The role of soil pH on soil carbonic anhydrase activity

Abstract

Abstract. Carbonic anhydrases (CAs) are metalloenzymes present in plants and microorganisms that catalyse the interconversion of CO 2 and water to bicarbonate and protons. Because oxygen isotopes are also exchanged during this reaction, the presence of CA also modifies the contribution of soil and plant CO 18 O fluxes to the global budget of atmospheric CO 18 O. The oxygen isotope signatures (δ 18 O) of these fluxes differ as leaf water pools are usually more enriched than soil water pools, and this difference is used to partition the net CO 2 flux over land into soil respiration and plant photosynthesis. Nonetheless, the use of atmospheric CO 18 O as a tracer of land surface CO 2 fluxes requires a good knowledge of soil CA activity. Previous studies have shown that significant differences in soil CA activity are found in different biomes and seasons, but our understanding of the environmental and ecological drivers responsible for the spatial and temporal patterns observed in soil CA activity is still limited. One factor that has been overlooked so far is pH. Soil pH is known to strongly influence microbial community composition, richness and diversity in addition to governing the speciation of CO 2 between the different carbonate forms. In this study we investigated the CO 2 -H 2 O isotopic exchange rate (k iso ) in six soils with pH varying from 4.5 to 8.5. We also artificially increased the soil CA concentration to test how pH and other soil properties (texture and phosphate content) affected the relationship between k iso and CA concentration. We found that soil pH was the primary driver of k iso after CA addition and that the chemical composition (i.e. phosphate content) played only a secondary role. We also found an offset between the δ 18 O of the water pool with which CO 2 equilibrates and total soil water (i.e. water extracted by vacuum distillation) that varied with soil texture. The reasons for this offset are still unknown.

Oxygen isotope exchange between water and carbon dioxide in soils is controlled by pH, nitrate availability and microbial biomass through links to carbonic anhydrase activity

“…The observed increase, contrary to the decrease (Figure 1 c) that would be expected to be induced by the shift in dissolved inorganic carbon speciation (Figure 1 b) at a constant carbonic anhydrase concentration and efficiency (Figure 1 a), suggests a greater abundance or the presence of more efficient forms of carbonic anhydrases at higher soil pH. Such an observation may result from changes in size or composition of the microbial communities involved as discussed (Sauze et al, , 2018. Alternatively this pattern might be driven by the up-regulation of carbonic anhydrase expression by organisms, which tend to maintain more neutral conditions than their environment (Krulwich et al, 2011), in order to control intra-extra cellular dissolved inorganic carbon gradients (Smith & Ferry, 2000) in response to changes in extra-cellular CO2 and bicarbonate availability (Figure 1 b).…”

“…Whilst the sensitivity of soil kiso to the presence of specific functional groups, like phototrophs which employ carbonic anhydrases in their carbon concentration mechanisms (Badger, 2003), is clear from these studies, the influence of wider community size and composition and it's utility in predicting variations remains uncertain. Soil kiso has also been shown to vary in response to soil pH, with greater rates under alkaline conditions (Sauze et al, 2018). The observed increase, contrary to the decrease (Figure 1 c) that would be expected to be induced by the shift in dissolved inorganic carbon speciation (Figure 1 b) at a constant carbonic anhydrase concentration and efficiency (Figure 1 a), suggests a greater abundance or the presence of more efficient forms of carbonic anhydrases at higher soil pH.…”

“…In alkaline conditions, the predominance of bicarbonate and carbonate acts to inhibit the rate of kiso associated with the hydration reaction and limit the influence of hydroxylation (Figure 1 c). The fact that kiso inferred from patterns in δ 18 O of CO2 fluxes observed under field (Seibt et al, 2006;Wingate et al, 2008Wingate et al, , 2009Wingate et al, , 2010 and laboratory conditions (Jones et al, 2017;Meredith et al, 2019;Sauze et al, 2017Sauze et al, , 2018 can exceed uncatalysed rates predicted by this theoretical basis by up to three orders of magnitude indicates a particular need to better understand variations in the expression of carbonic anhydrases and the controls on their activity in soil environments.…”

“…Indeed, such a response in order to maintain the supply of CO2 in bicarbonate dominated systems has been documented for aquatic phototrophs (Hopkinson et al, 2013). The chemistry of non-carbon anions may also play a role in controlling the activity of carbonic anhydrases (Tibell et al, 1984) with the presence of phosphate for example potentially inhibiting extra-cellular carbonic anhydrase activity in soil solutions and thus decreasing k iso (Sauze et al, 2018).…”

“…The presence of carbonic anhydrases increases the rate of the hydration reaction and the overall rate of interconversion. However, the influence of carbonic anhydrases, for a given concentration and efficiency, is also limited by the presence of high proton concentrations under acidic conditions that inhibit de-protonation required for enzyme regeneration (Rowlett et al, 2002;Sauze et al, 2018). The kiso resulting from these reactions is dependent on the relative abundance of CO2, which is only the dominant form of dissolved organic carbon under acidic conditions, to true carbonic acid, bicarbonate and carbonate in the system (Figure 1 b).…”