Restaurant occupational exposure affects the profiles of oral and gut pathobiomes and resistomes

Mengyu Wang¹Xueqin Li¹Xiao Liu²Ying Ye³Peng Zhou⁴Yifan Liu¹Liudan Zhu⁴Wei Wei²Zhenpeng Li²Zhe Li²Ruiheng Wu²Yao Peng²Ziyu Liu²Xin Lu^2*Jiayong Zhao³Biao Kan²

• ¹Shandong University, Jinan, China
• ²Chinese Center for Disease Control and Prevention, Beijing, China
• ³Henan Center for Disease Control and Prevention, Zhengzhou, China
• ⁴Zhengzhou Center for Disease Control and Prevention, Zhengzhou, China

Introduction: Restaurant occupational exposure refers to contact with food-processing environments, raw materials, and customers, which may influence the composition of the human microbiome. Differences and associations between human oral and gut pathobiome and their resistomes under restaurant occupational exposure remain unclear. We conducted a comprehensive metagenomic analysis of paired oral and fecal samples from Front-of-House (FOH) workers and Back-of-House (BOH) workers to elucidate the effects of occupational exposure in the restaurant environment on oral and gut pathobiome, antimicrobial resistance genes (ARGs), virulence factors (VFs), and mobile genetic elements (MGEs). Methods: We collected the oral and fecal samples from 35 FOH and 37 BOH workers across 24 Chinese restaurants in Zhengzhou, Henan, China. The diversity and relative abundances of microbial species, ARGs, VFs, and MGEs were compared. Clonal strains from paired oral and fecal samples were analyzed. The serovars of Salmonella were determined using the ucgMLST. Finally, we used the O2PLS method to explore relationships among ARG subtypes, bacterial communities (species-level), MGEs (subtype-level), and plasmids. Results: The gut microbiome acts as the primary reservoir, exhibiting greater alpha diversity and a higher burden of pathogens/resistomes (including high-risk Rank_I genes). In contrast, the oral microbiome was more sensitive to occupational differences. Significant beta diversity variations in microbiomes, antimicrobial resistance genes (ARGs), and virulence factors were observed exclusively in oral samples. Notably, Salmonella Typhimurium was significantly more prevalent in the oral cavity of BOH workers (R2 = 0.032, p = 0.047), indicating their potential role as intermediaries in foodborne pathogen transmission. Strain-level analysis confirmed that clonal strains of the opportunistic pathogen and probiotics were shared between the oral cavity and the gut. O2PLS analysis identified plasmids as the main correlates of ARGs. Discussion: While the gut serves as the primary reservoir for pathogens/resistomes, restaurant occupational exposure distinctly shapes oral microbial/resistome profiles, underscoring the critical need for reinforced hygiene management, particularly for BOH workers, to mitigate pathogen and resistance transmission.