Convergent dysbiosis of upper aerodigestive microbiota between patients with esophageal and oral cavity squamous cell carcinoma

Abstract

The bidirectional association between primary esophageal squamous cell carcinoma (ESCC) and oral cavity squamous cell carcinoma (OSCC) suggests common risk factors and oncogenic molecular processes but it is unclear whether these two cancers display similar patterns of dysbiosis in their upper aerodigestive microbiota (UADM). We conducted a case‐control study to characterize the microbial communities in esophageal lavage samples from 49 ESCC patients and oral rinse samples from 91 OSCC patients using 16S rRNA V3‐V4 amplicon sequencing. Compared with their respective non‐SCC controls from the same anatomical sites, 32 and 45 discriminative bacterial genera were detected in ESCC and OSCC patients, respectively. Interestingly, 20 of them were commonly enriched or depleted in both types of cancer, suggesting a convergent niche adaptation of upper aerodigestive SCC‐associated bacteria that may play important roles in the pathogenesis of malignancies. Notably, Fusobacterium, Selenomonas, Peptoanaerobacter and Peptostreptococcus were enriched in both ESCC and OSCC, whereas Streptococcus and Granulicatelia were commonly depleted. We further identified Fusobacterium nucleatum as the most abundant species enriched in the upper aerodigestive SCC microenvironment, and the higher relative abundances of Selenomonas danae and Treponema maroon were positively correlated with smoking. In addition, predicted functional analysis revealed several depleted (eg, lipoic acid and pyruvate metabolism) and enriched (eg, RNA polymerase and nucleotide excision repair) pathways common to both cancers. Our findings reveal a convergent dysbiosis in the UADM between patients with ESCC and OSCC, suggesting a shared niche adaptation of host‐microbiota interactions in the pathogenesis of upper aerodigestive tract malignancies.

Integrative analysis reveals associations between oral microbiota dysbiosis and host genetic and epigenetic aberrations in oral cavity squamous cell carcinoma

“…Demultiplexed short 16S reads passing quality filtering were imported into QIIME2 (v2021.4) to generate an amplicon sequence variant (ASV) table as previously described 6 . The representative reads were further assigned at the species level using pplacer by inserting into a phylogenetic tree inferred from complete sequences of the bacterial 16S rRNA gene to maximize phylogenetic likelihood 49 , 50 . ASVs with a total count >10 after removing reads assigned to archaea, mitochondria or chloroplasts were retained, with operational taxonomic unit (OTU) count tables showing the bacterial reads per sample at different taxonomic levels.…”

Promising dawn in tumor microenvironment therapy: engineering oral bacteria

“… 243 Except for colorectal cancer, after performing 16 S rRNA amplicon sequencing on 54 oral swab samples from OSCC patients, researchers found Peptostreptococcus was significantly enriched in OSCC recurrence, and it demonstrated a high diagnostic power or microbial marker for OSCC metastasis. 22 , 244 – 246 Furthermore, a meta-analysis has uncovered the augmented presence of the opportunistic pathobiont Peptostreptococcus in gastric cancer, with its abundance increasing progressively during the cancer progression. 247 Existing microbial data based on 16 S rRNA analysis have demonstrated substantial variations in Peptostreptococcus levels between gastric and nongastric cancer cases, showcasing its potential diagnostic efficacy and broad applicability for patients afflicted with gastric cancer.…”