The carbonic anhydrase activity of sinking and suspended particles in the North Pacific Ocean

Abstract

The enzyme carbonic anhydrase (CA) is crucial to many physiological processes involving CO2, from photosynthesis and respiration, to calcification and CaCO3 dissolution. We present new measurements of CA activity along a North Pacific transect, on samples from in situ pumps, sediment traps, discreet plankton samples from the ship's underway seawater line, plankton tows, and surface sediment samples from multicores. CA activity is highest in the surface ocean and decreases with depth, both in suspended and sinking particles. Subpolar gyre surface particles exhibit 10× higher CA activity per liter of seawater compared to subtropical gyre surface particles. Activity persists to 4700 m in the subpolar gyre, but only to 1000 m in the subtropics. All sinking CA activity normalized to particulate organic carbon (POC) follows a single relationship (CA/POC = 1.9 ± 0.2 × 10−7 mol mol−1). This relationship is consistent with CA/POC values in subpolar plankton tow material, suspended particles, and core top sediments. We hypothesize that most subpolar CA activity is associated with rapidly sinking diatom blooms, consistent with a large mat of diatomaceous material identified on the seafloor. Compared to the basin‐wide sinking CA/POC relationship, a lower subtropical CA/POC suggests that the inventory of subtropical biomass is different in composition from exported material. Pteropods also demonstrate substantial CA activity. Scaled to the volume within pteropod shells, first‐order CO2 hydration rate constants are elevated ≥ 1000× above background. This kinetic enhancement is large enough to catalyze carbonate dissolution within microenvironments, providing observational evidence for CA‐catalyzed, respiration‐driven CaCO3 dissolution in the shallow North Pacific.

The Role of Extracellular Carbonic Anhydrase in Biogeochemical Cycling: Recent Advances and Climate Change Responses

“…To date, the cellular quotas of Zn attached to CA in marine phytoplankton remain an open question. Subhas, et al [ 50 ] estimated the use of Zn quota by marine phytoplankton assemblages from the North Pacific Ocean to be in the range of 10–40% using Zn/phosphate and CA/particulate organic carbon (CA/POC) ratios. The estimated values are 10 times lower than our previous estimation from a laboratory experiment using monoculture solutions [ 18 ].…”

A Mechanistic Study of Carbonic Anhydrase‐Enhanced Calcite Dissolution

“…This ratio could potentially vary in other oceanographic provinces with different phytoplankton communities, as diatoms commonly have extracellular CA whereas cyanobacteria do not (Hopkinson et al, 2013). Scaled to the volume of individual pteropod shell and marine snow particles, Subhas et al (2019) calculated localized CA concentration of 0.06–0.32 mg CA g −1 seawater using the POC concentration and CA/POC ratio in these microenvironments. These CA concentrations are comparable to measured CA activities in extracellular diatom boundary layer and their internal compartments (0.09–6.8 mg CA g −1 seawater, Hopkinson et al, 2011, 2013) and are higher than those documented to catalyze calcite dissolution in natural seawater (0.01–0.04 mg CA g −1 seawater, Subhas et al, 2017).…”

“…CA exists both intracellularly (iCA) and extracellularly (eCA) and is often associated with the cell wall, plasma membrane, or periplasmic space (Badger, 2003; Burkhardt et al, 2001; Elzenga et al, 2000; Hopkinson et al, 2013; Moroney et al, 1985; Nimer et al, 1999; etc.). In natural seawater, eCA extracted from cell membranes is measured to be (3.0–20.1) × 10 −6 mg CA g −1 seawater in the Baltic Sea (Mustaffa et al, 2017) and (0–5.1) × 10 −9 M in the North Pacific (Subhas et al, 2019). Subhas et al (2019) also show that ~90% of the CA activity is externally bound in natural oceanic environments by showing similar CA activities between sonicated and vortexed samples.…”

“…In natural seawater, eCA extracted from cell membranes is measured to be (3.0–20.1) × 10 −6 mg CA g −1 seawater in the Baltic Sea (Mustaffa et al, 2017) and (0–5.1) × 10 −9 M in the North Pacific (Subhas et al, 2019). Subhas et al (2019) also show that ~90% of the CA activity is externally bound in natural oceanic environments by showing similar CA activities between sonicated and vortexed samples. In the North Pacific, CA activity in sinking particles normalized to particulate organic carbon (POC) follows a single relationship (CA/POC = (1.9 ± 0.2) × 10 −7 mol mol −1 ), consistent with CA/POC values in plankton tow materials and picked pteropods during the same cruise, whereas suspended particles have generally lower and varying CA/POC values of (0–2) × 10 −7 mol mol −1 .…”

“…In addition to its effects in vivo, CA has also been experimentally shown to catalyze the dissolution kinetics of calcium carbonate, in freshwater karst environments far from equilibrium (Liu, 2001; Liu et al, 2005) and in seawater near equilibrium (Subhas et al, 2017). The elevated carbonate dissolution rates in the presence of CA may have critical, yet underestimated, impact on the rate of chemical weathering (Liu et al, 2005; Thorley et al, 2015; Xie & Wu, 2014) and the rate at which alkalinity is recycled in the ocean (Subhas et al, 2019). In fact, the substantial amount of calcium carbonate dissolution in middepths (600 to 900 m) of the water column in the North Pacific (Berelson et al, 2007; Feely et al, 2002) likely occur within confined acidic environments such as diffusively limited marine snow aggregates or the guts of zooplankton/metazoan (Dong et al, 2019), and this leaves open the possibility that CA produced by marine organisms can catalyze the dissolution of calcium carbonate in these confined settings in situ (Subhas et al, 2019).…”