Electron Transport Chains as a Window into the Earliest Stages of Evolution

Our understanding of the origin and early evolution of life is generally studied under two different paradigms: bottom up and top down. Prebiotic chemistry and early Earth geochemistry allow researchers to explore possible origin of life scenarios. But for these “bottom up” approaches, even successful experiments only amount to a proof of principle. On the other hand, phylogenetic “top down” research on early evolutionary history is able to provide a historical account about ancient organisms, but is unable to investigate evolutionary events that occurred during and just after the origin of life. Here, we consider ancient electron transport chains (ETCs) as a potential bridge between prebiotic geochemistry and early evolutionary history. Current phylogenetic evidence suggests that the ATP synthase motor that converts pH gradients across membranes into stored chemical potential energy and the cellular organization that would have been required for membrane bioenergetics, both predate the last universal common ancestor (LUCA) of life. At the same time, recent experiments have shown that some aspects of modern electron transport chains can be replicated by minerals, protocells, and/or organic cofactors in the absence of proteins. We review the diversity of prokaryotic electron transport chains, describe current work on the early evolution of cellular organization and prebiotic membrane energetics, and advocate for several lines of research to bridge our understanding of the earliest evolution of membrane bioenergetics across prebiotic geochemistry and early evolution.

当前学界针对生命起源与早期演化的研究，通常依托两种不同范式展开：自下而上（bottom up）范式与自上而下（top down）范式。前生物化学与早期地球地球化学可助力研究者探索各类潜在的生命起源场景，但此类“自下而上”研究路径即便取得成功，也仅能提供原理性证明。另一方面，针对演化早期历史的系统发育“自上而下”研究，能够为远古生物提供详实的历史演化阐释，却无法探究生命起源过程中及起源后不久发生的演化事件。本文将古代电子传递链（electron transport chains, ETCs）视为连接前生物地球化学与早期演化历史的潜在桥梁。当前系统发育学证据显示，可将膜两侧pH梯度转化为储存化学势能的ATP合酶马达，以及支撑膜生物能学所需的细胞组织结构，二者均早于生命的最后通用共同祖先（last universal common ancestor, LUCA）。与此同时，近期实验证实，在无蛋白质参与的条件下，矿物、原细胞及有机辅因子可复现现代电子传递链的部分功能环节。本文综述了原核生物电子传递链的多样性，介绍了当前关于细胞组织结构早期演化与前生物膜能学的研究进展，并倡导开展多维度研究，以弥合我们在前生物地球化学与早期演化之间关于膜生物能学最早演化的认知鸿沟。