Unit of Microbiome Science and Biotechnology, Department of Pharmacy and Biotechnology, University of Bologna, via Belmeloro 6, 40126 Bologna, Italy; Fano Marine Center, the Inter-Institute Center for Research on Marine Biodiversity, Resources and Biotechnologies, viale Adriatico 1/N, 61032 Fano, Pesaro Urbino, Italy.
Unit of Microbiome Science and Biotechnology, Department of Pharmacy and Biotechnology, University of Bologna, via Belmeloro 6, 40126 Bologna, Italy.
Sci Total Environ. 2023 Aug 20;887:163948. doi: 10.1016/j.scitotenv.2023.163948. Epub 2023 May 5.
Marine mussels, especially Mytilus galloprovincialis, are well-established sentinel species, being naturally resistant to the exposure to multiple xenobiotics of natural and anthropogenic origin. Even if the response to multiple xenobiotic exposure is well known at the host level, the role of the mussel-associated microbiome in the animal response to environmental pollution is poorly explored, despite its potential in xenobiotic detoxification and its important role in host development, protection, and adaptation. Here, we characterized the microbiome-host integrative response of M. galloprovincialis in a real-world setting, involving exposure to a complex pattern of emerging pollutants, as occurs in the Northwestern Adriatic Sea. A total of 387 mussel individuals from 3 commercial farms, spanning about 200 km along the Northwestern Adriatic coast, and in 3 different seasons, were collected. Multiresidue analysis (for quantitative xenobiotic determination), transcriptomics (for host physiological response), and metagenomics (for host-associated microbial taxonomical and functional features) analyses were performed on the digestive glands. According to our findings, M. galloprovincialis responds to the presence of the complex pattern of multiple emerging pollutants - including the antibiotics sulfamethoxazole, erythromycin, and tetracycline, the herbicides atrazine and metolachlor, and the insecticide N,N-diethyl-m-toluamide - integrating host defense mechanisms, e.g., through upregulation of transcripts involved in animal metabolic activity, and microbiome-mediated detoxification functions, including microbial functionalities involved in multidrug or tetracycline resistance. Overall, our data highlight the importance of the mussel-associated microbiome as a strategic player for the orchestration of resistance to the multixenobiotic exposure at the holobiont level, providing strategic functionalities for the detoxification of multiple xenobiotic substances, as occurring in real world exposure settings. Complementing the host with microbiome-dependent xenobiotic degradative and resistance genes, the M. galloprovincialis digestive gland associated microbiome can have an important role in the detoxification of emerging pollutants in a context of high anthropogenic pressure, supporting the relevance of mussel systems as potential animal-based bioremediation tool.
海洋贻贝，尤其是厚壳贻贝，是一种成熟的哨兵物种，对自然和人为来源的多种外来化合物的暴露具有天然抗性。即使宿主对外来化合物暴露的反应在宿主水平上已经得到很好的研究，但贻贝相关微生物组在动物对环境污染的反应中的作用还没有得到充分的探索，尽管它在外来化合物解毒方面具有潜力，并且在宿主发育、保护和适应方面发挥着重要作用。在这里，我们在真实环境中描述了厚壳贻贝的微生物组-宿主综合反应，涉及到暴露于复杂的新兴污染物模式，就像在西北亚得里亚海发生的那样。从西北亚得里亚海沿岸 3 个商业养殖场收集了总共 387 个贻贝个体，这些个体分布在大约 200 公里的范围内，涉及 3 个不同的季节。对消化腺进行了多残留分析（用于定量测定外来化合物）、转录组学分析（用于宿主生理反应）和宏基因组学分析（用于宿主相关微生物分类学和功能特征）。根据我们的发现，厚壳贻贝对复杂的多种新兴污染物模式的存在作出反应，包括抗生素磺胺甲恶唑、红霉素和四环素、除草剂莠去津和甲草氯，以及杀虫剂 N,N-二乙基-间甲苯酰胺-整合宿主防御机制，例如，通过上调参与动物代谢活动的转录本，以及微生物介导的解毒功能，包括涉及多药或四环素抗性的微生物功能。总的来说，我们的数据强调了贻贝相关微生物组作为协调在整个生物群水平上对外来化合物暴露的抵抗的战略参与者的重要性，为多种外来化合物的解毒提供了战略功能，就像在真实的暴露环境中一样。厚壳贻贝的消化腺相关微生物组与宿主互补，具有依赖微生物的外来化合物降解和抗性基因，在高人为压力的情况下，可以在外来污染物的解毒中发挥重要作用，支持贻贝系统作为潜在的基于动物的生物修复工具的相关性。
