CO2-dependent carbon isotope fractionation in Archaea, Part I: Modeling the 3HP/4HB pathway

Abstract

The 3-hydroxypropionate/4-hydroxybutyrate (3HP/4HB) pathway of carbon fixation is found in thermophilic Crenarchaeota of the order Sulfolobales and in aerobic, ammonia-oxidizing Thaumarchaeota. Unlike all other known autotrophic carbon metabolisms, this pathway exclusively uses HCO_3- rather than CO_2 as the substrate for carbon fixation. Biomass produced by the 3HB/4HP pathway is relatively ^(13)C-enriched compared to biomass fixed by other autotrophic pathways, with total biosynthetic isotope effects (e_(Ar)) of ca. 3‰ in the Sulfolobales and ca. 20‰ in the Thaumarchaeota. Explanations for the difference between these values usually invoke the dual effects of thermophily and growth at low pH (low [HCO_3-]) for the former group vs. mesophily and growth at pH > 7 (high [HCO_3-]) for the latter group. Here we examine the model taxa Metallosphaera sedula and Nitrosopumilus maritimususing an isotope flux-balance model to argue that the primary cause of different e_(Ar) values more likely is the presence of carbonic anhydrase in M. sedula and its corresponding absence in N. maritimus. The results suggest that the pool of HCO_3-inside N. maritimus is out of isotopic equilibrium with CO_2 and that the organism imports < 10% HCO_3- from the extracellular environment. If correct and generalizable, the aerobic, ammonia-oxidizing marine Thaumarchaeota are dependent on passive CO_2 uptake and a slow rate of intracellular conversion to HCO_3-. Values of e_(Ar) should therefore vary in response to growth rate (μ) and CO_2 availability, analogous to eukaryotic algae, but in the opposite direction: e_(Ar) becomes smaller as [CO_(2(aq))] increases and/or μ decreases. Such an idea represents a testable hypothesis, both in the laboratory and in natural systems. Sensitivity to μ and CO_2 implies that measurements of e_(Ar) may hold promise as a pCO_2 paleobarometer.