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    Better living through multicellular life cycles

    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

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    Could used beer yeast be the solution to heavy metal contamination in water?

    A new analysis by researchers at MIT’s Center for Bits and Atoms (CBA) has found that inactive yeast could be effective as an inexpensive, abundant, and simple material for removing lead contamination from drinking water supplies. The study shows that this approach can be efficient and economic, even down to part-per-billion levels of contamination. Serious damage to human health is known to occur even at these low levels.

    The method is so efficient that the team has calculated that waste yeast discarded from a single brewery in Boston would enough to treat the city’s entire water supply. Such a fully sustainable system would not only purify the water but also divert what would otherwise be a waste stream needing disposal.

    The findings are detailed today in the journal Nature Communications Earth and Environment, in a paper by MIT Research Scientist Patritsia Statathou; Brown University postdoc and MIT Visiting Scholar Christos Athanasiou; MIT Professor Neil Gershenfeld, the director of CBA; and nine others at MIT, Brown, Wellesley College, Nanyang Technological University, and National Technical University of Athens.

    Lead and other heavy metals in water are a significant global problem that continues to grow because of electronic waste and discharges from mining operations. In the U.S. alone, more than 12,000 miles of waterways are impacted by acidic mine-drainage-water rich in heavy metals, the country’s leading source of water pollution. And unlike organic pollutants, most of which can be eventually broken down, heavy metals don’t biodegrade, but persist indefinitely and bioaccumulate. They are either impossible or very expensive to completely remove by conventional methods such as chemical precipitation or membrane filtration.

    Lead is highly toxic, even at tiny concentrations, especially affecting children as they grow. The European Union has reduced its standard for allowable lead in drinking water from 10 parts per billion to 5 parts per billion. In the U.S., the Environmental Protection Agency has declared that no level at all in water supplies is safe. And average levels in bodies of surface water globally are 10 times higher than they were 50 years ago, ranging from 10 parts per billion in Europe to hundreds of parts per billion in South America.

    “We don’t just need to minimize the existence of lead; we need to eliminate it in drinking water,” says Stathatou. “And the fact is that the conventional treatment processes are not doing this effectively when the initial concentrations they have to remove are low, in the parts-per-billion scale and below. They either fail to completely remove these trace amounts, or in order to do so they consume a lot of energy and they produce toxic byproducts.”

    The solution studied by the MIT team is not a new one — a process called biosorption, in which inactive biological material is used to remove heavy metals from water, has been known for a few decades. But the process has been studied and characterized only at much higher concentrations, at more than one part-per-million levels. “Our study demonstrates that the process can indeed work efficiently at the much lower concentrations of typical real-world water supplies, and investigates in detail the mechanisms involved in the process,” Athanasiou says.

    The team studied the use of a type of yeast widely used in brewing and in industrial processes, called S. cerevisiae, on pure water spiked with trace amounts of lead. They demonstrated that a single gram of the inactive, dried yeast cells can remove up to 12 milligrams of lead in aqueous solutions with initial lead concentrations below 1 part per million. They also showed that the process is very rapid, taking less than five minutes to complete.

    Because the yeast cells used in the process are inactive and desiccated, they require no particular care, unlike other processes that rely on living biomass to perform such functions which require nutrients and sunlight to keep the materials active. What’s more, yeast is abundantly available already, as a waste product from beer brewing and from various other fermentation-based industrial processes.

    Stathatou has estimated that to clean a water supply for a city the size of Boston, which uses about 200 million gallons a day, would require about 20 tons of yeast per day, or about 7,000 tons per year. By comparison, one single brewery, the Boston Beer Company, generates 20,000 tons a year of surplus yeast that is no longer useful for fermentation.

    The researchers also performed a series of tests to determine that the yeast cells are responsible for biosorption. Athanasiou says that “exploring biosorption mechanisms at such challenging concentrations is a tough problem. We were the first to use a mechanics perspective to unravel biosorption mechanisms, and we discovered that the mechanical properties of the yeast cells change significantly after lead uptake. This provides fundamentally new insights for the process.”

    Devising a practical system for processing the water and retrieving the yeast, which could then be separated from the lead for reuse, is the next stage of the team’s research, they say.

    “To scale up the process and actually put it in place, you need to embed these cells in a kind of filter, and this is the work that’s currently ongoing,” Stathatou says. They are also looking at ways of recovering both the cells and the lead. “We need to conduct further experiments, but there is the option to get both back,” she says.

    The same material can potentially be used to remove other heavy metals, such as cadmium and copper, but that will require further research to quantify the effective rates for those processes, the researchers say.

    “This research revealed a very promising, inexpensive, and environmentally friendly solution for lead removal,” says Sivan Zamir, vice president of Xylem Innovation Labs, a water technology research firm, who was not associated with this research. “It also deepened our understanding of the biosorption process, paving the way for the development of materials tailored to removal of other heavy metals.”

    The team also included Marios Tsezos at the National Technical University of Athens, in Greece; John Gross at Wellesley College; Camron Blackburn, Filippos Tourlomousis, and Andreas Mershin at MIT’s CBA; Brian Sheldon, Nitin Padture, Eric Darling at Brown University; and Huajian Gao at Brown University and Nanyang Technological University, in Singapore. More

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    Microbes and minerals may have set off Earth’s oxygenation

    For the first 2 billion years of Earth’s history, there was barely any oxygen in the air. While some microbes were photosynthesizing by the latter part of this period, oxygen had not yet accumulated at levels that would impact the global biosphere.

    But somewhere around 2.3 billion years ago, this stable, low-oxygen equilibrium shifted, and oxygen began building up in the atmosphere, eventually reaching the life-sustaining levels we breathe today. This rapid infusion is known as the Great Oxygenation Event, or GOE. What triggered the event and pulled the planet out of its low-oxygen funk is one of the great mysteries of science.

    A new hypothesis, proposed by MIT scientists, suggests that oxygen finally started accumulating in the atmosphere thanks to interactions between certain marine microbes and minerals in ocean sediments. These interactions helped prevent oxygen from being consumed, setting off a self-amplifying process where more and more oxygen was made available to accumulate in the atmosphere.

    The scientists have laid out their hypothesis using mathematical and evolutionary analyses, showing that there were indeed microbes that existed before the GOE and evolved the ability to interact with sediment in the way that the researchers have proposed.

    Their study, appearing today in Nature Communications, is the first to connect the co-evolution of microbes and minerals to Earth’s oxygenation.

    “Probably the most important biogeochemical change in the history of the planet was oxygenation of the atmosphere,” says study author Daniel Rothman, professor of geophysics in MIT’s Department of Earth, Atmospheric, and Planetary Sciences (EAPS). “We show how the interactions of microbes, minerals, and the geochemical environment acted in concert to increase oxygen in the atmosphere.”

    The study’s co-authors include lead author Haitao Shang, a former MIT graduate student, and Gregory Fournier, associate professor of geobiology in EAPS.

    A step up

    Today’s oxygen levels in the atmosphere are a stable balance between processes that produce oxygen and those that consume it. Prior to the GOE, the atmosphere maintained a different kind of equilibrium, with producers and consumers of oxygen  in balance, but in a way that didn’t leave much extra oxygen for the atmosphere.

    What could have pushed the planet out of one stable, oxygen-deficient state to another stable, oxygen-rich state?

    “If you look at Earth’s history, it appears there were two jumps, where you went from a steady state of low oxygen to a steady state of much higher oxygen, once in the Paleoproterozoic, once in the Neoproterozoic,” Fournier notes. “These jumps couldn’t have been because of a gradual increase in excess oxygen. There had to have been some feedback loop that caused this step-change in stability.”

    He and his colleagues wondered whether such a positive feedback loop could have come from a process in the ocean that made some organic carbon unavailable to its consumers. Organic carbon is mainly consumed through oxidation, usually accompanied by the consumption of oxygen — a process by which microbes in the ocean use oxygen to break down organic matter, such as detritus that has settled in sediment. The team wondered: Could there have been some process by which the presence of oxygen stimulated its further accumulation?

    Shang and Rothman worked out a mathematical model that made the following prediction: If microbes possessed the ability to only partially oxidize organic matter, the partially-oxidized matter, or “POOM,” would effectively become “sticky,” and chemically bind to minerals in sediment in a way that would protect the material from further oxidation. The oxygen that would otherwise have been consumed to fully degrade the material would instead be free to build up in the atmosphere. This process, they found, could serve as a positive feedback, providing a natural pump to push the atmosphere into a new, high-oxygen equilibrium.

    “That led us to ask, is there a microbial metabolism out there that produced POOM?” Fourier says.

    In the genes

    To answer this, the team searched through the scientific literature and identified a group of microbes that partially oxidizes organic matter in the deep ocean today. These microbes belong to the bacterial group SAR202, and their partial oxidation is carried out through an enzyme, Baeyer-Villiger monooxygenase, or BVMO.

    The team carried out a phylogenetic analysis to see how far back the microbe, and the gene for the enzyme, could be traced. They found that the bacteria did indeed have ancestors dating back before the GOE, and that the gene for the enzyme could be traced across various microbial species, as far back as pre-GOE times.

    What’s more, they found that the gene’s diversification, or the number of species that acquired the gene, increased significantly during times when the atmosphere experienced spikes in oxygenation, including once during the GOE’s Paleoproterozoic, and again in the Neoproterozoic.

    “We found some temporal correlations between diversification of POOM-producing genes, and the oxygen levels in the atmosphere,” Shang says. “That supports our overall theory.”

    To confirm this hypothesis will require far more follow-up, from experiments in the lab to surveys in the field, and everything in between. With their new study, the team has introduced a new suspect in the age-old case of what oxygenated Earth’s atmosphere.

    “Proposing a novel method, and showing evidence for its plausibility, is the first but important step,” Fournier says. “We’ve identified this as a theory worthy of study.”

    This work was supported in part by the mTerra Catalyst Fund and the National Science Foundation. More

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    Predator interactions chiefly determine where Prochlorococcus thrive

    Prochlorococcus are the smallest and most abundant photosynthesizing organisms on the planet. A single Prochlorococcus cell is dwarfed by a human red blood cell, yet globally the microbes number in the octillions and are responsible for a large fraction of the world’s oxygen production as they turn sunlight into energy.

    Prochlorococcus can be found in the ocean’s warm surface waters, and their population drops off dramatically in regions closer to the poles. Scientists have assumed that, as with many marine species, Prochlorococcus’ range is set by temperature: The colder the waters, the less likely the microbes are to live there.

    But MIT scientists have found that where the microbe lives is not determined primarily by temperature. While Prochlorococcus populations do drop off in colder waters, it’s a relationship with a shared predator, and not temperature, that sets the microbe’s range. These findings, published today in the Proceedings of the National Academy of Sciences, could help scientists predict how the microbes’ populations will shift with climate change.

    “People assume that if the ocean warms up, Prochlorococcus will move poleward. And that may be true, but not for the reason they’re predicting,” says study co-author Stephanie Dutkiewicz, senior research scientist in MIT’s Department of Earth, Atmospheric and Planetary Sciences (EAPS). “So, temperature is a bit of a red herring.”

    Dutkiewicz’s co-authors on the study are lead author and EAPS Research Scientist Christopher Follett, EAPS Professor Mick Follows, François Ribalet and Virginia Armbrust of the University of Washington, and Emily Zakem and David Caron of the University of Southern California at Los Angeles.

    Temperature’s collapse

    While temperature is thought to set the range of Prochloroccus and other phytoplankton in the ocean, Follett, Dutkiewicz, and their colleagues noticed a curious dissonance in data.

    The team examined observations from several research cruises that sailed through the northeast Pacific Ocean in 2003, 2016, and 2017. Each vessel traversed different latitudes, sampling waters continuously and measuring concentrations of various species of bacteria and phytoplankton, including Prochlorococcus. 

    The MIT team used the publicly archived cruise data to map out the locations where Prochlorococcus noticeably decreased or collapsed, along with each location’s ocean temperature. Surprisingly, they found that Prochlorococcus’ collapse occurred in regions of widely varying temperatures, ranging from around 13 to 18 degrees Celsius. Curiously, the upper end of this range has been shown in lab experiments to be suitable conditions for Prochlorococcus to grow and thrive.

    “Temperature itself was not able to explain where we saw these drop-offs,” Follett says.

    Follett was also working out an alternate idea related to Prochlorococcus and nutrient supply. As a byproduct of its photosynthesis, the microbe produces carbohydrate — an essential nutrient for heterotrophic bacteria, which are single-celled organisms that do not photosynthesize but live off the organic matter produced by phytoplankton.

    “Somewhere along the way, I wondered, what would happen if this food source Prochlorococcus was producing increased? What if we took that knob and spun it?” Follett says.

    In other words, how would the balance of Prochlorococcus and bacteria shift if the bacteria’s food increased as a result of, say, an increase in other carbohydrate-producing phytoplankton? The team also wondered: If the bacteria in question were about the same size as Prochlorococcus, the two would likely share a common grazer, or predator. How would the grazer’s population also shift with a change in carbohydrate supply?

    “Then we went to the whiteboard and started writing down equations and solving them for various cases, and realized that as soon as you reach an environment where other species add carbohydrates to the mix, bacteria and grazers grow up and annihilate Prochlorococcus,” Dutkiewicz says.

    Nutrient shift

    To test this idea, the researchers employed simulations of ocean circulation and marine ecosystem interactions. The team ran the MITgcm, a general circulation model that simulates, in this case, the ocean currents and regions of upwelling waters around the world. They overlaid a biogeochemistry model that simulates how nutrients are redistributed in the ocean. To all of this, they linked a complex ecosystem model that simulates the interactions between many different species of bacteria and phytoplankton, including Prochlorococcus.

    When they ran the simulations without incorporating a representation of bacteria, they found that Prochlorococcus persisted all the way to the poles, contrary to theory and observations. When they added in the equations outlining the relationship between the microbe, bacteria, and a shared predator, Prochlorococcus’ range shifted away from the poles, matching the observations of the original research cruises.

    In particular, the team observed that Prochlorococcus thrived in waters with very low nutrient levels, and where it is the dominant source of food for bacteria. These waters also happen to be warm, and Prochlorococcus and bacteria live in balance, along with their shared predator. But in more nutrient-rich enviroments, such as polar regions, where cold water and nutrients are upwelled from the deep ocean, many more species of phytoplankton can thrive. Bacteria can then feast and grow on more food sources, and in turn feed and grow more of its shared predator. Prochlorococcus, unable to keep up, is quickly decimated. 

    The results show that a relationship with a shared predator, and not temperature, sets Prochlorococcus’ range. Incorporating this mechanism into models will be crucial in predicting how the microbe — and possibly other marine species — will shift with climate change.

    “Prochlorococcus is a big harbinger of changes in the global ocean,” Dutkiewicz says. “If its range expands, that’s a canary — a sign that things have changed in the ocean by a great deal.”

    “There are reasons to believe its range will expand with a warming world,” Follett adds.” But we have to understand the physical mechanisms that set these ranges. And predictions just based on temperature will not be correct.” More

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    Zeroing in on the origins of Earth’s “single most important evolutionary innovation”

    Some time in Earth’s early history, the planet took a turn toward habitability when a group of enterprising microbes known as cyanobacteria evolved oxygenic photosynthesis — the ability to turn light and water into energy, releasing oxygen in the process.

    This evolutionary moment made it possible for oxygen to eventually accumulate in the atmosphere and oceans, setting off a domino effect of diversification and shaping the uniquely habitable planet we know today.  

    Now, MIT scientists have a precise estimate for when cyanobacteria, and oxygenic photosynthesis, first originated. Their results appear today in the Proceedings of the Royal Society B.

    They developed a new gene-analyzing technique that shows that all the species of cyanobacteria living today can be traced back to a common ancestor that evolved around 2.9 billion years ago. They also found that the ancestors of cyanobacteria branched off from other bacteria around 3.4 billion years ago, with oxygenic photosynthesis likely evolving during the intervening half-billion years, during the Archean Eon.

    Interestingly, this estimate places the appearance of oxygenic photosynthesis at least 400 million years before the Great Oxidation Event, a period in which the Earth’s atmosphere and oceans first experienced a rise in oxygen. This suggests that cyanobacteria may have evolved the ability to produce oxygen early on, but that it took a while for this oxygen to really take hold in the environment.

    “In evolution, things always start small,” says lead author Greg Fournier, associate professor of geobiology in MIT’s Department of Earth, Atmospheric and Planetary Sciences. “Even though there’s evidence for early oxygenic photosynthesis — which is the single most important and really amazing evolutionary innovation on Earth — it still took hundreds of millions of years for it to take off.”

    Fournier’s MIT co-authors include Kelsey Moore, Luiz Thiberio Rangel, Jack Payette, Lily Momper, and Tanja Bosak.

    Slow fuse, or wildfire?

    Estimates for the origin of oxygenic photosynthesis vary widely, along with the methods to trace its evolution.

    For instance, scientists can use geochemical tools to look for traces of oxidized elements in ancient rocks. These methods have found hints that oxygen was present as early as 3.5 billion years ago — a sign that oxygenic photosynthesis may have been the source, although other sources are also possible.

    Researchers have also used molecular clock dating, which uses the genetic sequences of microbes today to trace back changes in genes through evolutionary history. Based on these sequences, researchers then use models to estimate the rate at which genetic changes occur, to trace when groups of organisms first evolved. But molecular clock dating is limited by the quality of ancient fossils, and the chosen rate model, which can produce different age estimates, depending on the rate that is assumed.

    Fournier says different age estimates can imply conflicting evolutionary narratives. For instance, some analyses suggest oxygenic photosynthesis evolved very early on and progressed “like a slow fuse,” while others indicate it appeared much later and then “took off like wildfire” to trigger the Great Oxidation Event and the accumulation of oxygen in the biosphere.

    “In order for us to understand the history of habitability on Earth, it’s important for us to distinguish between these hypotheses,” he says.

    Horizontal genes

    To precisely date the origin of cyanobacteria and oxygenic photosynthesis, Fournier and his colleagues paired molecular clock dating with horizontal gene transfer — an independent method that doesn’t rely entirely on fossils or rate assumptions.

    Normally, an organism inherits a gene “vertically,” when it is passed down from the organism’s parent. In rare instances, a gene can also jump from one species to another, distantly related species. For instance, one cell may eat another, and in the process incorporate some new genes into its genome.

    When such a horizontal gene transfer history is found, it’s clear that the group of organisms that acquired the gene is evolutionarily younger than the group from which the gene originated. Fournier reasoned that such instances could be used to determine the relative ages between certain bacterial groups. The ages for these groups could then be compared with the ages that various molecular clock models predict. The model that comes closest would likely be the most accurate, and could then be used to precisely estimate the age of other bacterial species — specifically, cyanobacteria.

    Following this reasoning, the team looked for instances of horizontal gene transfer across the genomes of thousands of bacterial species, including cyanobacteria. They also used new cultures of modern cyanobacteria taken by Bosak and Moore, to more precisely use fossil cyanobacteria as calibrations. In the end, they identified 34 clear instances of horizontal gene transfer. They then found that one out of six molecular clock models consistently matched the relative ages identified in the team’s horizontal gene transfer analysis.

    Fournier ran this model to estimate the age of the “crown” group of cyanobacteria, which encompasses all the species living today and known to exhibit oxygenic photosynthesis. They found that, during the Archean eon, the crown group originated around 2.9 billion years ago, while cyanobacteria as a whole branched off from other bacteria around 3.4 billion years ago. This strongly suggests that oxygenic photosynthesis was already happening 500 million years before the Great Oxidation Event (GOE), and that cyanobacteria were producing oxygen for quite a long time before it accumulated in the atmosphere.

    The analysis also revealed that, shortly before the GOE, around 2.4 billion years ago, cyanobacteria experienced a burst of diversification. This implies that a rapid expansion of cyanobacteria may have tipped the Earth into the GOE and launched oxygen into the atmosphere.

    Fournier plans to apply horizontal gene transfer beyond cyanobacteria to pin down the origins of other elusive species.

    “This work shows that molecular clocks incorporating horizontal gene transfers (HGTs) promise to reliably provide the ages of groups across the entire tree of life, even for ancient microbes that have left no fossil record … something that was previously impossible,” Fournier says. 

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