May 2013
- Findley, Keisha; Oh, Julia; Yang, Joy
- Nature, Vol. 498, Issue 7454
Phasing amplicon sequencing on Illumina Miseq for robust environmental microbial community analysis
journal, June 2015
- Wu, Liyou; Wen, Chongqing; Qin, Yujia
- BMC Microbiology, Vol. 15, Issue 1
Accurate, Rapid Taxonomic Classification of Fungal Large-Subunit rRNA Genes
journal, December 2011
- Liu, Kuan-Liang; Porras-Alfaro, Andrea; Kuske, Cheryl R.
- Applied and Environmental Microbiology, Vol. 78, Issue 5
Defining dysbiosis and its influence on host immunity and disease: How changes in microbiota structure influence health
journal, June 2014
- Petersen, Charisse; Round, June L.
- Cellular Microbiology, Vol. 16, Issue 7
Mycobiota in gastrointestinal diseases
journal, November 2014
- Mukherjee, Pranab K.; Sendid, Boualem; Hoarau, Gautier
- Nature Reviews Gastroenterology & Hepatology, Vol. 12, Issue 2
The Fungal Mycobiome and Its Interaction with Gut Bacteria in the Host
journal, February 2017
- Sam, Qi; Chang, Matthew; Chai, Louis
- International Journal of Molecular Sciences, Vol. 18, Issue 2
A microbial signature for Crohn's disease
journal, February 2017
- Pascal, Victoria; Pozuelo, Marta; Borruel, Natalia
- Gut, Vol. 66, Issue 5
The Skin Microbiome in Atopic Dermatitis and Its Relationship to Emollients
journal, October 2015
- Lynde, Charles W.; Andriessen, Anneke; Bertucci, Vince
- Journal of Cutaneous Medicine and Surgery, Vol. 20, Issue 1
Molecular ecological network analyses
journal, January 2012
- Deng, Ye; Jiang, Yi-Huei; Yang, Yunfeng
- BMC Bioinformatics, Vol. 13, Issue 1
Preliminary analysis of salivary microbiome and their potential roles in oral lichen planus
journal, March 2016
- Wang, Kun; Lu, Wenxin; Tu, Qichao
- Scientific Reports, Vol. 6, Issue 1
Analysis of oral microbial community and Th17-associated cytokines in saliva of patients with oral lichen planus: Oral microbiota and interleukin17 in OLP
journal, March 2015
- Wang, Kun; Miao, Tianyu; Lu, Wenxin
- Microbiology and Immunology, Vol. 59, Issue 3
Bacteriome and Mycobiome Interactions Underscore Microbial Dysbiosis in Familial Crohn’s Disease
journal, September 2016
- Hoarau, G.; Mukherjee, P. K.; Gower-Rousseau, C.
- mBio, Vol. 7, Issue 5
The presence of bacteria within tissue provides insights into the pathogenesis of oral lichen planus
journal, July 2016
- Choi, Yun Sik; Kim, Yunji; Yoon, Hye-Jung
- Scientific Reports, Vol. 6, Issue 1
Unstimulated whole salivary flow rate and anxiolytics intake are independently associated with oral Candida infection in patients with oral lichen planus
journal, July 2013
- Bokor-Bratic, Marija; Cankovic, Milos; Dragnic, Natasa
- European Journal of Oral Sciences, Vol. 121, Issue 5
Anaerobic Bacteria Grow within Candida albicans Biofilms and Induce Biofilm Formation in Suspension Cultures
journal, October 2014
- Fox, Emily P.; Cowley, Elise S.; Nobile, Clarissa J.
- Current Biology, Vol. 24, Issue 20
Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009
- Schloss, P. D.; Westcott, S. L.; Ryabin, T.
- Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
Role of distinct CD4 + T helper subset in pathogenesis of oral lichen planus
journal, December 2015
- Wang, Hui; Zhang, Dunfang; Han, Qi
- Journal of Oral Pathology & Medicine, Vol. 45, Issue 6
The microbiology of oral lichen planus: Is microbial infection the cause of oral lichen planus?
journal, October 2017
- Baek, K.; Choi, Y.
- Molecular Oral Microbiology, Vol. 33, Issue 1
Oral Candida colonization and oral lichen planus
journal, May 2017
- Bombeccari, Gian Paolo; Giannì, Aldo Bruno; Spadari, Francesco
- Oral Diseases, Vol. 23, Issue 7
Prevalence of Candida spp., xerostomia, and hyposalivation in oral lichen planus - A controlled study
journal, May 2013
- Artico, G.; Freitas, Rs; Santos Filho, Am
- Oral Diseases, Vol. 20, Issue 3
Redefining the Human Oral Mycobiome with Improved Practices in Amplicon-based Taxonomy: Discovery of Malassezia as a Prominent Commensal
journal, March 2014
- Dupuy, Amanda K.; David, Marika S.; Li, Lu
- PLoS ONE, Vol. 9, Issue 3
IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance
journal, October 2007
- Zelante, Teresa; De Luca, Antonella; Bonifazi, Pierluigi
- European Journal of Immunology, Vol. 37, Issue 10
Temperature mediates continental-scale diversity of microbes in forest soils
journal, July 2016
- Zhou, Jizhong; Deng, Ye; Shen, Lina
- Nature Communications, Vol. 7, Issue 1
Malignant transformation of oral lichen planus and oral lichenoid lesions: A meta-analysis of 20095 patient data
journal, May 2017
- Aghbari, Sana Maher Hasan; Abushouk, Abdelrahman Ibrahim; Attia, Attia
- Oral Oncology, Vol. 68
Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population
journal, May 2017
- Koliada, Alexander; Syzenko, Ganna; Moseiko, Vladislav
- BMC Microbiology, Vol. 17, Issue 1
Community differentiation of the cutaneous microbiota in psoriasis
journal, December 2013
- Alekseyenko, Alexander V.; Perez-Perez, Guillermo I.; De Souza, Aieska
- Microbiome, Vol. 1, Issue 1
The Relation between Oral Candida Load and Bacterial Microbiome Profiles in Dutch Older Adults
journal, August 2012
- Kraneveld, Eefje A.; Buijs, Mark J.; Bonder, Marc J.
- PLoS ONE, Vol. 7, Issue 8
A prospective study of findings and management in 214 patients with oral lichen planus
journal, December 1991
- Silverman, Sol; Gorsky, Meir; Lozada-Nur, Francina
- Oral Surgery, Oral Medicine, Oral Pathology, Vol. 72, Issue 6
IL-17 Receptor Signaling in Oral Epithelial Cells Is Critical for Protection against Oropharyngeal Candidiasis
journal, November 2016
- Conti, Heather R.; Bruno, Vincent M.; Childs, Erin E.
- Cell Host & Microbe, Vol. 20, Issue 5
Cutting Edge: IL-17–Secreting Innate Lymphoid Cells Are Essential for Host Defense against Fungal Infection
journal, December 2012
- Gladiator, André; Wangler, Nicolette; Trautwein-Weidner, Kerstin
- The Journal of Immunology, Vol. 190, Issue 2
Works referencing / citing this record:
Dysbiosis of saliva microbiome in patients with oral lichen planus
journal, April 2020
- Yu, Fei Yan; Wang, Qian Qian; Li, Miao
- BMC Microbiology, Vol. 20, Issue 1