Late acquisition of the rTCA carbon fixation pathway by Chlorobi

• Published in: Nature ecology & evolution Vol. 7; no. 9; pp. 1398 - 1407
• Main Authors: Zhang, Xiaowen, Paoletti, Madeline M., Izon, Gareth, Fournier, Gregory P., Summons, Roger E.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.09.2023; Nature Publishing Group
• Subjects: 631/181; 704/47; Assembly; Autotrophy; Bacteria; Biological and Physical Anthropology; Biomedical and Life Sciences; Carbon; Carbon 13; Carbon Cycle; Carbon fixation; Carbon Isotopes; Carotenoids; Carotenoids - metabolism; Chlorobi; Chlorobi - chemistry; Chlorobi - metabolism; Creeks; Cyanobacteria; Ecology; Ecosystem; Energy efficiency; Evolutionary Biology; Fossils; Heterotrophic bacteria; Intolerance; Life Sciences; Oxygenation; Paleontology; Photoautotrophy; Tricarboxylic acid cycle; Tricarboxylic Acids - metabolism; Zoology
• ISSN: 2397-334X; 2397-334X
• DOI: 10.1038/s41559-023-02147-0

The reverse tricarboxylic acid (rTCA) cycle is touted as a primordial mode of carbon fixation due to its autocatalytic propensity and oxygen intolerance. Despite this inferred antiquity, however, the earliest rock record affords scant supporting evidence. In fact, based on the chimeric inheritance of rTCA cycle steps within the Chlorobiaceae, even the use of the chemical fossil record of this group is now subject to question. While the 1.64-billion-year-old Barney Creek Formation contains chemical fossils of the earliest known putative Chlorobiaceae-derived carotenoids, interferences from the accompanying hydrocarbon matrix have hitherto precluded the carbon isotope measurements necessary to establish the physiology of the organisms that produced them. Overcoming this obstacle, here we report a suite of compound-specific carbon isotope measurements identifying a cyanobacterially dominated ecosystem featuring heterotrophic bacteria. We demonstrate chlorobactane is 13 C-depleted when compared to contemporary equivalents, showing only slight 13 C-enrichment over co-existing cyanobacterial carotenoids. The absence of this diagnostic isotopic fingerprint, in turn, confirms phylogenomic hypotheses that call for the late assembly of the rTCA cycle and, thus, the delayed acquisition of autotrophy within the Chlorobiaceae. We suggest that progressive oxygenation of the Earth System caused an increase in the marine sulfate inventory thereby providing the selective pressure to fuel the Neoproterozoic shift towards energy-efficient photoautotrophy within the Chlorobiaceae. Compound-specific carbon isotope measurements of the 1.64-billion-year-old Barney Creek Formation show an ecosystem dominated by cyanobacteria and heterotrophic bacteria. Isotope data for carotenoids suggest that the assembly of the reverse tricarboxylic acid cycle in Chlorobi occurred later.