Role of horizontal gene transfers and microbial ecology in the evolution of fluxes through the tricarboxylic acid cycle

IF 1.7 4区 物理与天体物理 Q3 ASTRONOMY & ASTROPHYSICS International Journal of Astrobiology Pub Date : 2023-04-12 DOI:10.1017/s1473550423000095
Tymofii Sokolskyi, Shiladitya DasSarma
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Abstract

Abstract The origin of carbon fixation is a fundamental question in astrobiology. While the Calvin cycle is the most active on the modern Earth, the reductive tricarboxylic acid (TCA) cycle (rTCA) pathway for carbon fixation has been proposed to have played an important role in early evolution. In this study, we examined the evolution of key enzymes in the rTCA, which are rare in extant organisms, occurring in a few groups of Bacteria and Archaea. We investigated one of the least common reactions of this pathway, cleavage of citrate into oxaloacetate and acetyl-CoA, which can be performed by either a two-enzyme system (CCS/CCL) or a single enzyme (ACL) that is assumed to be the result of fusion of the two active sites into a single polypeptide. For broader context, we also studied functionally diverged homologues of these enzymes, succinyl-CoA synthetase (SCS) and citrate synthase. Our phylogenetic analysis of these enzymes in Bacteria and Archaea shows that SCS, a homologue of CCS from distant bacterial taxa capable of citrate cleavage, are monophyletic, suggesting linked horizontal gene transfers of SCS and citrate cleavage enzymes. We also found evidence of the horizontal transfer of SCS from a clade of anaerobic Archaea (Archaeoglobi, Methanomicrobia or Crenarchaeota) to an ancestor of Cyanobacteria/Melainabacteria clade – both of which share a succinate semialdehyde shunt in their oxidative TCA cycles. We identified new bacterial and archaeal taxa for which complete rTCA cycles are theoretically possible, including Syntrophobacter, Desulfofundulus, Beggiatoa, Caldithrix, Ca. Acidulodesulfobacterales and Ca. Micrarchaeota. Finally, we propose a mechanism for syntrophically-regulated fluxes through oxidative and rTCA reactions in microbial communities particularly Haloarchaea-Nanohaloarchaea symbiosis and its implications for carbon fixation during retinal-based phototrophy and the Purple Earth hypothesis. We discuss how the inclusion of an ecological perspective in the studies of evolution of ancient metabolic pathways may be beneficial to understanding the origin of life.
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水平基因转移和微生物生态学在三羧酸循环通量演化中的作用
碳固定的起源是天体生物学中的一个基本问题。虽然卡尔文循环是现代地球上最活跃的循环,但碳固定的还原性三羧酸循环(rTCA)途径被认为在早期进化中发挥了重要作用。在这项研究中,我们研究了在现存生物中罕见的rTCA关键酶的进化,这些酶发生在一些细菌和古细菌群中。我们研究了该途径中最不常见的反应之一,柠檬酸盐裂解成草酰乙酸和乙酰辅酶a,该反应可以通过双酶系统(CCS/CCL)或单酶系统(ACL)进行,这被认为是两个活性位点融合成单个多肽的结果。在更广泛的背景下,我们还研究了这些酶的功能分化同源物,琥珀酰辅酶a合成酶(SCS)和柠檬酸合成酶。我们对细菌和古细菌中这些酶的系统发育分析表明,SCS是来自能够裂解柠檬酸盐的遥远细菌分类群的CCS的同源物,是单系的,这表明SCS和柠檬酸盐裂解酶存在水平基因转移的联系。我们还发现了从厌氧古细菌分支(archaeoa archaebi, Methanomicrobia或Crenarchaeota)向蓝藻/黑藻分支的祖先水平转移SCS的证据-两者在其氧化TCA循环中共享琥珀酸半醛分流。我们发现了新的细菌和古细菌分类群,包括Syntrophobacter, Desulfofundulus, Beggiatoa, Caldithrix, Ca. Acidulodesulfobacterales和Ca. microarchaeota,理论上可能完整的rTCA循环。最后,我们提出了微生物群落中氧化和rTCA反应对共养调节通量的机制,特别是盐古菌-纳米盐古菌共生,以及它对视网膜光养过程中碳固定的影响和紫色地球假说。我们讨论了在古代代谢途径的进化研究中纳入生态学观点如何有助于理解生命的起源。
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来源期刊
International Journal of Astrobiology
International Journal of Astrobiology 地学天文-地球科学综合
CiteScore
3.70
自引率
11.80%
发文量
45
审稿时长
>12 weeks
期刊介绍: International Journal of Astrobiology is the peer-reviewed forum for practitioners in this exciting interdisciplinary field. Coverage includes cosmic prebiotic chemistry, planetary evolution, the search for planetary systems and habitable zones, extremophile biology and experimental simulation of extraterrestrial environments, Mars as an abode of life, life detection in our solar system and beyond, the search for extraterrestrial intelligence, the history of the science of astrobiology, as well as societal and educational aspects of astrobiology. Occasionally an issue of the journal is devoted to the keynote plenary research papers from an international meeting. A notable feature of the journal is the global distribution of its authors.
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