Many plankton journey from the cold, dark depths of our oceans to the surface, only to eventually drift down again into the darkness in a perpetual rhythm. Yet, how single-celled phytoplankton, most of which have no appendages to help them swim, make this pilgrimage has remained a mystery. In a paper publishing October 17 in the Cell Press journal Current Biology, researchers describe a species of bioluminescent phytoplankton, called Pyrocystis noctiluca, that balloons to six times their original size of a few hundred microns. This massive inflation allows the plankton to journey up to 200 meters toward the ocean's surface to capture sunlight, then sink back showcasing a unique strategy for long-distance ocean travel.
Phytoplankton are, on average, 5%–10% heavier than seawater, meaning that if they want to remain at the surface to photosynthesize, they have to find a way to best gravity. "We decided to work on things that seemingly have no appendages to swim," says senior author Manu Prakash, a marine biologist and bioengineer at Stanford University. "What we have discovered in this paper is that these P. noctiluca cells are like little submarines that can control their density so precisely that they can choose where they want to be in the water column."
On a research vessel off the coast of Hawaii, Prakash and a postdoctoral fellow at Stanford University, Adam Larson ( @Planktonico ), one of the first authors on the study, stumbled upon a bloom of P. noctiluca and surprisingly found two very different sizes in their nets. "It took a while to piece together why until we recorded the videos where we saw the cells doing this massive inflation," says Larson. "It can happen quite suddenly, so if you sleep by the microscope for 10 minutes, you might miss it."
To test what effects this rapid growth might have on the plankton, the research team utilized their novel "gravity machine." "The gravity machine allows us to see a single cell at subcellular resolution in an infinite water column," says Prakash. "It's a little bit like a Ferris wheel for gerbils or mice but for a single cell. It's the size of a dinner plate and rotates, so the cell doesn't know that it's not climbing or sinking in its own frame of reference." By altering water pressure and density within the gravity machine, the team can create a virtual reality environment mimicking the ocean's depths. With the machine, the team discovered that inflated cells were less dense than the surrounding seawater, letting them escape the downward pull of gravity and float toward the virtual surface.
Further investigation showed this expansion happens as a natural part of the plankton's cell cycle. Once a single-celled plankton divides into two, an internal structure called a vacuole, a kind of flexible water tank, filters in fresh water, causing the two new cells to massively grow in size. These two daughter cells, now swelled with the lighter freshwater, sail upward. "What we realized is that this is a very clever way to essentially slingshot in the ocean during cell division," Prakash says. "So, what happens during normal time? You're making a lot of proteins, you have tons of sunlight, and you make a lot of biomass until you get heavier and you sink. Then, you do cell division in the deeper waters and use inflation to get back to the size of the mother."
The entire cell cycle takes roughly 7 days, coinciding with the plankton's vertical pursuit of light and nutrients. "You can then see how this cell cycle could have evolved," says Prakash. "I think this is the first time we have clear evidence that the cell cycle, which is such a fundamental mechanism of controlling a cell and cell division, is possibly controlled by an ecological parameter."
With these insights in mind, using a theoretical framework, the team discovered the ecological parameter acting as a fundamental limit driving this evolution. "All cells experience a gravitational pull downward, and unless they or subsequent progeny fight back, they will sink forever to the bottom of the ocean in a gravitational trap," says postdoctoral fellow Rahul Chajwa, the other first author of the study, also at Stanford University. Now, using the results from the gravity machine, as well as their ecological and physiological observations, the research team has developed a mathematical framework that could be generalized and applied to all plankton in the ocean.
For future projects, Prakash's lab is looking to uncover hidden mysteries of a vast number of plankton who may use the new biochemistry to regulate density and move up and down the water column. "We have roughly around 600 species in our Behavioral Atlas right now, and we are systematically measuring all kinds of mechanisms. It's turning out that there are four or five different tricks all co-evolving for this function. I think one of the threads that's really fun is that we have a long list of organisms to study; because there are millions of species that live in the ocean, this is the tip of the iceberg."
Hongquan Li, a graduate student in the Prakash lab, is also an author on the study.
