Abstract
Squamous cell carcinoma of the oral (mobile) tongue (OMTC), a non-human papilloma virus-associated oral cancer, is rapidly increasing without clear etiology. Poor oral hygiene has been associated with oral cancers, suggesting that oral bacteriome (bacterial community) and mycobiome (fungal community) could play a role. While the bacteriome is increasingly recognized as an active participant in health, the role of the mycobiome has not been studied in OMTC. Tissue DNA was extracted from 39 paired tumor and adjacent normal tissues from patients with OMTC. Microbiome profiling, principal coordinate, and dissimilarity index analyses showed bacterial diversity and richness, and fungal richness, were significantly reduced in tumor tissue (TT) compared to their matched non-tumor tissues (NTT, P<0.006). Firmicutes was the most abundant bacterial phylum, which was significantly increased in TT compared to NTT (48% vs. 40%, respectively; P=0.004). Abundance of Bacteroidetes and Fusobacteria were significantly decreased in TT compared to matched NTT (P≤0.003 for both). Abundance of 22 bacterial and 7 fungal genera was significantly different between the TT and NTT, including Streptococcus, which was the most abundant and significantly increased in the tumor group (34% vs. 22%, P<0.001). Abundance of fungal genus Aspergillus in TT correlated negatively with bacteria (Actinomyces, Prevotella, Streptococcus), but positively with Aggregatibacter. Patients with high T-stage disease had lower mean differences between TT and NTT compared with patients with low T-stage disease (0.07 vs. 0.21, P=0.04). Our results demonstrate differences in bacteriome and mycobiome between OMTC and their matched normal oral epithelium, and their association with T-stage.
Highlights
Squamous cell carcinoma of the oral tongue, arising at the anterior two-thirds of the tongue, has been rapidly increasing and has become the second most common malignancy in the oral cavity [1, 2]
The total number of reads associated with bacteriome and mycobiome were 3,093,772 and 4,550,121 respectively, which were passed through quality filters, resulting in 1,997,240 and 1,149,569 sequences used for operational taxonomic units (OTUs) assignments (26,279 and 14,369 mean sequences per sample, respectively)
Principal coordinate analysis (PCO), clustered dendograms, and Bray-Curtis dissimilarity index analyses showed that the tumor and non-tumor samples exhibited considerable overlap in clustering at both phylum and genus levels, for bacterial and fungal biota (Figure 1)
Summary
Squamous cell carcinoma of the oral (mobile) tongue, arising at the anterior two-thirds of the tongue, has been rapidly increasing and has become the second most common malignancy in the oral cavity [1, 2]. While human papillomavirus (HPV) is etiologic for the increased incidence of base of tongue tumors (89% HPV+), HPV is rarely found (2.3%) in oral tongue cancer [3,4,5]. The etiology of this increasingly common disease has remained unclear, and warrants investigation for discovery of additional pathogenic pathways. In/on the human body, bacterial cells outnumber human cells 10:1, with the total bacteriome-to-human gene content ratio approximating 350:1. Studying the microbiota was largely limited to culturable organisms before the advent of metagenomics, the detection of the genomic content of microbes. Metagenomics allows for detection of both culturable and nonculturable microbes, permitting us to describe bacterial communities
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