Department of Biosciences, Biotechnology and Environment, University of Bari "Aldo Moro", Via Orabona 4, Bari, 70124, Italy.
Center of Marine Sciences (CCMar), University of Algarve, Campus Gambelas, Faro, 8005-139, Portugal.
Microbiome. 2024 Mar 7;12(1):47. doi: 10.1186/s40168-023-01740-6.
Macroalgae, especially reds (Rhodophyta Division) and browns (Phaeophyta Division), are known for producing various halogenated compounds. Yet, the reasons underlying their production and the fate of these metabolites remain largely unknown. Some theories suggest their potential antimicrobial activity and involvement in interactions between macroalgae and prokaryotes. However, detailed investigations are currently missing on how the genetic information of prokaryotic communities associated with macroalgae may influence the fate of organohalogenated molecules.
To address this challenge, we created a specialized dataset containing 161 enzymes, each with a complete enzyme commission number, known to be involved in halogen metabolism. This dataset served as a reference to annotate the corresponding genes encoded in both the metagenomic contigs and 98 metagenome-assembled genomes (MAGs) obtained from the microbiome of 2 red (Sphaerococcus coronopifolius and Asparagopsis taxiformis) and 1 brown (Halopteris scoparia) macroalgae. We detected many dehalogenation-related genes, particularly those with hydrolytic functions, suggesting their potential involvement in the degradation of a wide spectrum of halocarbons and haloaromatic molecules, including anthropogenic compounds. We uncovered an array of degradative gene functions within MAGs, spanning various bacterial orders such as Rhodobacterales, Rhizobiales, Caulobacterales, Geminicoccales, Sphingomonadales, Granulosicoccales, Microtrichales, and Pseudomonadales. Less abundant than degradative functions, we also uncovered genes associated with the biosynthesis of halogenated antimicrobial compounds and metabolites.
The functional data provided here contribute to understanding the still largely unexplored role of unknown prokaryotes. These findings support the hypothesis that macroalgae function as holobionts, where the metabolism of halogenated compounds might play a role in symbiogenesis and act as a possible defense mechanism against environmental chemical stressors. Furthermore, bacterial groups, previously never connected with organohalogen metabolism, e.g., Caulobacterales, Geminicoccales, Granulosicoccales, and Microtrichales, functionally characterized through MAGs reconstruction, revealed a biotechnologically relevant gene content, useful in synthetic biology, and bioprospecting applications. Video Abstract.
大型藻类，尤其是红藻（红藻门）和褐藻（褐藻门），以产生各种卤代化合物而闻名。然而，它们产生这些代谢物的原因和这些代谢物的命运在很大程度上仍然未知。一些理论认为它们具有潜在的抗菌活性，并参与了大型藻类和原核生物之间的相互作用。然而，目前还缺乏关于与大型藻类相关的原核生物群落的遗传信息如何影响有机卤代分子命运的详细研究。
为了解决这一挑战，我们创建了一个专门的数据集，其中包含 161 种酶，每种酶都有一个完整的酶委员会编号，已知这些酶参与卤代代谢。该数据集作为参考，注释了从 2 种红藻（扇叶冠瘤藻和伞形马尾藻）和 1 种褐藻（泡叶藻）微生物组中获得的宏基因组 contigs 和 98 个宏基因组组装基因组（MAGs）中编码的相应基因。我们检测到许多脱卤相关基因，特别是具有水解功能的基因，这表明它们可能参与降解广泛的碳氢卤化物和卤代芳烃分子，包括人为化合物。我们在 MAGs 中发现了一系列降解基因功能，涵盖了各种细菌目，如红杆菌目、根瘤菌目、钙杆菌目、双球菌目、单胞菌目、颗粒球菌目、微毛菌目和假单胞菌目。与降解功能相比，我们还发现了与卤代抗菌化合物和代谢物生物合成相关的基因。
这里提供的功能数据有助于理解仍然很大程度上未被探索的未知原核生物的作用。这些发现支持了大型藻类作为真核生物的假说，其中卤代化合物的代谢可能在共生发生中发挥作用，并作为对环境化学胁迫的可能防御机制。此外，通过 MAGs 重建功能表征的以前从未与有机卤代物代谢相关的细菌群，如钙杆菌目、双球菌目、颗粒球菌目和微毛菌目，揭示了具有生物技术相关性的基因内容，可用于合成生物学和生物勘探应用。视频摘要。
