Coastal Oregon Marine Experiment Station, Department Fisheries and Wildlife, Hatfield Marine Science Center, Oregon State University, Newport, OR 97365;
Experimental Physics Department, Saarland University, D-66041 Saarbruecken, Germany.
Proc Natl Acad Sci U S A. 2022 Jan 18;119(3). doi: 10.1073/pnas.2108655119.
Animals use geomagnetic fields for navigational cues, yet the sensory mechanism underlying magnetic perception remains poorly understood. One idea is that geomagnetic fields are physically transduced by magnetite crystals contained inside specialized receptor cells, but evidence for intracellular, biogenic magnetite in eukaryotes is scant. Certain bacteria produce magnetite crystals inside intracellular compartments, representing the most ancient form of biomineralization known and having evolved prior to emergence of the crown group of eukaryotes, raising the question of whether magnetite biomineralization in eukaryotes and prokaryotes might share a common evolutionary history. Here, we discover that salmonid olfactory epithelium contains magnetite crystals arranged in compact clusters and determine that genes differentially expressed in magnetic olfactory cells, contrasted to nonmagnetic olfactory cells, share ancestry with an ancient prokaryote magnetite biomineralization system, consistent with exaptation for use in eukaryotic magnetoreception. We also show that 11 prokaryote biomineralization genes are universally present among a diverse set of eukaryote taxa and that nine of those genes are present within the Asgard clade of archaea Lokiarchaeota that affiliates with eukaryotes in phylogenomic analysis. Consistent with deep homology, we present an evolutionary genetics hypothesis for magnetite formation among eukaryotes to motivate convergent approaches for examining magnetite-based magnetoreception, molecular origins of matrix-associated biomineralization processes, and eukaryogenesis.
动物利用地磁场作为导航线索，但磁性感知的感觉机制仍知之甚少。一种观点认为，地磁场是由特殊受体细胞内的磁铁矿晶体物理转换而来的，但真核生物细胞内生物磁铁矿的证据很少。某些细菌在细胞内隔室中产生磁铁矿晶体，这代表了已知最古老的生物矿化形式，并且在真核生物冠群出现之前就已经进化，这就提出了一个问题，即真核生物和原核生物的磁铁矿生物矿化是否可能具有共同的进化历史。在这里，我们发现鲑鱼嗅觉上皮含有排列成紧密簇的磁铁矿晶体，并确定与磁性嗅觉细胞差异表达的基因与古老的原核生物磁铁矿生物矿化系统具有共同的祖先，这与在真核生物磁受体中适应使用有关。我们还表明，11 种原核生物矿化基因普遍存在于一组多样化的真核生物分类群中，其中 9 种基因存在于 Lokiarchaeota 的 Asgard 分支中，该分支在系统发育分析中与真核生物有关。与深同源性一致，我们提出了一个关于真核生物中磁铁矿形成的进化遗传学假设，以激发对基于磁铁矿的磁受体、基质相关生物矿化过程的分子起源以及真核生物起源的趋同方法的研究。
