Department of Life Science and Biotechnology, The National Institute of Advanced Industrial Science and Technology, Ibaraki 305-0817, Japan.
Biogeochemistry Research Center, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Kanagawa 237-0061, Japan.
Proc Natl Acad Sci U S A. 2024 Jun 18;121(25):e2322120121. doi: 10.1073/pnas.2322120121. Epub 2024 Jun 14.
Life harnessing light energy transformed the relationship between biology and Earth-bringing a massive flux of organic carbon and oxidants to Earth's surface that gave way to today's organotrophy- and respiration-dominated biosphere. However, our understanding of how life drove this transition has largely relied on the geological record; much remains unresolved due to the complexity and paucity of the genetic record tied to photosynthesis. Here, through holistic phylogenetic comparison of the bacterial domain and all photosynthetic machinery (totally spanning >10,000 genomes), we identify evolutionary congruence between three independent biological systems-bacteria, (bacterio)chlorophyll-mediated light metabolism (chlorophototrophy), and carbon fixation-and uncover their intertwined history. Our analyses uniformly mapped progenitors of extant light-metabolizing machinery (reaction centers, [bacterio]chlorophyll synthases, and magnesium-chelatases) and enzymes facilitating the Calvin-Benson-Bassham cycle (form I RuBisCO and phosphoribulokinase) to the same ancient Terrabacteria organism near the base of the bacterial domain. These phylogenies consistently showed that extant phototrophs ultimately derived light metabolism from this bacterium, the last phototroph common ancestor (LPCA). LPCA was a non-oxygen-generating (anoxygenic) phototroph that already possessed carbon fixation and two reaction centers, a type I analogous to extant forms and a primitive type II. Analyses also indicate chlorophototrophy originated before LPCA. We further reconstructed evolution of chlorophototrophs/chlorophototrophy post-LPCA, including vertical inheritance in Terrabacteria, the rise of oxygen-generating chlorophototrophy in one descendant branch near the Great Oxidation Event, and subsequent emergence of Cyanobacteria. These collectively unveil a detailed view of the coevolution of light metabolism and Bacteria having clear congruence with the geological record.
生命利用光能改变了生物学与地球的关系——将大量的有机碳和氧化剂带到地球表面，从而形成了今天以有机营养和呼吸为主导的生物圈。然而，我们对生命如何驱动这一转变的理解在很大程度上依赖于地质记录；由于与光合作用相关的遗传记录的复杂性和稀缺性，许多问题仍然没有得到解决。在这里，通过对细菌域和所有光合作用机制（总共跨越>10000 个基因组）的整体系统发育比较，我们确定了三个独立的生物系统——细菌、（细菌）叶绿素介导的光代谢（叶绿素营养）和碳固定——之间的进化一致性，并揭示了它们的交织历史。我们的分析一致地将现存的光代谢机制（反应中心、[细菌]叶绿素合酶和镁螯合酶）和促进卡尔文-本森-巴斯汉姆循环（I 型 RuBisCO 和磷酸核酮糖激酶）的酶的祖先进化体映射到细菌域底部附近的同一个古老的 Terrabacteria 生物上。这些系统发育一致表明，现存的光养生物最终从这个细菌，即最后的光养共同祖先（LPCA）中获得了光代谢。LPCA 是一种不产生氧气的（厌氧）光养生物，已经拥有碳固定和两个反应中心，一个类似于现存形式的 I 型和一个原始的 II 型。分析还表明，叶绿素营养起源于 LPCA 之前。我们进一步重建了 LPCA 后叶绿素营养生物/叶绿素营养的进化，包括 Terrabacteria 中的垂直遗传、大氧化事件附近一个后裔分支中氧气产生的叶绿素营养的兴起，以及随后蓝细菌的出现。这些共同揭示了光代谢和细菌共同进化的详细视图，与地质记录有明显的一致性。
