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 3rather than CO 2 as the substrate for carbon fixation. Biomass produced by the 3HB/4HP pathway is relatively 13 Cenriched compared to biomass fixed by other autotrophic pathways, with total biosynthetic isotope effects ( 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 [ ]) for the latter group. Here we HCO-3 examine the model taxa Metallosphaera sedula and Nitrosopumilus maritimus using an isotope fluxbalance model to argue that the primary cause of different  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 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 HCO-3 marine Thaumarchaeota are dependent on passive CO 2 uptake and a slow rate of intracellular conversion to. Values of  Ar should therefore vary in response to growth rate () and CO 2 availability, analogous HCO-3 to eukaryotic algae, but in the opposite direction:  Ar becomes smaller as [CO 2(aq) ] increases and/or  decreases. Such an idea represents a testable hypothesis, both in the laboratory and in natural systems. Sensitivity to  and CO 2 implies that measurements of  Ar may hold promise as a pCO 2 paleobarometer. 3 CO 2-yet isotopically, it is distinct. The marked difference in  Ar values between thermoacidophilic Sulfolobales and the ammoniaoxidizing marine Thaumarchaeota is well recognized (e.g., Könneke et al., 2012; 2014) but has not yet been quantitatively explained. Explanation of the 20‰  Ar value in Thaumarchaeota generally invokes both

Archaeal lipid biomarker constraints on the Paleocene-Eocene carbon isotope excursion

“…6 ; [DIC] ≥ 2 mM) δ 13 C cren is offset by a predictable fractionation factor from δ 13 C DIC (refs. 40,41 ) and that the change in δ 13 C cren during the PETM closely approximates the CIE in the global exogenic carbon reservoir. We further couple δ 13 C cren to TEX 86 analyses which allows simultaneous reconstruction of CIE and temperature change in low-carbonate sediments, thereby circumventing confounding effects of carbonate dissolution prevalent during the PETM and other climate warming events.…”

“…Flux balance modeling 41 and environmental data 40 suggest that carbon isotopic fractionation in marine Thaumarchaeota originates from passive CO 2 transport into the cell combined with slow conversion to HCO 3 - , resulting in a dependence of the expressed fractionation factor on the dissolved CO 2 concentration. Importantly, the effect is inverse to the influence of p CO 2 on carbon isotopic fractionation in phytoplankton, resulting in a smaller fractionation factor (ε DIC-Cren ) at high dissolved CO 2 concentrations 40,41 . Due to the p CO 2 increase during the PETM ε DIC-Cren may have been smaller by 0.75 ± 0.15‰ (range 0.6–0.9‰) during the peak-PETM compared to the pre-PETM (assuming Paleocene-Eocene atmospheric p CO 2 of ~850–2200 ppm, refs.…”

“…ε DIC-Cren was calculated for pre-PETM and peak-PETM boundary conditions (Supplementary Fig. 4) using the flux balance model by Pearson et al 41 . Boundary conditions 13,17 were set as: 25 °C seawater temperature, salinity 35, [DIC] 2000–3000 µmol kg -1 , pH 7.75–7.45.…”

Microbial Methane From Methylphosphonate Isotopically Records Source

“…However, these groups of microbes are differentially distributed with depth, and likely impart distinct carbon isotope values onto the MPn, given that PEP arises through distinct metabolic pathways. For example, the C isotope delta value of bulk biomass from cultures of the AOA N. maritimus was −20‰ depleted relative to the inorganic bicarbonate C‐delta value (Könneke et al, ), where fractionation was attributed to the biotin‐dependent acetyl/propionyl‐CoA carboxylase—an inorganic carbon fixation enzyme (Pearson et al, ). Methane from MPn derived from autotrophic AOA's would have a different delta value than that from SAR11 and drive different observed fractionations, given that SAR11‐type organisms acquire anabolic organic carbon from a variety of heterotrophic substrates (Malmstrom et al, ; Mary et al, ; Mou et al, ; Rappé et al, ).…”

Carbon isotope excursions during the late Miocene recorded by lipids of marine Thaumarchaeota, Piedmont Basin, Mediterranean Sea

“…Such concerns were recently discarded (cf. Pearson et al, 2019;Besseling et al, 2020), although it has been put forward that ε values could depend on growth rate and carbon dioxide concentration, resulting in deviations of up to ±2‰ between the measured and the reconstructed δ 13 C DIC values of modern seawater (cf. Hurley et al, 2019).…”