Metagenomic and culture-based genomics reveal virulence and resistance risks in Manila clam microbiomes

IF 5.4 1区农林科学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY

Food microbiology Pub Date : 2026-06-01 Epub Date: 2025-12-04 DOI:10.1016/j.fm.2025.105001

Yaling Wang , Linan He , Xing Hu , Yuhan Guan , Xiangnan Chen , Jiahui Du , Jiayan Chen , Chensheng Ma , Lianwei Ye

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Abstract

Bivalves are important aquaculture products whose safety is shaped by their microbiomes. Here, we present the first comprehensive characterization of Manila clam (Ruditapes philippinarum) microbiomes using both shotgun metagenomics (6 clams) and culture-based genomics (169 isolates, 40 draft genomes), integrating community, functional, and antimicrobial resistance profiling. Communities were dominated by Proteobacteria (99.3–99.9 %), with Pseudoalteromonas and Vibrio collectively accounting for 74.9–99.7 % and showing strong inverse correlations, defining Pseudoalteromonas-dominated, Vibrio-dominated, and mixed states. Species richness ranged from 22 to 180 per sample. Recognized human pathogens occurred at low abundance (<0.3 %), including Vibrio parahaemolyticus, Vibrio alginolyticus, and Photobacterium damselae, while opportunistic vibrios expanded in some clams (e.g., Vibrio cyclitrophicus 57.9 %). We reconstructed 34 high-quality MAGs, seven resolved to species (Pseudoalteromonas tetraodonis, V. cyclitrophicus, Shewanella aquimarina), alongside unclassified lineages. Metagenomes encoded 14 virulence-factor categories with 2281 subtypes, and isolate genomes added 93 further subtypes, including high-virulence loci in Escherichia coli and type III secretion genes in V. parahaemolyticus. Resistomes spanned 18 antibiotic classes with 511 subtypes; isolates contributed 22 additional antibiotic resistance genes(ARGs), including extended-spectrum β-lactamases (bla_CTX-M-102) and bla_NDM-1. Four carbapenemase-producing isolates (three Shewanella algae, one V. parahaemolyticus) carried blaNDM-1 on IncC plasmids, with the V. parahaemolyticus plasmid transferable to E. coli. Two P. tetraodonis MAGs encoded RiPP-like and terpene biosynthetic clusters plus phage-defense systems, consistent with Vibrio suppression. These findings demonstrate that clam microbiomes fluctuate between protective (Pseudoalteromonas) and pathogenic (Vibrio–Shewanella) states, providing a first integrated framework for assessing microbial risk, antimicrobial resistance, and food safety interventions in bivalve aquaculture.

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宏基因组学和基于培养的基因组学揭示了马尼拉蛤微生物群的毒力和耐药性风险

双壳类是重要的水产养殖产品，其安全性取决于其微生物群。在这里，我们首次使用散弹枪宏基因组学（6只蛤）和基于培养的基因组学（169个分离株，40个草稿基因组）对马尼拉蛤（Ruditapes philippinarum）微生物组进行了全面的描述，整合了群落、功能和抗菌素耐药性分析。群落以变形菌门（99.3 - 99.9%）为主，假互变单胞菌和弧菌共占74.9 - 99.7%，呈较强的负相关关系，分别为假互变单胞菌为主、弧菌为主和混合状态。物种丰富度在22 ~ 180种之间。已知的人类病原体以低丰度（0.3%）出现，包括副溶血性弧菌、溶藻弧菌和豆selae光杆菌，而机会性弧菌在一些蛤蜊中扩张（例如，嗜环弧菌57.9%）。我们重建了34个高质量的mag，其中7个分解为种（四齿异假单胞菌，环状营养菌，水生希瓦氏菌），以及未分类的谱系。宏基因组编码了14个毒力因子类别，共2281个亚型，分离基因组增加了93个亚型，包括大肠杆菌的高毒力位点和副溶血性弧菌的III型分泌基因。抗性体跨越18个抗生素类，有511个亚型；分离株贡献了22个额外的抗生素耐药基因（ARGs），包括广谱β-内酰胺酶（blaCTX-M-102）和blaNDM-1。4株产碳青霉烯酶的分离株（3株希瓦氏菌藻类，1株副溶血性弧菌）在IncC质粒上携带blaNDM-1，其中副溶血性弧菌质粒可转移到大肠杆菌中。两个P. tetraodonis MAGs编码ripp样和萜烯生物合成簇以及噬菌体防御系统，与弧菌抑制一致。这些发现表明，蛤的微生物群在保护性（假互变单胞菌）和致病性（希瓦氏弧菌）状态之间波动，为评估双壳类水产养殖中的微生物风险、抗菌素耐药性和食品安全干预措施提供了第一个综合框架。

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来源期刊

Food microbiology 工程技术-生物工程与应用微生物

CiteScore

11.30

自引率

3.80%

发文量

179

审稿时长

44 days

期刊介绍： Food Microbiology publishes original research articles, short communications, review papers, letters, news items and book reviews dealing with all aspects of the microbiology of foods. The editors aim to publish manuscripts of the highest quality which are both relevant and applicable to the broad field covered by the journal. Studies must be novel, have a clear connection to food microbiology, and be of general interest to the international community of food microbiologists. The editors make every effort to ensure rapid and fair reviews, resulting in timely publication of accepted manuscripts.