A widespread species of ocean-dwelling microorganisms has been found to employ a never-before-seen alternative method of photosynthesis.
The discovery has implications not only for scientists' basic understanding of photosynthesis—arguably the most important biological process on Earth—but also for the amount of carbon dioxide that phytoplankton pull from the atmosphere.
Until now, it was thought that all the photosynthetic algae and bacteria living in the ocean drew carbon dioxide out of the air and used it to build sugars and other carbon-rich molecules to use as fuel. But two new studies by researchers at Stanford and the Carnegie Institution show that Synechococcus, a type of cyanobacteria (formerly called blue-green algae) that dominates much of the world's oceans, has evolved a mechanism that short-circuits photosynthetic carbon-dioxide fixation while still producing energy. The alternate approach is found in regions of the ocean where some of the ingredients necessary for traditional photosynthesis are in short supply.
"The amount of carbon dioxide being drawn down by the phytoplankton in nutrient-poor oceans might turn out to be significantly lower than we thought," said Shaun Bailey, a postdoctoral researcher working in the Carnegie Institution's Department of Plant Biology with Arthur Grossman, a staff scientist at the institution and a professor, by courtesy, in Stanford's Biology Department.
Bailey is the lead author of the paper describing part of the work in Biochimica et Biophysica Acta 1777 (2008). Kate Mackey, a graduate student in civil and environmental engineering at Stanford, is lead author of a second paper describing the work, currently in press at Limnology and Oceanography.
Until now, researchers have estimated marine photosynthetic activity by analyzing satellite images of the world's oceans to determine how much chlorophyll was in the water. Since chlorophyll is needed for photosynthesis, it was thought that measuring its concentration would be a straightforward way of estimating the amount of photosynthesis that would occur and therefore how much carbon dioxide would be consumed, or "fixed," by the phytoplankton. But the new work suggests that the relationship between the amount of chlorophyll in the water and the amount of carbon dioxide fixation by phytoplankton is not consistent throughout the world's oceans.
"There is a new twist on photosynthesis here, and that has to be accounted for when it comes to CO2 modeling," Bailey said, adding that, in some cases, the models may overestimate the amount of carbon fixation that occurs in nutrient-poor waters.
It is not yet clear what the finding might mean to studies of long-term global warming, he said, but it will have to be incorporated into any models that include carbon fixing by phytoplankton as a factor.
Synechococcus caught the interest of Grossman and his team because it thrives in vast areas of the ocean that are relatively deficient in iron, an element that is critical for certain reactions in the normal process of photosynthesis. How Synechococcus could maintain its abundance in the face of that deficiency was a puzzle.
"It seems that Synechococcus in the oligotrophic [nutrient-poor] oceans has solved the iron problem, at least in part by short-circuiting the standard photosynthetic process," Grossman said. "Much of the time this organism bypasses stages in photosynthesis that require the most iron. As it turns out, these are also the stages in which CO2 is taken from the atmosphere."
"We realized very quickly that there was something different about the Synechococcus that we were studying," said Bailey, the lead postdoctoral fellow working on the project. "The uptake of CO2 and the photosynthetic activities didn't match, so we knew that something other than CO2 was being consumed by photosynthesis, and it turned out to be oxygen." The researchers have tentatively identified the enzyme involved in this process to be plastoquinol terminal oxidase, or PTOX.
Bailey worked with Synechococcus in the laboratory, but recently this newly discovered phenomenon was shown to occur in nature by Mackey, who made direct measurements of photosynthesis in field samples from the Atlantic and Pacific oceans.
"The low-nutrient, low-iron environments account for about half of the area of the world's oceans, so they represent a large portion of the Earth's surface available for photosynthesis," Mackey said. "Our findings show that this novel cycle occurs in two major ocean basins and suggest that a substantial amount of energy from sunlight gets re-routed away from carbon fixation during photosynthesis. This may mean that less CO2 is being removed from the atmosphere by the open ocean photosynthetic organisms than was previously believed."
"This discovery represents a paradigm shift in our view of photosynthesis by organisms in the vast, nutrient-starved areas of the open ocean," said Joe Berry of the Carnegie Institution's Department of Global Ecology. "We had assumed that like higher plants, the goal was to make carbohydrates from CO2 and store them for later use as a source of energy for any number of cellular functions or growth. We now know that some organisms short-circuit this complicated process, using light in a minimalist way to power cellular processes directly with a far simpler and cheaper—in terms of scarce nutrients such as iron—photosynthetic apparatus. We don't know the full significance of this finding yet, but it is certain to change the way we interpret optical measurements of photosynthetic pigments in the ocean and the way we model ocean productivity."
Wolf Frommer, director of the Carnegie Institution's Department of Plant Biology, agreed on the discovery's ground-breaking importance. "If we thought we have understood photosynthesis, this study proves that there is much to be learned about these basic physiological processes," he said.
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