Late acquisition of the rTCA carbon fixation pathway by Chlorobi

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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 13C-depleted when compared to contemporary equivalents, showing only slight 13C-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.

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Financial support was provided via the Simons Foundation under the auspices of Simons Collaboration on the Origin of Life (grant no. 290361FY18 to R.E.S.). G.P.F. and M.M.P. were supported by the National Science Foundation Integrated Earth Systems award EAR (grant no. 1615426 to G.P.F). X.Z. was sponsored by the Shanghai Pujiang Programme. G.I. acknowledges receipt of a MISTI Global Seed Award. We recognize formative discussions with various members of the Summons Laboratory, particularly Benjamin Uveges who helped with provision of graphics. R.E.S. thanks the Hanse-Wissenschaftskolleg for support during the finalization of this report.

Department of Earth, Atmospheric and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA

Xiaowen Zhang, Madeline M. Paoletti, Gareth Izon, Gregory P. Fournier & Roger E. Summons

School of Oceanography, Shanghai Jiao Tong University, Shanghai, China

Xiaowen Zhang

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R.E.S. conceived the study and secured the funding to support the research. G.P.F. and M.M.P. independently conducted the phylogenomic analysis. X.Z. developed and verified the analytical procedure, eradicating the UCM that allowed isotopic analysis of the BCF carotenoids. X.Z. collected the isotopic data with laboratory support from G.I. X.Z. wrote the initial draft of the paper after which all authors contributed.

Correspondence to Xiaowen Zhang or Roger E. Summons.

The authors declare no competing interests.

Nature Ecology & Evolution thanks Alexis Gilbert, Kliti Grice and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Zhang, X., Paoletti, M.M., Izon, G. et al. Late acquisition of the rTCA carbon fixation pathway by Chlorobi. Nat Ecol Evol (2023). https://doi.org/10.1038/s41559-023-02147-0

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Received: 10 February 2023

Accepted: 30 June 2023

Published: 03 August 2023

DOI: https://doi.org/10.1038/s41559-023-02147-0

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