Metagenomics reveals the risk of antibiotic resistance genes and co-occurrence in Chinese traditional fermented bean products

The natural symbiotic fermentation by diverse microorganisms significantly influences the quality and safety of traditional fermented soybean products, imparting them with distinct flavor and nutrition. Economic growth, population increase, and intensive production practices in crop-producing regions have altered bacterial communities and facilitated the accumulation of antibiotic resistance genes. Although shotgun metagenomic sequencing is widely employed for resistance gene analysis in environmental studies, the comprehensive understanding of bacterial communities, epidemiological distribution, coexistence patterns, and host information related to antibiotic resistance genes in fermented bean products remains incompletely elucidated. We performed a comprehensive metagenomic sequencing study on locally characteristic traditional fermented bean products (such as sufu and bean paste) across 10 provinces and cities in China. Our investigation systematically analyzed microbial communities and antibiotic resistance profiles in fermented bean products, shedding light on the coexistence patterns and host information of resistance genes. The study findings revealed the presence of bacteria with potential health risks. We identified 1854 distinct subtypes of antibiotic resistance genes (ARGs) resistant to over 20 antibiotics. To assess the potential harm of these ARGs, we established a "Risk ARG Library for Fermented Bean Products" comprising 87 ARGs primarily hosted by Escherichia, Citrobacter, and Raoultella. This suggests their significant role in hosting and potentially transmitting these harmful resistance genes. In summary, our study enhances the comprehensive understanding of resistance profiles in fermented bean products, crucial for preventing and managing foodborne multidrug-resistant bacteria.

多种微生物介导的自然共生发酵，对传统发酵大豆制品的品质与安全具有显著调控作用，同时赋予其独特的风味与营养特性。作物主产区的经济增长、人口扩张与集约化生产模式，已显著改变了当地细菌群落结构，并推动了抗生素抗性基因的累积。尽管鸟枪宏基因组测序（shotgun metagenomic sequencing）已广泛应用于环境研究中的抗性基因分析，但学界对发酵豆制品中细菌群落、抗生素抗性基因（antibiotic resistance genes, ARGs）的流行病学分布、共存模式及其宿主信息的全面认知仍有待进一步阐明。本研究针对中国10个省市的本土特色传统发酵豆制品（如腐乳（sufu）、豆酱）开展了系统性宏基因组测序分析，系统解析了发酵豆制品中的微生物群落结构与抗生素抗性谱，阐明了抗性基因的共存模式与宿主关联信息。研究结果显示，部分受试样本中存在具有潜在健康风险的细菌类群。本次研究共鉴定出1854种不同亚型的抗生素抗性基因（ARGs），可对20余种抗生素产生耐药性。为评估这些ARGs的潜在危害，我们构建了“发酵豆制品风险抗性基因库（Risk ARG Library for Fermented Bean Products）”，其中包含87种主要由埃希氏菌属（Escherichia）、柠檬酸杆菌属（Citrobacter）以及拉乌尔菌属（Raoultella）宿主携带的ARGs，这表明上述菌属在携带并潜在传播这些有害抗性基因的过程中发挥了关键作用。综上，本研究深化了学界对发酵豆制品抗性特征的全面认知，对食源性多重耐药菌的防控与管理具有重要的现实意义。