Carbon isotope evidence for the global physiology of Proterozoic cyanobacteria

Abstract

Ancestral cyanobacteria are assumed to be prominent primary producers after the Great Oxidation Event [≈2.4 to 2.0 billion years (Ga) ago], but carbon isotope fractionation by extant marine cyanobacteria (α-cyanobacteria) is inconsistent with isotopic records of carbon fixation by primary producers in the mid-Proterozoic eon (1.8 to 1.0 Ga ago). To resolve this disagreement, we quantified carbon isotope fractionation by a wild-type planktic β-cyanobacterium (Synechococcus sp. PCC 7002), an engineered Proterozoic analog lacking a CO2-concentrating mechanism, and cyanobacterial mats. At mid-Proterozoic pH and pCO2 values, carbon isotope fractionation by the wild-type β-cyanobacterium is fully consistent with the Proterozoic carbon isotope record, suggesting that cyanobacteria with CO2-concentrating mechanisms were apparently the major primary producers in the pelagic Proterozoic ocean, despite atmospheric CO2 levels up to 100 times modern. The selectively permeable microcompartments central to cyanobacterial CO2-concentrating mechanisms (“carboxysomes”) likely emerged to shield rubisco from O2 during the Great Oxidation Event.

Effects of CO2 and RuBisCO concentration on cyanobacterial growth and carbon isotope fractionation

“…Theoretically, under high CO2 concentrations, the intrinsic kinetic isotope effect of RuBisCO is expressed and maximizes εp (Bidigare et al, 1997;Hayes, 1993;Schubert & Jahren, 2012;Wilkes et al, 2018). Under these conditions, other cellular modules, such as carbon concentrating mechanisms capable of discriminating carbon isotopes, produce negligible impact on net carbon discrimination at the organismal level (Hurley et al, 2021;Laws et al, 2002). The positive relationship between CO2 concentration and carbon isotope fractionation has been observed empirically for a variety of autotrophs (Freeman & Hayes, 1992;Hinga et al, 1994;Schubert & Jahren, 2012;Wilkes et al, 2018), including for cyanobacteria in particular (Eichner et al, 2015;Hurley et al, 2021).…”

“…Under these conditions, other cellular modules, such as carbon concentrating mechanisms capable of discriminating carbon isotopes, produce negligible impact on net carbon discrimination at the organismal level (Hurley et al, 2021;Laws et al, 2002). The positive relationship between CO2 concentration and carbon isotope fractionation has been observed empirically for a variety of autotrophs (Freeman & Hayes, 1992;Hinga et al, 1994;Schubert & Jahren, 2012;Wilkes et al, 2018), including for cyanobacteria in particular (Eichner et al, 2015;Hurley et al, 2021). Other studies showed that photoautotrophs that grew under a lower pH, and thus a higher proportion of CO2, also exhibited higher carbon fractionation (Mizutani & Wada, 1982;Roeske & O'Leary, 1984;Wang, Yeager, & Lu, 2016;Yoshioka, 1997).…”

“…This discrepancy might be attributable to several intracellular physiological and metabolic features that additionally shift the isotopic composition of organism biomass. These include the activation of carbon-concentrating mechanisms such as the partitioning of RuBisCO into carboxysomes (Hurley, Wing, Jasper, Hill, & Cameron, 2021;Laws, Popp, Cassar, & Tanimoto, 2002;Price, Badger, Woodger, & Long, 2008;Raven, Cockell, & De La Rocha, 2008), the diffusive transport of CO2 (Hayes, 1993;Rau, Riebesell, & Wolf-Gladrow, 1996), and intermediary carbon-fixing steps (Eungrasamee, Miao, Incharoensakdi, Lindblad, & Jantaro, 2019; H. I. Guy & Evans, 1996;Hayes, 1993;Rothschild & DesMarais, 1989).…”

“…CC-BY-NC-ND 4.0 International license available under a was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made Popp, 1997), and CO2 concentration (Eichner, Thoms, Kranz, & Rost, 2015;Freeman & Hayes, 1992;Hinga et al, 1994;Hurley et al, 2021;Schubert & Jahren, 2012;Wilkes, Lee, McClelland, Rickaby, & Pearson, 2018). These variations indicate a compelling need to comprehensively characterize both internal and external factors that can affect isotope fractionation, though the study of each tend to be siloed in biological and geobiological fields, respectively.…”

Computational Modeling and Evolutionary Implications of Biochemical Reactions in Bacterial Microcompartments

“…These models could be combined with recent computational approaches in metabolic evolution [82]. This approach could allow systematic investigation on how evolutionary intermediates in CCM evolution may have responded to environmental changes during proposed times of carboxysome origination such as the Great Oxidation Event (GOE) approximately 2.3-2.5 billion years ago [83]. A dramatic increase in atmospheric O2 concentrations across the GOE relative to slowly declining CO2 concentrations led to an ~100 million fold increase in O2:CO2 ratios, which could have provided a selective pressure driving the encapsulation of oxygen-sensitive enzymes, such as RuBisCO.…”