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Increased virulence of the oral microbiome in oral squamous cell carcinoma revealed by metatranscriptome analyses
Open accessAbstract
Oral squamous cell carcinoma (OSCC) is the most prevalent and most commonly studied oral cancer. However, there is a void regarding the role that the oral microbiome may play in OSCC. Although the relationship between microbial community composition and OSCC has been thoroughly investigated, microbial profiles of the human microbiome in cancer are understudied. Here we performed a small pilot study of community-wide metatranscriptome analysis to profile mRNA expression in the entire oral microbiome in OSCC to reveal molecular functions associated with this disease. Fusobacteria showed a statistically significantly higher number of transcripts at tumour sites and tumour-adjacent sites of cancer patients compared to the healthy controls analysed. Regardless of the community composition, specific metabolic signatures were consistently found in disease. Activities such as iron ion transport, tryptophanase activity, peptidase activities and superoxide dismutase were over-represented in tumour and tumour-adjacent samples when compared to the healthy controls. The expression of putative virulence factors in the oral communities associated with OSCC showed that activities related to capsule biosynthesis, flagellum synthesis and assembly, chemotaxis, iron transport, haemolysins and adhesins were upregulated at tumour sites. Moreover, activities associated with protection against reactive nitrogen intermediates, chemotaxis, flagellar and capsule biosynthesis were also upregulated in non-tumour sites of cancer patients. Although they are preliminary, our results further suggest that Fusobacteria may be the leading phylogenetic group responsible for the increase in expression of virulence factors in the oral microbiome of OSCC patients. A search of the oral microbiome has revealed a group of bacteria closely associated with the most common type of oral cancer, and whose activity may play a role in its development. Oral squamous cell carcinoma (OSCC) has been linked to tobacco and alcohol consumption, but there’s increasing interest in the role bacteria might play in its initiation and growth. To better understand the behaviour of the various microbes present in the mouths of healthy people and those with OSCC, Jorge Frias-Lopez at the University of Florida in Gainesville and his colleagues carried out a metatranscriptome analysis, which identifies the most actively expressed genes. This revealed significant differences in their microbial communities, with Fusidobacteria particularly enriched and hyperactive in patients with OSCC. The team also identified microbial activities that were consistently associated with cancer.
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“This is demonstrated by the association of various disease states with the oral microbiome, including not only caries and periodontal disease but also oral, esophageal, pancreatic, and colorectal cancers, cardiovascular disease, and inflammatory bowel disease.147, 148, 149, 150, 151, 152, 153”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [147]
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InfluentialDysbiosis of Oral Microbiota During Oral Squamous Cell Carcinoma Development
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BackgroundMicrobiomes, Their Function, and Cancer: How Metatranscriptomics Can Close the Knowledge Gap
Aitmanaitė, L., Širmonaitis, K., & Russo, G. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241813786 · Cited by 28
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BackgroundInfluentialPotential role of epithelial–mesenchymal transition induced by periodontal pathogens in oral cancer
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“30 Noticeably, the results of different studies are not completely consistent.”
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Oral microbiome and oral cancer – The probable nexus
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Heterogeneous lineage-specific arginine deiminase expression within dental microbiome species
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“We chose this isolation kit as it is designed to efficiently isolate small RNAs ( 200 nt), as well as total RNA, which play a crucial role in regulating bacterial global gene expression and are routinely used for microbiome studies (74–76).”
MethodChiscuzzu, F., Crescio, C., Varrucciu, S., Rizzo, D., Sali, M., Delogu, G., & Bussu, F. (2025) · Cancers · doi:10.3390/cancers17020171 · Cited by 22
“In 2018, Yost et al. carried out a meta-transcriptome analysis to profile mRNA expression in the oral microbiome in OSCC [68].”
Dysbiosis of Oral Microbiome: A Key Player in Oral Carcinogenesis? A Critical Review
Devaraja, K., & Aggarwal, S. (2025) · Biomedicines · doi:10.3390/biomedicines13020448 · Cited by 25
“…collected, the collection procedure (rinse, passive wash, swab, scrapping or biopsy) the pre-collection steps (use of oral washes, type of reagent used), and the selection of controls (normal healthy controls or contralateral normal mucosal lesions from cancer patients) [89,96,121,122,159].”
Arthur, R. A., Bezerra, R. D. S., Ximenez, J. P. B., Merlin, B. L., Morraye, R. D. A., Neto, J. V., Fava, N. D. M. N., Figueiredo, D. L. A., de Biagi, C. A. O., Summer Course 2020 group, et al. (2021) · Brazilian Journal of Microbiology · doi:10.1007/s42770-021-00491-6 · Cited by 21
“hanced pattern for iron transport in microbiomes associated with OSCC [78].”
BackgroundSantacroce, L., Muzio, E. L., Bottalico, L., Spirito, F., Charitos, I. A., Passarelli, P. C., & Jirillo, E. (2022) · Endocrine Metabolic & Immune Disorders - Drug Targets · doi:10.2174/1871530322666220629101357 · Cited by 22
Baraniya, D., Chitrala, K. N., & Al-Hebshi, N. N. (2022) · Journal of Oral Microbiology · doi:10.1080/20002297.2022.2073866 · Cited by 21
The Microbiome’s Influence on Head and Neck Cancers
Dorobisz, K., Dorobisz, T. A., & Zatoński, T. (2023) · Current Oncology Reports · doi:10.1007/s11912-022-01352-7 · Cited by 21
Microbial community alteration in tongue squamous cell carcinoma
Ye, P., Liu, Y., Cai, Y.-J., Yang, H., Xu, H., & Lu, Z.-Y. (2021) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-021-11593-4 · Cited by 18
Jain, V. K., Baraniya, D., El-Hadedy, D. E., Chen, T., Slifker, M. J., Alakwaa, F., Cai, K. Q., Chitrala, K. N., Fundakowski, C., & Al-Hebshi, N. N. (2023) · Cancer Research Communications · doi:10.1158/2767-9764.crc-22-0349 · Cited by 17
Dumitrescu, R., Bolchis, V., Fratila, A. D., Jumanca, D. E., Buzatu, B. L. R., Sava-Roşianu, R., Alexa, V. T., Găluşcan, A., & Bălean, O. (2025) · Microorganisms · doi:10.3390/microorganisms13020373 · Cited by 18
Khatoon, E., Hegde, M., Kumar, A., Daimary, U. D., Sethi, G., Bishayee, A., & Kunnumakkara, A. B. (2022) · Archives of Pharmacal Research · doi:10.1007/s12272-022-01398-y · Cited by 18
Association between oral microflora and gastrointestinal tumors (Review)
Li, X., Zhu, S., Zhang, T., & Chen, X. (2021) · Oncology Reports · doi:10.3892/or.2021.8111 · Cited by 19
“This is consistent with the conclusion of Yost et al (55), which indicated that Fusobacteria contained a significantly higher number of transcripts in patients with cancer than in healthy controls at tumor sites and tumor‑adjacent sites.”
Diwan, P., Nirwan, M., Bahuguna, M., Kumari, S. P., Wahlang, J., & Gupta, R. K. (2023) · Pathogens · doi:10.3390/pathogens12080996 · Cited by 20
Standardized studies of the oral microbiome: From technology‐driven to hypothesis‐driven
Gao, C., Li, X., Zhao, X., Yang, P., Wang, X., Chen, X., Chen, N., & Chen, F. (2022) · iMeta · doi:10.1002/imt2.19 · Cited by 15
Multi-omics analysis of fecal samples in colorectal cancer Egyptians patients: a pilot study
Khattab, R. H., Abo-Hammam, R. H., Salah, M., Hanora, A., Shabayek, S., & Zakeer, S. (2023) · BMC Microbiology · doi:10.1186/s12866-023-02991-x · Cited by 15
“Yost et al., 2018 reported that Dialister was more active in the tumor sites [48].”
BackgroundCrowley, C., Selvaraj, A., Hariharan, A., Healy, C. M., & Moran, G. P. (2024) · Microbial Genomics · doi:10.1099/mgen.0.001217 · Cited by 15
“The virulence landscape at oral tumour sites has also been investigated and it has been found, using meta-transcriptomic analysis, that pathways including iron acquisition, oxidative stress response and peptidase activity were increased at OSCC sites [20].”
Insights into the oral microbiota in human systemic cancers
Su, L., Yang, R., Sheng, Y., Ullah, S., Zhao, Y., Shunjiayi, H., Zhao, Z., & Wang, Q. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1369834 · Cited by 15
Zanetta, P., Squarzanti, D. F., Sorrentino, R., Rolla, R., Valletti, P. A., Garzaro, M., Dell’Era, V., Amoruso, A., & Azzimonti, B. (2021) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2021.1872487 · Cited by 15
He, B., Cao, Y., Zhuang, Z., Deng, Q., Qiu, Y., Pan, L., Zheng, X., Shi, B., Lin, L., & Chen, F. (2024) · Head & Neck · doi:10.1002/hed.27795 · Cited by 14
“32 However, some different genera found in this study did not fully overlap with those found in the United States, 33 Australia, 34 Japan, 35 or Sri Lanka, 29 such as Fusobacterium and Porphyromonas were also reported to be more abundant in the oral cancer group.”
ResultAgurto, M. I. G., Valenzuela, N. O., Canedo-Marroquín, G., Espinoza, D., & Tortora, S. C. (2024) · Cancers · doi:10.3390/cancers16203545 · Cited by 16
“Additionally, F. nucleatum boosts the production of haemolysins and adhesins and strengthens its iron transport system to support DNA synthesis and cellular respiration, thereby promoting microbial survival and proliferation within the tumour environment [101].”
BackgroundDóra, D., Kiraly, P., Somodi, C., Ligeti, B., Dulka, E., Gálffy, G., & Lohinai, Z. (2024) · Journal of Translational Medicine · doi:10.1186/s12967-024-05835-y · Cited by 16
“In addition, it was reported in patients with oral squamous cell carcinoma (OSCC) evaluated by MTR analysis, that an increase in peptidase activity, oxidative stress, and iron acquisition is overrepresented in tumor samples compared to healthy tissues [19].”
Araújo, L. L., Lourenço, T. G. B., & Colombo, A. P. V. (2023) · Journal of Applied Oral Science · doi:10.1590/1678-7757-2022-0359 · Cited by 17
Starska, K. (2025) · Cancers · doi:10.3390/cancers17213478 · Cited by 14
“Yost et al. [118] assessed the mRNA expression profile across the entire oral microbiome in OSCC with the aim of identifying specific molecular and metabolic functions associated with this disease.”
Selvaraj, A., McManus, G., Healy, C. M., & Moran, G. P. (2024) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2024.1417946 · Cited by 13
Li, X., Jia, Y., Li, Y., Hei, H., Zhang, S., & Qin, J. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1582166 · Cited by 12
Ahmad, S., Jayamanne, D. T., Bergamin, S., Lawless, A. K., Guminski, A. D., Lee, A. V., Yuile, A., Wheeler, H., Eade, T., Back, M., et al. (2025) · Cancers · doi:10.3390/cancers17162667 · Cited by 18
“Fusobacterium , reported in 12 studies, was consistently enriched in patients, re-inforcing its role in epithelial invasion, immune modulation, and inflammation-driven tumor progression [44,45].”
Emerging implications of bacterial biofilm in cancer biology: Recent updates and major perspectives
Kushwaha, M., Nukala, V., Singh, A. K., Makharia, G. K., Mohan, A., Kumar, A., & Dalal, N. (2024) · Gut Microbes Reports · doi:10.1080/29933935.2024.2339270 · Cited by 13
Ramos, R. T., Sodré, C. S., Rodrigues, P. M. G., da Silva, A. M. P., Fuly, M. S., dos Santos, H. F., Gonçalves, L. S., Ferreira, D. D. C., & Ribeiro, M. G. (2020) · Oral and Maxillofacial Surgery · doi:10.1007/s10006-020-00873-4 · Cited by 12
Liu, X., Li, X., Xie, M., Guo, J.-Y., Zheng, X., Shi, S., Cui, Q., Zhang, D., Zhang, Z., & Wang, Z. (2023) · Journal of Stomatology Oral and Maxillofacial Surgery · doi:10.1016/j.jormas.2023.101736 · Cited by 12
The Function of the Oral Microbiome in Health and Disease
Frias‐Lopez, J., & Duran-Pinedo, A. E. (2020) · Springer eBooks · doi:10.1007/978-3-030-42990-4_10 · Cited by 12
Self-citationShitozawa, Y., Haro, K., Ogawa, M., Miyawaki, A., Saito, M., & Fukuda, K. (2022) · Scientific Reports · doi:10.1038/s41598-022-21031-8 · Cited by 11
Alteration of oral bacteriome of smokeless tobacco users and their association with oral cancer
Sajid, M., Sharma, P., Srivastava, S., Hariprasad, R., Singh, H., & Bharadwaj, M. (2023) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-023-12534-z · Cited by 12
Reyes, M., Urra, H., & Peña‐Oyarzún, D. (2025) · Frontiers in Oral Health · doi:10.3389/froh.2025.1575721 · Cited by 10
Recent advancements in artificial intelligence‐powered cancer prediction from oral microbiome
Soghli, N., Khormali, A., Mahboubi, D., Peng, A., & Miguez, P. A. (2025) · Periodontology 2000 · doi:10.1111/prd.70000 · Cited by 13
Cell Junctions in Periodontal Health and Disease: An Insight
Puzhankara, L., Rajagopal, A., Kedlaya, M. N., Karmakar, S., Nayak, N., & Shanmugasundaram, S. (2023) · European Journal of Dentistry · doi:10.1055/s-0043-1775726 · Cited by 8
“This results in the inhibition of E-cadherin, upregulation of vimentin, β -catenin, and matrix metalloproteinases (MMPs) 54 with the transition from the epithelial to the mesenchymal phenotype affecting the integrity of the intercellular junctions of the epithelium.”
Raudenská, M., Bugajová, M., Kalfeřt, D., Plzák, J., Šubrt, A., Tesařová, P., & Masařík, M. (2024) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2024.189216 · Cited by 8
Relationships between oral microbiome and head and neck squamous cell carcinoma: a systematic review
Guévelou, J. L., Larnaudie, A., Béné, M. C., Cocherie, T., Perazzi, M., El-Houat, Y., Kammerer, E., Bastit, V., & Pointreau, Y. (2025) · Oral Oncology · doi:10.1016/j.oraloncology.2025.107571 · Cited by 9
Guan, Z., Qi, H., & Feng, Q. (2025) · Open Research (University of Surrey) · doi:10.1002/viw.20240153 · Cited by 6
Metadata
- Authors
- Yost, S., Stashenko, P., Choi, Y., Kukuruzinska, M., Genco, C. A., Salama, A., Weinberg, E. O., Kramer, C. D., & Frias-Lopez, J.
- Affiliations
- The Forsyth Institute (US)
- Boston University (US)
- Tufts University (US)
- ORCID
- Venue
- International Journal of Oral Science
- Published
- 2018-11-12
- Volume
- 10
- Issue
- 4
- Pages
- 32-32
- ISSN
- 1674-2818 (ISSN-L)
- 2049-3169
- PMC
- PMC6232154
- OpenAlex
- W2901836693
- Cited by
- 144
- References
- 73
- Citations by year
- 2026: 12 · 2025: 24 · 2024: 13 · 2023: 25 · 2022: 28 · 2021: 18 · 2020: 20 · 2019: 4
- FWCI
- 12.07
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- International Journal of Oral Science (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- Boston University (Evans Center for Interdisciplinary Biomedical Research ARC)
- Forsyth Institute Pilot Grant
- Topics
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Health Sciences › Medicine › Otorhinolaryngology › Head and Neck Cancer Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- oral squamous cell carcinoma, oral microbiota, metatranscriptomics, Fusobacteria, virulence factors, microbial gene expression, iron transport, tryptophanase, superoxide dismutase, capsule biosynthesis, flagellar biosynthesis, chemotaxis, hemolysin, adhesins, reactive nitrogen intermediates
- MeSH terms
- Carcinoma, Squamous Cell, Humans, Mouth Neoplasms, Phylogeny, Pilot Projects, RNA, Messenger, Virulence, Virulence Factors, Metagenome, Transcriptome, Microbiota
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