Drift against the Tide


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Diatom cells expressing ROS-sensitive proteins in the nucleus (green) and chlorophyll (red)


They are the foundation of the entire marine food chain – without them there would be no life in the ocean. They are also responsible for half the photosynthetic activity on the planet – rivaling rainforests in carbon dioxide absorbed and oxygen released. These are impressive feats for phytoplankton – microscopic single-celled organisms that range in size from 1 to 100 microns (smaller than the width of a human hair) and make up less than one percent of Earth’s biomass.

The name phytoplankton means “plant drifters” in Greek.  But are they really just passive wanderers at the mercy of the ocean currents, or is there more to them than meets the eye? Dr. Assaf Vardi of the Weizmann Institute’s Plant Sciences Department is looking to overturn this common paradigm by revealing the molecular mechanisms underpinning their ecological success. In new research published in Proceedings of the National Academy of Sciences (PNAS), Vardi, and Dr. Shilo Rosenwasser and their team have discovered that phytoplankton have developed an active stress surveillance system to help them cope with their ever-changing environment.
Dr. Assaf Vardi
Vardi: “Phytoplankton blooms are amazing biological phenomena, forming communities that span thousands of kilometers across the ocean and depths of up to 100 meters. But such environmental stresses as lack of carbon dioxide, sunlight or nutrients, or virus attacks, among other factors, can cause a bloom’s rapid demise. To be ecologically successful, an organism needs to be alert and on guard in order to respond and adapt to its environment.”

The research team found that phytoplankton’s stress surveillance system begins at home. When organisms carry out metabolic processes such as photosynthesis and respiration, they produce a toxic byproduct called ROS (reactive oxygen species). At low levels, this is usually no cause for concern – in fact, it has recently been recognized that ROS may function as signals to promote cell proliferation and survival. When phytoplankton cells are exposed to environmental stress, however, as in many pathophysiological conditions, ROS are overproduced; and this can lead to disease and ultimately to cell death.
Using a unique proteomics approach, which was developed by Vardi’s team in collaboration with Dr. Yishai Levin of the Nancy and Stephen Grand Israel National Center for Personalized Medicine, the scientists discovered that phytoplankton have a large network of hundreds of ROS-sensitive proteins. This protein network can respond rapidly to changes in ROS levels produced under various stress conditions and transmit signals aimed at activating specific biological pathways. The information they perceive is then used to determine the cell’s fate: If ROS levels are relatively low, the cell can “rescue” itself by adapting its metabolic activity so that less ROS are produced; antioxidants are also produced to “scavenge” the extra ROS and reduce their toxic effects. If ROS reach levels beyond repair, however, a type of programmed cell suicide is activated.

By coupling the proteomics approach to live measurements of ROS levels in different subcellular locations under stress conditions, the scientists can now predict which sub-network of proteins will be activated under a given stress condition and the specific metabolic pathways they will trigger to achieve stress acclimation. They have also shown that the surveillance system works in a rapid and reversible manner – an important factor in enabling it to continually detect new stress.
Diagram of ROS-sensitive proteins in key metabolic pathways and their intracellular locations in diatoms. Identified ROS-sensitive proteins are highlighted in red, showing the difference in degree of oxidation when the cell is under stress. ROS-sensitive reactions participating in nitrogen metabolism are highlighted in bold


To corroborate these findings, the scientists conducted a more specific investigation into what happens to cells under conditions of nitrogen starvation – nitrogen being an essential component for the formation of blooms. They revealed that different locations within the cell respond differently to fluctuations in nitrogen availability, suggesting that this may serve as a signaling mechanism allowing cross-talk between intracellular organelles. These organelles can then mount an appropriate response, triggering specific biological pathways according to the cell’s needs.

“The beauty of these findings is that phytoplankton ‘invented’ photosynthesis more than 2.3 billion years ago, which helped to drive evolution. But the downside is that with the production of oxygen came toxic ROS. We believe that they co-evolved this sensor protein network to help them adapt to environmental stress,” says Vardi. “At the same time, the suggestion that single-celled organisms have a program to activate cell death raises controversial questions: How do single-celled organisms carry genes that cause death in the first place? And since cellular suicide is an evolutionary dead end for the single cell, what are the consequences of such cell fate decisions for the population of cells?”
Understanding the ecology and evolution of these ancient microorganisms has wide-ranging implications, which may, among other things, help reveal how highly conserved metabolic pathways across kingdoms adapt to high ROS levels or gauge the effect of a bloom’s demise on global warming. Those adaptations may also have implications for the understanding of human cellular metabolism, in which ROS play a crucial role in health and disease, as well as advancing the use of phytoplankton and other microorganisms in the biotech industry for biofuel development.  
Dr. Assaf Vardi's research is supported by Charles Rothschild, Brazil; Roberto and Renata Ruhman, Brazil; Luis Stuhlberger, Brazil; the Lord Sieff of Brimpton Memorial Fund; the European Research Council; and the estate of Samuel and Alwyn J. Weber. Dr. Vardi is the incumbent of the Edith and Nathan Goldenberg Career Development Chair.