It is true that many organisms, including some macroalgae, get CO2 from bicarbonate, and that may be where the misunderstanding arises. That process uses bicarbonate, but does not consume any alkalinity.
I discuss that in this article:
Photosynthesis and the Reef Aquarium, Part I: Carbon Sources by Randy Holmes-Farley - Reefkeeping.com
Obtaining Carbon Dioxide from Bicarbonate: Carbonic Anhydrase
If an organism is to obtain carbon dioxide from bicarbonate, several potential processes are available, and different organisms take different approaches. In many cases, the exact mechanisms have not been established. It is much easier to show that bicarbonate is a source of carbon dioxide for marine organisms than to show exactly how they take it up. A bicarbonate ion, being charged and insoluble in organic phases, cannot readily diffuse across cell membranes, so other mechanisms are needed.
Such uncertainty of mechanism is the case for
Ulva lactuca, for example. It has been shown to be able to photosynthesize when out of the water (say, exposed at low tide), taking up carbon dioxide directly, and also when in the water, taking up bicarbonate.10 But the exact mechanism of using bicarbonate to obtain carbon dioxide isn't known in this species.
One common way to use bicarbonate is for the cells exposed to the seawater to use extracellular carbonic anhydrase on their surfaces. As mentioned above, the enzyme carbonic anhydrase catalyzes the hydration and dehydration of carbon dioxide and carbonic acid, respectively. These organisms present this enzyme to the bicarbonate-rich seawater surrounding them. Because the bicarbonate is naturally in rapid equilibrium with carbonic acid, and the carbonic anhydrase keeps the carbonic acid in rapid equilibrium with unhydrated carbon dioxide, the bicarbonate is used as a ready pool to supply carbon dioxide to passively cross cell membranes and be taken up (shown schematically below).
The agarophyte
Gracilaria lemaneiformis11 has been shown to take up carbon in this fashion. It has carbonic anhydrase both inside the organism and out. Inhibiting either of these types of carbonic anhydrase greatly decreases photosynthesis, but adding an anion transport inhibitor does not. Adding TRIS buffer to the extracellular fluid (seawater) also has no effect (the purpose of which is discussed in the following section relating to proton pumping as a possible mechanism).
Photosynthesis in this organism is greatly reduced as the pH is raised (73% reduction when going from pH 8.0 to 9.0), presumably because the bicarbonate's propensity to form carbonic acid is reduced at higher pH.
The brown alga,
Hizikia fusiforme (Sargassaceae),12 from the South China Sea, has also been shown to exhibit carbonic anhydrase activity, both inside and out, and has been shown to be incapable of actively and directly transporting bicarbonate. Consequently, its carbon dioxide concentration likely operates by the mechanism shown above.
Two species of marine prymnesiophytes (
Dicrateria inornataand
Ochrosphaera neapolitana)13 have been shown, through the use of various carbonic anhydrase inhibitors, to use extracellular carbonic anhydrase to collect carbon dioxide from ambient bicarbonate. They also employ an energy dependent process for taking up carbon dioxide itself. Growth in high carbon dioxide environments represses the expression of carbonic anhydrase active in these species, but does not reduce the active uptake of carbon dioxide.
Obtaining Carbon Dioxide from Bicarbonate: Direct Uptake
An alternative way to obtain carbon dioxide via seawater bicarbonate is to take up the bicarbonate through protein transport mechanisms across the cell membranes, and then once inside the cells where it is needed, carbonic anhydrase converts it into carbon dioxide and hydroxide ion. The hydroxide is then pumped out, or H+ is pumped in, to achieve pH balance.
Transporting ions across cell membranes using protein transporters is a widespread mechanism whereby organisms can get needed ions across a membrane through which they do not normally diffuse. Some of these are active transporters, using chemical energy to "pull" ions out of the extracellular fluid (our push them out, as necessary), and other transporters simply allow specific ions to pass though from high concentration on one side to lower concentration on the other side.
The marine red alga
Gracilaria conferta has been shown to have an active bicarbonate uptake mechanism.14 Three marine bloom-forming (red tide) dinoflagellates,
Prorocentrum minimum,
Heterocapsa triquetra and
Ceratium lineatum,15have been shown to take up bicarbonate directly. They show little carbonic anhydrase activity, yet bicarbonate accounts for approximately 80% of the carbon dioxide they use in photosynthesis. It is believed that these dinoflagellates are not carbon limited in photosynthesis due to their efficient direct bicarbonate uptake mechanisms.
The marine diatom
Phaeodactylum tricornutum16 was found not only to have an active bicarbonate uptake mechanism, but the researchers further identified at least two different mechanisms. In particular, they showed that part of the uptake depended on the presence of extracellular potassium, and this part of the total carbon dioxide uptake was eliminated when potassium was missing from the medium. A second direct bicarbonate uptake mechanism was independent of potassium, indicating the presence of at least two different pathways for transporting bicarbonate into this organism.
Obtaining Carbon Dioxide from Bicarbonate: Proton Pumping
Another way to obtain carbon dioxide via seawater bicarbonate is to pump H+ out of the cells into the extracellular fluid (seawater near the cells) or into a special cavity where bicarbonate is present.17 This low pH causes the bicarbonate to become protonated to become carbonic acid. The carbonic acid can then transform into carbon dioxide, and pass across the cell membranes.
The seagrass
Zostera noltii Hornem18 has been shown, for example, to use proton pumping to gather bicarbonate in the form of carbonic acid from the water. It contains no extracellular carbonic anhydrase, but rather uses ATP (adenosine triphosphate, the fundamental currency of chemical energy in most organisms) to drive the export of H+. Evidence for this mechanism is found by adding a buffer to the seawater (TRIS) without changing the pH. This buffer keeps the pH near the cell surface constant, counteracting the beneficial effect of the proton pumping in lowering pH and converting bicarbonate into carbonic acid. The simple presence of a non-absorbed buffer in the water can decrease the rate of photosynthesis in this organism by almost 80%.
Interestingly, those seagrass specimens acclimated to high light (where high rates of photosynthesis and consequent uptake of bicarbonate would be highest) showed the greatest ability to actively take up bicarbonate. In high light experiments, these previously high light-acclimated specimens were shown to be only light limited, while the shade-acclimated organisms were both light and carbon limited when put into high light.18 Other seagrass species (e.g.,
Z. mulleriand
Z. marina) have been shown to have external carbonic anhydrase, and so may have different uptake mechanisms.18
Photosynthesis of Macroalgae as a Function of pH
One of the side effects of the necessity of taking up carbon dioxide to photosynthesize is that pH may affect the rate of photosynthesis, because the amount of carbon dioxide (as CO2or H2CO3) in the water varies with pH. Assuming constant carbonate alkalinity, the effect is quite strong. A drop of 0.3 pH units implies a doubling of the carbon dioxide concentration. A reef aquarium at pH 8.5, for example, has one fourth the carbon dioxide of a reef aquarium at pH 7.9, assuming the carbonate alkalinity is the same.
Aquarists may rightly wonder whether organisms are able to photosynthesize efficiently as the pH is raised. The answer is mixed. Some can and some cannot. Those organisms that rely solely on carbon dioxide may not. Those that rely on both carbon dioxide and bicarbonate have a better chance of retaining efficiency at higher pH because a much larger amount of bicarbonate is present, and it does not change as rapidly with pH over the range of interest to aquarists.
Table 1 shows the response of a variety of macroalgae in terms of their ability to photosynthesize at pH 8.1 and 8.7. In seawater with constant carbonate alkalinity, there is 20% as much carbon dioxide at pH 8.7 as at pH 8.1, so an organism relying on carbon dioxide alone might experience a large drop in photosynthetic rate over this range. Clearly, the response varies with species.
Chaetomorpha aerea, in particular, may be of substantial interest to aquarists. It is not necessarily the exact species that many grow in refugia (which is unidentified as far as I can tell), but this species of
Chaetomorpha shows a 25% drop in photosynthesis when exposed to the higher pH. That drop is not as large as some other species, but may still be important, and it is more than many other species of macroalgae.
Of course, the photosynthesis rate does not necessarily translate to growth rates. If other nutrients are limiting growth (nitrogen, phosphorus, iron, etc.), then it may not matter if the rate of photosynthesis is reduced at higher pH. But because these nutrients are often present in surplus in reef aquaria, it may well be that carbon uptake is limiting in some cases, and in those cases aquarists might benefit from ensuring that the pH is not too high.
