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    An abundant phytoplankton feeds a global network of marine microbes

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    One of the hardest-working organisms in the ocean is the tiny, emerald-tinged Prochlorococcus marinus. These single-celled “picoplankton,” which are smaller than a human red blood cell, can be found in staggering numbers throughout the ocean’s surface waters, making Prochlorococcus the most abundant photosynthesizing organism on the planet. (Collectively, Prochlorococcus fix as much carbon as all the crops on land.) Scientists continue to find new ways that the little green microbe is involved in the ocean’s cycling and storage of carbon.Now, MIT scientists have discovered a new ocean-regulating ability in the small but mighty microbes: cross-feeding of DNA building blocks. In a study appearing today in Science Advances, the team reports that Prochlorococcus shed these extra compounds into their surroundings, where they are then “cross-fed,” or taken up by other ocean organisms, either as nutrients, energy, or for regulating metabolism. Prochlorococcus’ rejects, then, are other microbes’ resources.What’s more, this cross-feeding occurs on a regular cycle: Prochlorococcus tend to shed their molecular baggage at night, when enterprising microbes quickly consume the cast-offs. For a microbe called SAR11, the most abundant bacteria in the ocean, the researchers found that the nighttime snack acts as a relaxant of sorts, forcing the bacteria to slow down their metabolism and effectively recharge for the next day.Through this cross-feeding interaction, Prochlorococcus could be helping many microbial communities to grow sustainably, simply by giving away what it doesn’t need. And they’re doing so in a way that could set the daily rhythms of microbes around the world.“The relationship between the two most abundant groups of microbes in ocean ecosystems has intrigued oceanographers for years,” says co-author and MIT Institute Professor Sallie “Penny” Chisholm, who played a role in the discovery of Prochlorococcus in 1986. “Now we have a glimpse of the finely tuned choreography that contributes to their growth and stability across vast regions of the oceans.”Given that Prochlorococcus and SAR11 suffuse the surface oceans, the team suspects that the exchange of molecules from one to the other could amount to one of the major cross-feeding relationships in the ocean, making it an important regulator of the ocean carbon cycle.“By looking at the details and diversity of cross-feeding processes, we can start to unearth important forces that are shaping the carbon cycle,” says the study’s lead author, Rogier Braakman, a research scientist in MIT’s Department of Earth, Atmospheric and Planetary Sciences (EAPS).Other MIT co-authors include Brandon Satinsky, Tyler O’Keefe, Shane Hogle, Jamie Becker, Robert Li, Keven Dooley, and Aldo Arellano, along with Krista Longnecker, Melissa Soule, and Elizabeth Kujawinski of Woods Hole Oceanographic Institution (WHOI).Spotting castawaysCross-feeding occurs throughout the microbial world, though the process has mainly been studied in close-knit communities. In the human gut, for instance, microbes are in close proximity and can easily exchange and benefit from shared resources.By comparison, Prochlorococcus are free-floating microbes that are regularly tossed and mixed through the ocean’s surface layers. While scientists assume that the plankton are involved in some amount of cross-feeding, exactly how this occurs, and who would benefit, have historically been challenging to probe; any stuff that Prochlorococcus cast away would have vanishingly low concentrations,and be exceedingly difficult to measure.But in work published in 2023, Braakman teamed up with scientists at WHOI, who pioneered ways to measure small organic compounds in seawater. In the lab, they grew various strains of Prochlorococcus under different conditions and characterized what the microbes released. They found that among the major “exudants,” or released molecules, were purines and pyridines, which are molecular building blocks of DNA. The molecules also happen to be nitrogen-rich — a fact that puzzled the team. Prochlorococcus are mainly found in ocean regions that are low in nitrogen, so it was assumed they’d want to retain any and all nitrogen-containing compounds they can. Why, then, were they instead throwing such compounds away?Global symphonyIn their new study, the researchers took a deep dive into the details of Prochlorococcus’ cross-feeding and how it influences various types of ocean microbes.They set out to study how Prochlorococcus use purine and pyridine in the first place, before expelling the compounds into their surroundings. They compared published genomes of the microbes, looking for genes that encode purine and pyridine metabolism. Tracing the genes forward through the genomes, the team found that once the compounds are produced, they are used to make DNA and replicate the microbes’ genome. Any leftover purine and pyridine is recycled and used again, though a fraction of the stuff is ultimately released into the environment. Prochlorococcus appear to make the most of the compounds, then cast off what they can’t.The team also looked to gene expression data and found that genes involved in recycling purine and pyrimidine peak several hours after the recognized peak in genome replication that occurs at dusk. The question then was: What could be benefiting from this nightly shedding?For this, the team looked at the genomes of more than 300 heterotrophic microbes — organisms that consume organic carbon rather than making it themselves through photosynthesis. They suspected that such carbon-feeders could be likely consumers of Prochlorococcus’ organic rejects. They found most of the heterotrophs contained genes that take up either purine or pyridine, or in some cases, both, suggesting microbes have evolved along different paths in terms of how they cross-feed.The group zeroed in on one purine-preferring microbe, SAR11, as it is the most abundant heterotrophic microbe in the ocean. When they then compared the genes across different strains of SAR11, they found that various types use purines for different purposes, from simply taking them up and using them intact to breaking them down for their energy, carbon, or nitrogen. What could explain the diversity in how the microbes were using Prochlorococcus’ cast-offs?It turns out the local environment plays a big role. Braakman and his collaborators performed a metagenome analysis in which they compared the collectively sequenced genomes of all microbes in over 600 seawater samples from around the world, focusing on SAR11 bacteria. Metagenome sequences were collected alongside measurements of various environmental conditions and geographic locations in which they are found. This analysis showed that the bacteria gobble up purine for its nitrogen when the nitrogen in seawater is low, and for its carbon or energy when nitrogen is in surplus — revealing the selective pressures shaping these communities in different ocean regimes.“The work here suggests that microbes in the ocean have developed relationships that advance their growth potential in ways we don’t expect,” says co-author Kujawinski.Finally, the team carried out a simple experiment in the lab, to see if they could directly observe a mechanism by which purine acts on SAR11. They grew the bacteria in cultures, exposed them to various concentrations of purine, and unexpectedly found it causes them to slow down their normal metabolic activities and even growth. However, when the researchers put these same cells under environmentally stressful conditions, they continued growing strong and healthy cells, as if the metabolic pausing by purines helped prime them for growth, thereby avoiding the effects of the stress.“When you think about the ocean, where you see this daily pulse of purines being released by Prochlorococcus, this provides a daily inhibition signal that could be causing a pause in SAR11 metabolism, so that the next day when the sun comes out, they are primed and ready,” Braakman says. “So we think Prochlorococcus is acting as a conductor in the daily symphony of ocean metabolism, and cross-feeding is creating a global synchronization among all these microbial cells.”This work was supported, in part, by the Simons Foundation and the National Science Foundation. More

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      in Environment

      Ocean microbes get their diet through a surprising mix of sources, study finds

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      One of the smallest and mightiest organisms on the planet is a plant-like bacterium known to marine biologists as Prochlorococcus. The green-tinted microbe measures less than a micron across, and its populations suffuse through the upper layers of the ocean, where a single teaspoon of seawater can hold millions of the tiny organisms.

      Prochlorococcus grows through photosynthesis, using sunlight to convert the atmosphere’s carbon dioxide into organic carbon molecules. The microbe is responsible for 5 percent of the world’s photosynthesizing activity, and scientists have assumed that photosynthesis is the microbe’s go-to strategy for acquiring the carbon it needs to grow.

      But a new MIT study in Nature Microbiology today has found that Prochlorococcus relies on another carbon-feeding strategy, more than previously thought.

      Organisms that use a mix of strategies to provide carbon are known as mixotrophs. Most marine plankton are mixotrophs. And while Prochlorococcus is known to occasionally dabble in mixotrophy, scientists have assumed the microbe primarily lives a phototrophic lifestyle.

      The new MIT study shows that in fact, Prochlorococcus may be more of a mixotroph than it lets on. The microbe may get as much as one-third of its carbon through a second strategy: consuming the dissolved remains of other dead microbes.

      The new estimate may have implications for climate models, as the microbe is a significant force in capturing and “fixing” carbon in the Earth’s atmosphere and ocean.

      “If we wish to predict what will happen to carbon fixation in a different climate, or predict where Prochlorococcus will or will not live in the future, we probably won’t get it right if we’re missing a process that accounts for one-third of the population’s carbon supply,” says Mick Follows, a professor in MIT’s Department of Earth, Atmospheric and Planetary Sciences (EAPS), and its Department of Civil and Environmental Engineering.

      The study’s co-authors include first author and MIT postdoc Zhen Wu, along with collaborators from the University of Haifa, the Leibniz-Institute for Baltic Sea Research, the Leibniz-Institute of Freshwater Ecology and Inland Fisheries, and Potsdam University.

      Persistent plankton

      Since Prochlorococcus was first discovered in the Sargasso Sea in 1986, by MIT Institute Professor Sallie “Penny” Chisholm and others, the microbe has been observed throughout the world’s oceans, inhabiting the upper sunlit layers ranging from the surface down to about 160 meters. Within this range, light levels vary, and the microbe has evolved a number of ways to photosynthesize carbon in even low-lit regions.

      The organism has also evolved ways to consume organic compounds including glucose and certain amino acids, which could help the microbe survive for limited periods of time in dark ocean regions. But surviving on organic compounds alone is a bit like only eating junk food, and there is evidence that Prochlorococcus will die after a week in regions where photosynthesis is not an option.

      And yet, researchers including Daniel Sher of the University of Haifa, who is a co-author of the new study, have observed healthy populations of Prochlorococcus that persist deep in the sunlit zone, where the light intensity should be too low to maintain a population. This suggests that the microbes must be switching to a non-photosynthesizing, mixotrophic lifestyle in order to consume other organic sources of carbon.

      “It seems that at least some Prochlorococcus are using existing organic carbon in a mixotrophic way,” Follows says. “That stimulated the question: How much?”

      What light cannot explain

      In their new paper, Follows, Wu, Sher, and their colleagues looked to quantify the amount of carbon that Prochlorococcus is consuming through processes other than photosynthesis.

      The team looked first to measurements taken by Sher’s team, which previously took ocean samples at various depths in the Mediterranean Sea and measured the concentration of phytoplankton, including Prochlorococcus, along with the associated intensity of light and the concentration of nitrogen — an essential nutrient that is richly available in deeper layers of the ocean and that plankton can assimilate to make proteins.

      Wu and Follows used this data, and similar information from the Pacific Ocean, along with previous work from Chisholm’s lab, which established the rate of photosynthesis that Prochlorococcus could carry out in a given intensity of light.

      “We converted that light intensity profile into a potential growth rate — how fast the population of Prochlorococcus could grow if it was acquiring all it’s carbon by photosynthesis, and light is the limiting factor,” Follows explains.

      The team then compared this calculated rate to growth rates that were previously observed in the Pacific Ocean by several other research teams.

      “This data showed that, below a certain depth, there’s a lot of growth happening that photosynthesis simply cannot explain,” Follows says. “Some other process must be at work to make up the difference in carbon supply.”

      The researchers inferred that, in deeper, darker regions of the ocean, Prochlorococcus populations are able to survive and thrive by resorting to mixotrophy, including consuming organic carbon from detritus. Specifically, the microbe may be carrying out osmotrophy — a process by which an organism passively absorbs organic carbon molecules via osmosis.

      Judging by how fast the microbe is estimated to be growing below the sunlit zone, the team calculates that Prochlorococcus obtains up to one-third of its carbon diet through mixotrophic strategies.

      “It’s kind of like going from a specialist to a generalist lifestyle,” Follows says. “If I only eat pizza, then if I’m 20 miles from a pizza place, I’m in trouble, whereas if I eat burgers as well, I could go to the nearby McDonald’s. People had thought of Prochlorococcus as a specialist, where they do this one thing (photosynthesis) really well. But it turns out they may have more of a generalist lifestyle than we previously thought.”

      Chisholm, who has both literally and figuratively written the book on Prochlorococcus, says the group’s findings “expand the range of conditions under which their populations can not only survive, but also thrive. This study changes the way we think about the role of Prochlorococcus in the microbial food web.”

      This research was supported, in part, by the Israel Science Foundation, the U.S. National Science Foundation, and the Simons Foundation. More

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      in Environment

      Better living through multicellular life cycles

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      Cooperation is a core part of life for many organisms, ranging from microbes to complex multicellular life. It emerges when individuals share resources or partition a task in such a way that each derives a greater benefit when acting together than they could on their own. For example, birds and fish flock to evade predators, slime mold swarms to hunt for food and reproduce, and bacteria form biofilms to resist stress.

      Individuals must live in the same “neighborhood” to cooperate. For bacteria, this neighborhood can be as small as tens of microns. But in environments like the ocean, it’s rare for cells with the same genetic makeup to co-occur in the same neighborhood on their own. And this necessity poses a puzzle to scientists: In environments where survival hinges on cooperation, how do bacteria build their neighborhood?

      To study this problem, MIT professor Otto X. Cordero and colleagues took inspiration from nature: They developed a model system around a common coastal seawater bacterium that requires cooperation to eat sugars from brown algae. In the system, single cells were initially suspended in seawater too far away from other cells to cooperate. To share resources and grow, the cells had to find a mechanism of creating a neighborhood. “Surprisingly, each cell was able to divide and create its own neighborhood of clones by forming tightly packed clusters,” says Cordero, associate professor in the Department of Civil and Environmental Engineering.

      A new paper, published today in Current Biology, demonstrates how an algae-eating bacterium solves the engineering challenge of creating local cell density starting from a single-celled state.

      “A key discovery was the importance of phenotypic heterogeneity in supporting this surprising mechanism of clonal cooperation,” says Cordero, lead author of the new paper.

      Using a combination of microscopy, transcriptomics, and labeling experiments to profile a cellular metabolic state, the researchers found that cells phenotypically differentiate into a sticky “shell” population and a motile, carbon-storing “core.” The researchers propose that shell cells create the cellular neighborhood needed to sustain cooperation while core cells accumulate stores of carbon that support further clonal reproduction when the multicellular structure ruptures.

      This work addresses a key piece in the bigger challenge of understanding the bacterial processes that shape our earth, such as the cycling of carbon from dead organic matter back into food webs and the atmosphere. “Bacteria are fundamentally single cells, but often what they accomplish in nature is done through cooperation. We have much to uncover about what bacteria can accomplish together and how that differs from their capacity as individuals,” adds Cordero.

      Co-authors include Julia Schwartzman and Ali Ebrahimi, former postdocs in the Cordero Lab. Other co-authors are Gray Chadwick, a former graduate student at Caltech; Yuya Sato, a senior researcher at Japan’s National Institute of Advanced Industrial Science and Technology; Benjamin Roller, a current postdoc at the University of Vienna; and Victoria Orphan of Caltech.

      Funding was provided by the Simons Foundation. Individual authors received support from the Swiss National Science Foundation, Japan Society for the Promotion of Science, the U.S. National Science Foundation, the Kavli Institute of Theoretical Physics, and the National Institutes of Health. More