The discovery of membrane-enclosed, metabolically functional organelles in Bacteria has transformed our understanding of the subcellular complexity of prokaryotic cells. Biomineralization of magnetic nanoparticles within magnetosomes by magnetotactic bacteria (MTB) is a fascinating example of prokaryotic organelles. Magnetosomes, as nano-sized magnetic sensors in MTB, facilitate cell navigation along the local geomagnetic field, a behaviour referred to as magnetotaxis or microbial magnetoreception. Recent discovery of novel MTB outside the traditionally recognized taxonomic lineages suggests that MTB diversity across the domain Bacteria are considerably underestimated, which limits understanding of the taxonomic distribution and evolutionary origin of magnetosome organelle biogenesis. Here, we perform the most comprehensive metagenomic analysis available of MTB communities and reconstruct metagenome-assembled MTB genomes from diverse ecosystems. Discovery of MTB in acidic peatland soils suggests widespread MTB occurrence in waterlogged soils in addition to subaqueous sediments and water bodies. A total of 168 MTB draft genomes have been reconstructed, which represent nearly a 3-fold increase over the number currently available and more than double the known MTB species at the genome level. Phylogenomic analysis reveals that these genomes belong to 13 Bacterial phyla, six of which were previously not known to include MTB. These findings indicate a much wider taxonomic distribution of magnetosome organelle biogenesis across the domain Bacteria than previously thought. Comparative genome analysis reveals a vast diversity of magnetosome gene clusters involved in magnetosomal biogenesis in terms of gene content and synteny residing in distinct taxonomic lineages. Phylogenetic analyses of core magnetosome proteins in this largest available and taxonomically diverse dataset support an unexpectedly early evolutionary origin of magnetosome biomineralization, likely ancestral to the origin of the domain Bacteria. These findings expand the taxonomic and phylogenetic diversity of MTB across the domain Bacteria and shed new light on the origin and evolution of microbial magnetoreception. Potential biogenesis of the magnetosome organelle in the close descendants of the last bacterial common ancestor has important implications for our understanding of the evolutionary history of bacterial cellular complexity and emphasizes the biological significance of the magnetosome organelle.

中文翻译：

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扩大细菌领域的磁性细胞器生物发生


细菌中膜封闭、具有代谢功能的细胞器的发现改变了我们对原核细胞亚细胞复杂性的理解。趋磁细菌（MTB）对磁小体内磁性纳米粒子的生物矿化是原核细胞器的一个有趣的例子。磁小体作为 MTB 中的纳米级磁传感器，有助于细胞沿局部地磁场导航，这种行为称为趋磁性或微生物磁感受。最近在传统公认的分类谱系之外发现的新型 MTB 表明，细菌领域的 MTB 多样性被大大低估，这限制了对磁小体细胞器生物发生的分类分布和进化起源的理解。在这里，我们对 MTB 群落进行了最全面的宏基因组分析，并从不同的生态系统中重建了宏基因组组装的 MTB 基因组。在酸性泥炭地土壤中发现 MTB 表明，除了水下沉积物和水体之外，MTB 还广泛存在于浸水土壤中。总共重建了 168 个 MTB 基因组草案，比目前可用的数量增加了近 3 倍，是基因组水平上已知 MTB 物种的两倍多。系统发育基因组分析表明，这些基因组属于 13 个细菌门，其中 6 个细菌门以前并不知道包括 MTB。这些发现表明，细菌领域内磁小体细胞器生物发生的分类分布比之前想象的要广泛得多。比较基因组分析揭示了参与磁小体生物发生的磁小体基因簇在不同分类谱系中的基因内容和同线性方面的巨大多样性。 在这个最大的可用且分类学上多样化的数据集中对核心磁小体蛋白的系统发育分析支持了磁小体生物矿化的出乎意料的早期进化起源，可能是细菌域起源的祖先。这些发现扩大了 MTB 在细菌领域的分类学和系统发育多样性，并为微生物磁感受的起源和进化提供了新的线索。最后一个细菌共同祖先的近代后代中磁小体细胞器的潜在生物发生对于我们理解细菌细胞复杂性的进化史具有重要意义，并强调了磁小体细胞器的生物学意义。