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How the “Other” ATP Synthase Saves the Planet

Photo: Pacific Ocean, by NASA, Apollo 11, Public domain, via Wikimedia Commons.

ATP synthase has been featured here many times because of its exquisite rotary mechanism and efficient operation. Viewers of animations like ours on YouTube usually need little convincing that it looks designed. And when they learn more details, like its 6,000-rpm speed, its crankshaft, and three-part ATP manufacturing center, the intuition becomes difficult to dislodge, even when evolutionists insist it emerged by chance. It’s a well-deserved icon of intelligent design.

The one most often referred to is the F-type of ATP synthase shown in the video. But there’s another one — the V-type ATPase — that is no less wondrous. It looks similar to the F-type, but V-type ATPases (let’s call them VHA) work in reverse: instead of using the proton motive force generated by the electron transport chain to manufacture ATP, they spend the ATP “energy currency” molecules to pump protons into organelles, thereby increasing the acidity. They are often found on the membranes of vacuoles that need H+ ions to lower the pH for phagocytosis or other types of digestive or recycling functions. Scientists have now shown they are more widely distributed in the cell than thought.

Our body cells contain both types of ATPase. But why do I say that these VHA rotary engines save the planet? A report by Daniel P. Yee in Current Biology tells the story. 

It Begins in the Ocean

Diatoms, dinoflagellates, and coccolithophores are dominant groups of marine eukaryotic phytoplankton that are collectively responsible for the majority of primary production in the ocean. [Emphasis added.]

Primary production represents the bottom of the food chain, on which higher organisms depend. Photosynthetic microbes in the ocean are the major players. For present purposes, we can ignore the authors’ evolutionary story about how these marine microbes obtained their VHAs by some “selective advantage.” It suffices to focus on what the molecular machines do: 

Since intracellular digestive vacuoles are ubiquitously acidified by V-type H+-ATPase (VHA), proton pumps were proposed to acidify the microenvironment around secondary chloroplasts to promote the dehydration of dissolved inorganic carbon (DIC) into CO2, thus enhancing photosynthesis.

We report that VHA is localized around the chloroplasts of centric diatoms and that VHA significantly contributes to their photosynthesis across a wide range of oceanic irradiances.

More photosynthesis means more primary production, and more support for a diverse biosphere. 

Based on the contribution of diatoms to ocean biogeochemical cycles, VHA-mediated enhancement of photosynthesis contributes at least 3.5 Gtons of fixed carbon per year (or 7% of primary production in the ocean), providing an example of a symbiosis-derived evolutionary innovation with global environmental implications.

Once again, the evolutionary tale is non-essential for the surprising implication: all life benefits from the enhancement of photosynthesis provided by VHA molecular motors in diatoms. The 7 percent number is undoubtedly much higher if the other dominant groups of marine phytoplankton are factored in. Additional tests showed the research team that similar VHA-mediated enhancement of photosynthesis occurs in coccolithophores, dinoflagellates, and probably in all photosynthetic organisms.

The paper’s diagram of VHA in Figure 2 looks almost identical to the F-type ATP synthase except for the direction of proton (H+ ion) flow. Both types could be described by ID proponents as irreducibly complex molecular engines based on the parts list alone:

The VHA is a holoenzyme protein complex that is composed of 16 subunits, with a membrane spanning V0-domain and cytosolic facing catalytic V1-domain (Figure 2A). Transcriptomic analysis of synchronized cultures of T. pseudonana [a centric diatom] demonstrated constitutive mRNA expression of all VHA subunits, suggesting that VHA is important throughout the cell cycle (Figure 2B). However, the VHA holoenzyme can have multiple subcellular localizations and functions.

While the familiar F-type ATP synthase is localized to the mitochondria (in animals) or chloroplasts (in photosynthetic microbes and plants), V-types are found in other subcellular locations. They perform more functions due to their proton-pumping action that can adjust pH of their surroundings. This has made them difficult to study. A few functions are known.

But How Many Others Are There?

In diatoms, VHA has been reported in the membranes of vacuoleschloroplast endoplasmic reticulum (cER), and silica deposition vesicles (SDVs), where it is strictly required for biomineralization of the silica cell wall and cell division. The complexity and functional versatility of VHA are challenges for genetic manipulation approaches that would constitutively destabilize multiple physiological functions and confound phenotypic interpretation. They also rule out the use of transcriptomics to infer the physiological role(s) of VHA, as these analyses cannot not provide information about the subcellular localization of the VHA holoenzyme.

The authors were excited about another implication of their discovery: carbon sequestration. Because VHA machines substantially enhance photosynthesis, it means more carbon is converted into CO2 which the chloroplast needs for sugar synthesis. The slight pH decrease provided by the VHA proton pumps changes the chemistry to favor CO2 production, which would be bad; but simultaneously, it creates a gradient that favors moving the CO2 into the chloroplast instead of into the cytoplasm where it would escape into the atmosphere. As a result, more oxygen is released by photosynthesis, less CO2 is released into the atmosphere during photosynthesis, and when the diatoms die and fall to the ocean floor, they take the solid carbon with them. V-type ATPases thus perform another global function for the biosphere: a carbon-concentrating mechanism (CCM).

VHA is a universal feature of eukaryotic cells and is present in a number of organelles, including endosomes, phagosomes, macropinosomes, lysosomes, Golgi, and melanosomes. Since VHA invariably acidifies the lumen of each of these organelles to pH ≤ 6, we deduce that VHA in the cER/PP membranes of T. pseudonana must accomplish a similar effect. This is significant, because at pH ≤ 6.3, the majority of DIC [dissolved inorganic carbon] equilibrates to CO2. Hence, we propose that VHA promotes CO2 accumulation in the microenvironment external to the chloroplast. Consistent with model simulations of DIC fluxes in the diatom CCM, some of the CO2 would diffuse back into the cytoplasm (pH ∼ 7.2). However, the higher pH in the chloroplast stroma (pH ∼ 8.15) establishes a more favorable partial pressure gradient for CO2 diffusion into this compartment (Figure S3B). The next steps follow the established CCM of microalgae. In the stroma, CO2is immediately hydrated into HCO3− under catalysis by carbonic anhydrase, which is shuttled into the thylakoid lumen where pH is ≤ 6 due to H+ pumping associated with photosynthetic electron transport chain. At the acidic pH, HCO3− dehydrates into CO2 and diffuses into the pyrenoid matrix, saturating RuBisCo to maximize carbon fixation rates.

A Remarkable Synergy 

This shows a remarkable synergy of molecular machines and chemistry in a highly localized microenvironment. VHAs acidify the chloroplast exterior, helping carbonic anhydrase use the excess CO2 to produce more bicarbonate ions. The pH gradient favors these negative ions to flow toward the proton motive force being generated by the electron transport chain (Complexes I-IV) that are powering the F-type ATP synthase motors (Complex V). As the bicarbonate ions dehydrate back to CO2 where the pH drops inside the chloroplast, they saturate Rubisco enzymes that convert the CO2 into nutrients for life. 

Notice this careful pH-mediated series of delicate chemical reactions. Within this microenvironment, CO2 gets utilized where needed, but is not released into the atmosphere. The products of Rubisco favor carbon compounds that will get buried in the ocean floor. The result? A carbon-concentrating mechanism that helps the atmosphere gain more oxygen but less carbon dioxide, while enriching the biosphere with nutrients. VHA, the “other” ATP synthase, saves the planet! VHA should be seen as a key player in the carbon cycle, the oxygen cycle, the food chain, and the climate. 

Nearly Unrestrained Wonder

The authors can hardly restrain their wonder at all this:

In summary, O2 production, 13C-NanoSIMS, and 14C-P-E measurements demonstrated that VHA significantly contributes to photosynthetic carbon fixation that is retained as biomass. Given that diatoms contribute nearly 50% of carbon fixation in the ocean, the component of photosynthesis that depends on VHA represents between ∼7% and 25% of oceanic primary production, or between 3.5 and 13.5 Gtons of fixed carbon per year (Table S3). These numbers can only increase after accounting for VHA-mediated photosynthesis in other secondary endosymbiotic phytoplankton (Figure 1) and photosymbiotic invertebrates. In addition, diatoms constitute about half of the biomass that sinks into the ocean’s interior. Based on our measurements of the contribution of VHA on both gross and net productivity in diatoms, VHA-mediated carbon fixation is poised to significantly contribute to the biological pump that shuttles organic carbon to the ocean’s interiorand, on a geologic time scale, to the biomass buried in the continental margin that formed fossil fuel deposits. Even by the most conservative estimate, the cooption of VHA for the enhancement of photosynthesis is a symbiosis-derived evolutionary innovation with global environmental implications.

Some future day, when biologists finally admit that evolution is incapable of innovation of complex finely tuned cooperative systems, all scientists will marvel at the intelligent design that gives us air to breathe and edible carbon to ingest under a moderate climate. Some of us are ahead of that time.