To paraphrase Mark Twain, reports of declining phytoplankton in the North Atlantic may have been greatly exaggerated. A prominent 2019 study used ice cores in Antarctica to suggest that during the industrial era, with worrying implications that the trend might continue.

But new research led by the 91±ŹÁÏ shows that marine phytoplankton — on which larger organisms throughout the marine ecosystem depend — may be more stable than believed in the North Atlantic. The team’s analysis of an ice core going back 800 years shows that a more complex atmospheric process may explain the recent trends.

The was published the week of Nov. 13 in the Proceedings of the National Academy of Sciences.

Tiny floating photosynthetic organisms known as phytoplankton form the base of the marine ecosystem. These microscopic creatures are also important to the planet as a whole, producing roughly half the oxygen in Earth’s atmosphere.

Since phytoplankton are hard to count, scientists attempt to measure their abundance in other ways. Phytoplankton emit dimethyl sulfide, an odorous gas that gives beaches their distinctive smell. Once airborne, the dimethyl sulfide converts to methanesulfonic acid, or MSA, and sulfate. These eventually fall out onto land or snow, making ice cores one way to measure past population sizes.

“Greenland ice cores show a decline in MSA concentrations over the industrial era, which was concluded to be a sign of declining primary productivity in the North Atlantic,” said lead author , a 91±ŹÁÏ doctoral student in atmospheric sciences. “But our study of sulfate in a Greenland ice core shows that MSA alone can’t tell us the whole story when it comes to primary productivity.”

Since the mid-1800s, factories and tailpipes have also been spewing sulfur-containing gases into the air. Those gases have slightly different forms of sulfur atoms that make it possible to distinguish the marine and land-based sources in ice cores.

The new study goes further back than the previous study by measuring several sulfur-containing molecules in an ice core from central Greenland with layers spanning the years 1200 to 2006. The authors show that human-generated pollutants changed the atmosphere’s chemistry. This, in turn, altered the fate of the gases emitted by phytoplankton.

“When looking at the ice cores, we found that sulfate derived from phytoplankton increased during the industrial era,” Jongebloed said. “In other words, the decline in MSA is ‘offset’ by the simultaneous increase in phytoplankton-derived sulfate, indicating that phytoplankton-derived sulfur emissions have remained stable overall.”

When that balance is included in the calculations, the phytoplankton populations seem fairly stable since the mid-1800s. The researchers caution, however, that marine ecosystems remain under threat from many directions.

“Measuring both MSA and phytoplankton-derived sulfate gives us a fuller picture of how the emissions from marine primary producers have changed — or not changed — over time,” said senior author , a 91±ŹÁÏ professor of atmospheric sciences.

“Ice core measurements along with other independent estimates of phytoplankton abundance (such as chlorophyll measurements) and paired with modeling studies (which help us estimate how atmospheric chemistry and climate change over time) can help us understand how marine productivity has changed in the past and how productivity might change in the future.”

Other co-authors are research scientist , doctoral student and former undergraduates and at the 91±ŹÁÏ; Jihong Cole-Dai and Carleigh Larrick at South Dakota State University; William Porter and Linia Tashmim at the University of California, Riverside; and Lei Geng at the University of Science and Technology of China.

The study was funded by the National Science Foundation and the National Natural Science Foundation of China.

For more information, contact Jongebloed at ujongebl@uw.edu or Alexander at beckya@uw.edu.

In the frigid waters surrounding Antarctica, an unusual seasonal cycle occurs. During winter, from March to October, the sun barely rises. As seawater freezes it rejects salts, creating pockets of extra-salty brine where microbes live in winter. In summer, the sea ice melts under constant daylight, producing warmer, fresher water at the surface.

This remote ecosystem is home to much of the Southern Ocean’s photosynthetic life. A new 91±ŹÁÏ study provides the first measurements of how sea-ice algae and other single-celled life adjust to these seasonal rhythms, offering clues to what might happen as this environment shifts under climate change.

The , published Sept. 15 in the International Society for Microbial Ecology’s ISME Journal, contains some of the first measurements of how sea-ice microbes respond to changing conditions.

“We know very little about how sea-ice microbes respond to changes in salinity and temperature,” said lead author , a 91±ŹÁÏ postdoctoral researcher who did the work while pursuing her doctorate in oceanography at the 91±ŹÁÏ. “And until now we knew almost nothing about the molecules they produce and use in chemical reactions to stay alive, which are important for supporting higher organisms in the ecosystem as well as for climate impacts, like carbon storage and cloud formation.”

The polar oceans play an important role in global ocean currents and in supporting marine ecosystems. Microbes form the base of the food web, supporting larger life forms.

“Polar oceans make up a significant portion of the world’s oceans, and these are very productive waters,” said senior author , a 91±ŹÁÏ assistant professor of oceanography. “These waters support big swarms of krill, the whales that come to feed on those krill, and either polar bears or penguins. And the start of that whole ecosystem are these single-celled microscopic algae. We just know so little about them.”

The tiny organisms are also important for the climate, since they quietly perform photosynthesis and soak up carbon from the atmosphere. Polar algae are especially good at producing sulfur-containing molecules that give beaches their distinctive smell and, when lofted into the air in sea spray, promote formation of clouds that can reduce penetration of solar rays.

Antarctic sea ice, though long stable, is at an this year.

In other oceans, satellite instruments can capture dramatic seasonal phytoplankton blooms from space — but that isn’t possible for microbes hidden under sea ice. And Antarctic waters are particularly challenging to visit, leaving researchers with almost no measurements in winter.

In late 2018, Dawson and co-author traveled to , a U.S. research station on the West Antarctic Peninsula. They used a small boat to sample seawater and sea ice at the same nearby sites every three days.

Back on shore, the two graduate students performed 10-day experiments in tanks to see which microbes grew as temperature and salinity were adjusted to mimic sea-ice formation and melt. They also shipped samples back to Seattle for more complex measurements of the samples’ genetics and metabolites, the small organic molecules produced by the cell.

Results revealed how single-celled algae deal with their fluctuating environments. As temperatures drop, the cells produce cryoprotectants, similar to antifreeze, to prevent their cellular fluid from crystallizing. Many of the most common cryoprotectant molecules were the same across different microbial lifeforms.

As salinity changes, to avoid either bursting in freshening waters or becoming desiccated like raisins in salty conditions, the cells change the concentration of salt-like organic molecules. Many such molecules serve a dual role as cryoprotectants, to balance conditions inside and outside the cell to maintain water balance.

The results show that under short-term temperature and salinity changes, community structure in each sample remained stable while adjusting the production of protective molecules. Different microbe species showed consistent responses to changing conditions. This should simplify modeling future responses to climate change, Young said.

Results also hint that the production of omega-3 fatty acids may decline in lower-salinity environments. This would be bad news for consumers of krill oil supplements, and for the marine ecosystem that relies on those algae-derived nutrients. Future research now underway by the 91±ŹÁÏ group aims to confirm that result — especially with the prospect of increasing freshwater input from melting sea ice and glaciers.

“We’re interested in how these sea-ice algae contend with changes in temperature, salinity and light under normal conditions,” Dawson said. “But then we also have climate change, which is completely remodeling the landscape in terms of when sea ice is forming, how much sea ice forms, how long it stays before it melts, as well as the quantity of freshwater input from glaciers. So we’re both trying to capture what’s happening now, and also asking how that can inform what might happen in the future.”

The study was funded by the National Science Foundation, the Simons Foundation, and the Alfred P. Sloan Foundation. Other co-authors are Anitra Ingalls, Jody Deming, Joshua Sacks and Laura Carlson at the 91±ŹÁÏ; Natalia Erazo, Elizabeth Connors and Jeff Bowman at Scripps Institution of Oceanography; and Veronica Mierzejewski at Arizona State University.

For more information, contact Dawson at hmdawson@uw.edu or Young at youngjn@uw.edu.

Single-celled organisms in the open ocean use a diverse array of genetic tools to detect light, even in tiny amounts, and respond, according to a study published the week of Feb. 1 in the Proceedings of the National Academy of Sciences.

“If you look in the ocean environment, all these different organisms have this day-night cycle. They are very in tune with each other, even as they get moved around. How do they know when it’s day? How do they know when it’s night?” said lead author , a research scientist in oceanography at the 91±ŹÁÏ.

Though invisible to the human eye, ocean microbes support all marine life, from sardines to whales. Knowing these communities’ inner workings could reveal how they will fare under changing ocean conditions.

“Just like rainforests generate oxygen and take up carbon dioxide, ocean organisms do the same thing in the world’s oceans. People probably don’t realize this, but these unicellular organisms are about as important as rainforests for our planet’s functioning,” Coesel said.

By analyzing RNA filtered out of seawater samples collected throughout the day and night, the study identifies four main groups of photoreceptors, many of them new. This genetic activity uses light to trigger changes in the metabolism, growth, cell division, movements and death of marine organisms.

The discovery of these new genetic “light switches” could also aid in the field of , in which a cell’s function can be controlled with light exposure. Today’s optogenetic tools are engineered by humans, but versions from nature might be more sensitive or better detect light of particular wavelengths, the researchers said.

“This work dramatically expanded the number of photoreceptors — the different kinds of those on-off switches — that we know of,” said senior author , a 91±ŹÁÏ professor of oceanography.

Not surprisingly, many of the new tools were for light in the blue range, since water filters out red wavelengths (which is why oceans appear blue). Some were also for green light, Coesel said.

The researchers collected water samples far from shore and looked at all genetic activity from protists: single-celled organisms with a nucleus. They filtered the water to select organisms measuring between 200 nanometers to one-tenth of a millimeter across. These included photosynthetic organisms, like algae, which absorb light for energy, as well as other single-celled plankton that gain energy by consuming other organisms.

The team collected samples every four hours, day and night, for four days in the North Pacific near Hawaii. Researchers used trackers to follow the currents about 15 meters (50 feet) below the surface so that the samples came from the same water mass.

The study also looked at samples that came from a depth of 120 and 150 meters (400 and 500 feet), in the ocean’s “twilight zone.” Even there, the genetic activity showed that the organisms were responding to very low levels of sunlight.

While the sun is up, these organisms gain energy and grow in size, and at night, when the ultraviolet light is less damaging to their DNA, they undergo cell division.

“Daylight is important for ocean organisms, we know that, we take it for granted. But to see the rhythm of genetic activity during these four days, and the beautiful synchronicity, you realize just how powerful light is,” Armbrust said.

Future work will look at places farther from the equator, where plankton communities are more subjected to the changing seasons.

This research was funded by the Simons Foundation and the National Science Foundation’s Extreme Science and Engineering Discovery Environment program. Other co-authors are Ryan Groussman, Rhonda Morales and François Ribalet at the 91±ŹÁÏ; Bryndan Durham at the University of Florida; Sarah Hu at Woods Hole Oceanographic Institution; and David Caron at the University of Southern California.

For more information, contact Coesel at coesel@uw.edu or Armbrust at armbrust@uw.edu.

The most common organism in the oceans, and possibly on the entire planet, is a family of single-celled marine bacteria called SAR11. These drifting organisms look like tiny jelly beans and have evolved to outcompete other bacteria for scarce resources in the oceans.

We now know that this group of organisms thrives despite — or perhaps because of — the ability to host viruses in their DNA. A published in May in Nature Microbiology could lead to new understanding of viral survival strategies.

91±ŹÁÏ oceanographers discovered that the bacteria that dominate seawater, known as Pelagibacter or SAR11, hosts a unique virus. The virus is of a type that spends most of its time dormant in the host’s DNA but occasionally erupts to infect other cells, potentially carrying some of its host’s genetic material along with it.

“Many bacteria have viruses that exist in their genomes. But people had not found them in the ocean’s most abundant organisms,” said co-lead author , a 91±ŹÁÏ associate professor of oceanography. “We suspect it’s probably common, or more common than we thought — we just had never seen it.”

This virus’ two-pronged survival strategy differs from similar ones found in other organisms. The virus lurks in the host’s DNA and gets copied as cells divide, but for reasons still poorly understood, it also replicates and is released from other cells.

The new study shows that as many as 3% of the SAR11 cells can have the virus multiply and split, or lyse, the cell — a much higher percentage than for most viruses that inhabit a host’s genome. This produces a large number of free viruses and could be key to its survival.

“There are 10 times more viruses in the ocean than there are bacteria,” Morris said. “Understanding how those large numbers are maintained is important. How does a virus survive? If you kill your host, how do you find another host before you degrade?”

The study could prompt basic research that could help clarify host–virus interactions in other settings.

“If you study a system in bacteria, that is easier to manipulate, then you can sort out the basic mechanisms,” Morris said. “It’s not too much of a stretch to say it could eventually help in biomedical applications.”

The 91±ŹÁÏ oceanography group had published a previous paper in 2019 looking at how marine phytoplankton, including SAR11, use sulfur. That allowed the researchers to cultivate two new strains of the ocean-dwelling organism and analyze one strain, NP1, with the latest genetic techniques.

Co-lead author collected samples off the coast of Oregon during a research cruise. She diluted the seawater several times and then used a sulfur-containing substance to grow the samples in the lab — a difficult process, for organisms that prefer to exist in seawater.

The team then sequenced this strain’s DNA at the in Seattle.

“In the past we got a full genome, first try,” Morris said. “This one didn’t do that, and it was confusing because it’s a very small genome.”

The researchers found that a virus was complicating the task of sequencing the genome. Then they discovered a virus wasn’t just in that single strain.

“When we went to grow the NP2 control culture, lo and behold, there was another virus. It was surprising how you couldn’t get away from a virus,” said Cain, who graduated in 2019 with a 91±ŹÁÏ bachelor’s in oceanography and now works in a 91±ŹÁÏ research lab.

Cain’s experiments showed that the virus’ switch to replicating and bursting cells is more active when the cells are deprived of nutrients, lysing up to 30% of the host cells. The authors believe that bacterial genes that hitch a ride with the viruses could help other SAR11 maintain their competitive advantage in nutrient-poor conditions.

“We want to understand how that has contributed to the evolution and ecology of life in the oceans,” Morris said.

Co-authors are postdoctoral researcher and associate professor in the 91±ŹÁÏ Department of Biochemistry. The study was funded by the National Science Foundation and the National Institutes of Health’s National Institute of Allergy and Infectious Disease.

For more information, contact Morris at morrisrm@uw.edu or 206-221-7228 and Cain at kcain97@uw.edu.

A by 91±ŹÁÏ oceanographers, published this summer in Nature Microbiology, looks at how photosynthetic microbes and ocean bacteria use sulfur, a plentiful marine nutrient.

Sulfur is the odorous element that gives beaches their distinctive smell. The new study focused on sulfonates, in which a sulfur atom is connected to three oxygen atoms and a carbon-based molecule. In the ocean, phytoplankton use energy from the sun to create sulfonate molecules. Bacteria then consume the sulfonates to gain nutrients and energy.

, then a 91±ŹÁÏ postdoctoral researcher in oceanography and now an assistant professor at the University of Florida, drew on recent genetic studies of soils to learn which microbial pathways are used to process sulfonates in the ocean. The study first focused on 36 marine microbes that the team cultured in the lab, using a 91±ŹÁÏ-developed method to test which organisms produce sulfonates on their own in a lab environment.

The study discovered “some striking similarities between sulfonate pathways in terrestrial and ocean systems,” Durham wrote in a in Nature Microbiology that discusses the project. In soils, plants typically produce sulfonates. In the oceans most sulfonates are also produced by photosynthetic organisms, in this case by unicellular phytoplankton.

The study then considered microbes in the open ocean that cannot yet be bred in the lab. During a 2015 north of Hawaii co-led by a team of researchers including and , both professors of oceanography and senior authors on the new study, microbial samples were collected at different times of day and night. The researchers then froze the samples in order to analyze their genetic and chemical contents back in Seattle.

“We returned from sea with a freezer’s worth of samples that generated over six terabytes of data for us to explore,” Durham wrote, “a major computational hurdle.”

The team eventually succeeded in extracting the relevant data and found patterns that backed up the findings from the lab samples. They also detected a day–night rhythm in sulfonate metabolism that reflects the activity of photosynthetic organisms.

“Sulfonates are produced and consumed by certain groups of microbes, so we can use them to track specific relationships in seawater communities,” Durham said. “And because sulfonates contain a carbon–sulfur bond, they are part of the global carbon cycle which controls the flux of carbon dioxide into and out of the ocean. This is increasingly important to understand as the climate changes.”

Other co-authors are Angela Boysen, Laura Carlson, Ryan Groussman, Katherine Heal, Kelsy Cain, Rhonda Morales, Sacha Coesel and Robert Morris, all at the 91±ŹÁÏ. This research was funded by the National Science Foundation, the Simons Foundation and the Gordon and Betty Moore Foundation.

For more information, contact Durham at b.durham@ufl.edu, Armbrust at armbrust@uw.edu, or Ingalls at aingalls@uw.edu.

“Thinking of arsenic as not just a bad guy, but also as beneficial, has reshaped the way that I view the element,” said first author , who did the research for her doctoral thesis at the 91±ŹÁÏ and is now a postdoctoral fellow at the Woods Hole Oceanographic Institution and the Massachusetts Institute of Technology.

The was published this week in the .

“We’ve known for a long time that there are very low levels of arsenic in the ocean,” said co-author , a 91±ŹÁÏ professor of oceanography. “But the idea that organisms could be using arsenic to make a living — it’s a whole new metabolism for the open ocean.”

The researchers analyzed seawater samples from a region below the surface where oxygen is almost absent, forcing life to seek other strategies. These regions may expand under climate change.

“In some parts of the ocean there’s a sandwich of water where there’s no measurable oxygen,” Rocap said. “The microbes in these regions have to use other elements that act as an electron acceptor to extract energy from food.”

The most common alternatives to oxygen are nitrogen or sulfur. But Saunders’ early investigations suggested arsenic could also work, spurring her to look for the evidence.

The team analyzed samples collected during a 2012 research cruise to the tropical Pacific, off the coast of Mexico. Genetic analyses on DNA extracted from the seawater found two genetic pathways known to convert arsenic-based molecules as a way to gain energy. The genetic material was targeting two different forms of arsenic, and authors believe that the pathways occur in two organisms that cycle arsenic back and forth between different forms.

Results suggest that arsenic-breathing microbes make up less than 1% of the microbe population in these waters. The microbes discovered in the water are probably distantly related to the arsenic-breathing microbes found in hot springs or contaminated sites on land.

“What I think is the coolest thing about these arsenic-respiring microbes existing today in the ocean is that they are expressing the genes for it in an environment that is fairly low in arsenic,” Saunders said. “It opens up the boundaries for where we could look for organisms that are respiring arsenic, in other arsenic-poor environments.”

Biologists believe the strategy is a holdover from Earth’s early history. During the period when life arose on Earth, oxygen was scarce in both the air and in the ocean. Oxygen became abundant in Earth’s atmosphere only after photosynthesis became widespread and converted carbon dioxide gas into oxygen.

Early lifeforms had to gain energy using other elements, such as arsenic, which was likely more common in the oceans at that time.

“We found the genetic signatures of pathways that are still there, remnants of the past ocean that have been maintained until today,” Saunders said.

Arsenic-breathing populations may grow again under climate change. Low-oxygen regions are projected to expand, and dissolved oxygen is predicted to drop throughout the marine environment.

“For me, it just shows how much is still out there in the ocean that we don’t know,” Rocap said.

Saunders recently collected more water samples from the same region and is now trying to grow the arsenic-breathing marine microbes in a lab in order to study them more closely.

“Right now we’ve got bits and pieces of their genomes, just enough to say that yes, they’re doing this arsenic transformation,” Rocap said. “The next step would be to put together a whole genome and find out what else they can do, and how that organism fits into the environment.”

Co-author collected the samples and led the DNA sequencing effort as a 91±ŹÁÏ postdoctoral research scientist and now holds a faculty position at the University of Maryland. The other co-author is , a research scientist in the 91±ŹÁÏ School of Oceanography. The study was funded by a graduate fellowship from NASA and a research grant from the National Science Foundation.

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For more information, contact Saunders at jaci@whoi.edu or Rocap at 206-685-9994 or rocap@uw.edu.

When it comes to the well-being of coral reefs, for many years scientists focused on , an event that can endanger corals and the diverse marine ecosystems that they support. In bleaching, high temperatures or other stressors cause corals to expel Symbiodinium, the beneficial, brightly colored microbes that would normally share excess energy and nutrients with corals. Bleaching ultimately starves corals and endangers the entire reef ecosystem.

But over the last two decades, scientists have realized that other microbes are also critical for coral health, including communities of bacteria that live on coral surfaces and in their tissues. These bacteria constitute the coral microbiome. High temperatures — even below the threshold for bleaching — can coral microbiomes, leaving corals .

But scientists lack comprehensive data about the bacteria that make up the microbiomes of the more than 1,500 coral species worldwide. That is starting to change thanks to the , a collaboration among researchers at the 91±ŹÁÏ Bothell, Pennsylvania State University and Oregon State University. The team is studying the diversity of bacteria within corals and how it has changed over time.

In their first comprehensive survey of healthy corals, Nov. 22 in the journal , the team reports that coral bacteria are a surprisingly diverse bunch — and that different sections of the coral body can host unique communities of bacteria.

“This project represents one of the most comprehensive efforts to identify what kinds of bacteria are present in diverse groups of tropical corals, how the types of bacteria can differ over coral anatomy, and how the symbiotic relationships between corals and bacteria have changed over coral evolution,” said senior and corresponding author , an assistant professor of biological sciences at 91±ŹÁÏ Bothell.

Their findings reveal what a relatively healthy coral microbiome looks like in a variety of coral species, and how coral microbiomes have formed and evolved. Understanding the microbiome may even help predict which corals will survive heat waves or disease outbreaks.

“Just like the bacteria within our gut help us digest food and protect us from pathogens, the normal bacteria associated with corals can also help them process nutrients and help protect them against disease,” said Zaneveld.

The team partnered with scientists at James Cook University and the Australian Institute of Marine Science to collect 691 small tissue samples from 236 different healthy corals along the Great Barrier Reef. The researchers took samples from up to three different tissues in each coral: the hard skeleton of calcium carbonite, the soft inner tissue and the outer mucus layer. The corals sampled included diverse species that have, in some cases, been evolving separately for tens of millions of years.

The researchers sequenced sections of DNA from bacteria in those tissue samples, which they used to identify the types of bacteria in healthy microbiomes for each coral species and tissue. They discovered that the mucus, skeleton and soft tissue all contain distinct microbial communities — and that the richness and diversity of bacterial species present differed greatly by tissue type. In general, the skeleton contained the greatest diversity of bacteria, a finding which surprised the team. They had been expecting the mucus, which coats the coral and forms a barrier between itself and the environment, to harbor the most diverse microbiome. Instead, the mucus microbiome was often the least diverse.

The team also discovered that coral species differed the most in the composition of their tissue microbiomes. While mucus microbiomes also differed by coral species, they were also strongly influenced by environmental factors such as location, temperature and depth. The major differences between coral species raised questions about the age of these associations between corals and their microbes, and how they have changed over time.

The researchers found that distantly related corals were more likely to have highly different microbiomes. Corals that were more closely related typically had similar microbiomes. This pattern, known as , was strongest for the microbiomes from inside the corals’ stony skeletons. Though the team discovered that many coral-bacteria associations are likely recent, at least four types of bacteria evolved together with certain groups of corals over millions of years.

Now the researchers hope to gather additional data on healthy coral microbiomes to learn why some species have strikingly different types of microbiomes and to investigate how tissues in the same coral establish and maintain different microbiomes.

“We want to understand what roles that different factors — such as the coral’s immune system or its environment — play in shaping the microbiome,” said Zaneveld. “These answers could help us understand how the microbiome affects coral health, and what goes wrong when the corals are stressed.”

Stony corals have been around for more than 400 million years, and today’s coral reefs shelter fish that and harbor . Stressors linked to climate change are already linked to . But simply studying coral microbiomes will not save reefs, Zaneveld said.

“The Great Barrier Reef is huge — roughly twice the size of the state of Washington — so there is probably no drug or beneficial microbe we can add to the water to save it,” said Zaneveld. “But, we can save coral reefs by fighting back against climate change.”

Only tackling the root causes of coral reef decline — through measures to slow climate change and reduce both overfishing and nutrient pollution — will ultimately help corals, he said.

“And if we do, we can also save intricate bacterial symbioses that evolved over millions of years, and that may hold the key to new medical drugs that we would otherwise lose from the world forever,” said Zaneveld.

Co-lead authors of the paper are postdoctoral researchers F. Joseph Pollock at Pennsylvania State University and Ryan McMinds at Oregon State University. Co-authors are Styles Smith and MĂłnica Medina at Pennsylvania State University; David Bourne at James Cook University and the Australian Institute of Marine Science; Bette Willis at James Cook University; and Rebecca Vega Thurber at Oregon State University. The research was funded by the National Science Foundation.

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For more information, contact Zaneveld at 425-352-3789 or zaneveld@uw.edu.

Grant number: 1442306

This microbiological version of the “” is a new paradigm suggested by scientists at the 91±ŹÁÏ Bothell and Oregon State University. It may suggest who would benefit most from screens to identify the microbes that reside in their gut, with implications for drug therapy, management of chronic diseases and other aspects of medical care.

On Aug. 24, the researchers published a in outlining their adaptation of the Anna Karenina principle for the microbial realm. The principle gets its name from the opening line of the novel “Anna Karenina” by Leo Tolstoy: “All happy families are alike; each unhappy family is unhappy in its own way.”

It turns out that this observation applies to perturbed microbiotas of humans and animals. When these microbiotas are unhappy, each is unhappy in its own way.

“This line of thinking started with studies of the microbiology of threatened corals,” said lead and corresponding author , an assistant professor of biological sciences at 91±ŹÁÏ Bothell. “We found that several stressors made the types of bacteria on corals more variable, allowing blooms of different harmful bacteria on each coral.”

“We were struck by similarities to HIV/AIDs. After HIV suppresses the immune system, patients become vulnerable to opportunistic pathogens — but you can’t predict which one will infect any particular patient. It turns out that this microbial variation is a pattern common to many — though certainly not all — stressors and diseases, and occurs in helpful microbes as well as harmful ones.”

Before joining the 91±ŹÁÏ Bothell faculty, Zaneveld was a postdoctoral researcher at OSU, working with assistant professor of microbiology . It was there that they formulated the idea that microbial communities might behave more in line with Tolstoy’s words than scientists had previously thought.

“When microbiologists have looked at how microbiomes change when their hosts are stressed from any number of factors — temperature, smoking, diabetes, for example — they’ve tended to assume directional and predictable changes in the community,” said Vega Thurber, who is also a corresponding author on the perspective. “After tracking many datasets of our own we rarely seemed to find this pattern but rather found a distinct one where microbiomes actually change in a stochastic, or random, way.”

Zaneveld and Vega Thurber worked with OSU doctoral student to survey the academic and research literature on microbial changes caused by perturbation. They found those stochastic — or random — changes to be a common occurrence, but one that researchers have tended to discard or bury deep in supplementary materials, rather than highlight in their reports.

“What’s amazing is how obvious these Anna Karenina principle effects are — if you’re looking for them — and how easy they are to miss if you’re searching for a more conventional pattern,” said Zaneveld. “When researchers have reported them, they’ve often assumed that they are a unique quirk of the microbiology of their disease of interest, rather than a more general phenomenon.”

Their work drew together diverse ideas and experiments from microbiome research — including observations from humans and other animals and across multiple human diseases. They propose new methods for analyzing microbiome data to identify situations where the Anna Karenina principle might be at work.

“When healthy, our microbiomes look alike, but when stressed each one of us has our own microbial ‘snowflake,'” said Vega Thurber. “You or I could be put under the same stress, and our microbiomes will respond in different ways — that’s a very important facet to consider for managing approaches to personalized medicine. Stressors like antibiotics or diabetes can cause different people’s microbiomes to react in very different ways.”

Humans and animals are filled with symbiotic communities of microorganisms that often fill key roles in normal physiological function and also influence susceptibility to disease. Predicting how these communities of organisms respond to perturbations — anything that alters the systems’ function — is one of microbiologists’ essential challenges.

Studies of microbiome dynamics have typically looked for patterns that shift microbiomes from a healthy, stable state to a “dysbiotic,” stable state; dysbiosis refers to any unusual configuration of the microbiome with negative consequences for the health of the host. By the Anna Karenina principle, the microbial communities of dysbiotic individuals vary more in composition than in healthy individuals.

The researchers found patterns consistent with Anna Karenina effects in other systems as well, such as the lungs of smokers. Since microbiomes also influence how patients respond to medical drugs, conditions that make the microbiome more variable — such as inflammatory bowel disorders — may also make more variable patients’ responses to drugs from digoxin to asprin.

But, to consider and test these possibilities, scientists must first discuss the Anna Karenina effect among themselves.

“This is the start of a conversation, and not all diseases will show these patterns,” said Zaneveld. “But when you see the same pattern everywhere — from corals enduring high temperatures to wild chimpanzees with suppressed immunity — it suggests we should pay very close attention to the mechanisms that produce it.”

“I hope that by drawing together these research findings from diverse areas, we accelerate the development of common tools and language to understand the role of chance in shaping the microbial part of ourselves.”

The research was funded by the National Science Foundation.

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For more information, contact Zaneveld at 425-352-3789 or zaneveld@uw.edu and Vega Thurber at 541-737-185 or Rebecca.Vega-Thurber@oregonstate.edu.

Adapted from by the OSU .

91±ŹÁÏ oceanographers have now found that vitamin B-12 exists in two distinct versions in the oceans. A microbe thought to be a main supplier of B-12 in the open oceans, cyanobacteria, is actually making a “pseudo” version that only its kin can use.

The has implications for where algae and other organisms can get a vitamin that is essential to fueling marine life. The paper is in the Jan. 10 issue of the Proceedings of the National Academy of Sciences.

“I think the world is getting used to the idea that all lifeforms are in some ways dependent on microorganisms,” said corresponding author , a 91±ŹÁÏ associate professor of oceanography. “This is another case where microorganisms are playing a really big role in the survival of others, but not quite in the way that we had expected.”

All animals, from humans to whales to sea cucumbers, need vitamin B-12. But only certain microbes can make the complex, cobalt-containing molecule. For land dwellers a main source is the microbes that thrive in animals’ guts, which is why beef is such a good source of B-12. Shellfish also accumulate a lot of B-12. In the surface waters of the open oceans, a main supplier of B-12 was believed to have been .

But the new paper uses various techniques — including sampling in the Pacific Ocean, genetic analyses and growing bacterial cultures in the lab — to prove that cyanobacteria make a different form, known as “pseudo” B-12.

That means that all the other light-absorbing phytoplankton in the oceans are getting their B-12 from somewhere else.

“Phytoplankton are incredibly important as the base of the marine food web, for oxygen generation on Earth and carbon uptake in the ocean,” said first author , a 91±ŹÁÏ doctoral student in oceanography. “Somebody’s making B-12 for them, and it’s not who we thought it was.”

The first hint of a knockoff form of B-12 came from the marine algae , a popular health supplement. Analyses of its contents in Japan showed an unusual form of the B-12 molecule.

In previous research, Heal developed a in seawater that can distinguish between similar molecules. The new study applied that technique to see where different forms of vitamin B-12 exist in the open ocean.

“When I started looking, I saw that in some parts of the ocean the pseudo B-12 is even more common than the regular B-12,” Heal said.

The research confirms that virtually all cyanobacteria, the dominant form of light-harvesting organisms in oceanic gyres and other parts of the open ocean, only make and use pseudo B-12. The two forms of B-12 are incompatible, so cyanobacteria also have a different form of the protein that requires that vitamin to function.

“Nobody has shown that this molecule, pseudo B-12, exists in the environment,” Heal said. “Now we know where it comes from, why it’s there, and we have some hints that it can be rearranged.”

The marine environment might contain a specialized subset of microbes that can convert pseudo B-12 into regular B-12, creating a sort of black market for the converted vitamins.

“That would require several specific microbes to coexist in the same place, and suggests a complex interdependency,” Ingalls said.

The authors also show that for many parts of the ocean it now appears that regular B-12 is directly supplied by marine archaea. Experiments in the study show that archaea may be the dominant source of B-12 in parts of the ocean where they live, furthering from the 91±ŹÁÏ research group.

“To understand the marine ecosystem, you have to understand what supports growth,” Ingalls said. “We know where nitrogen and phosphorus come from. But for vitamin B-12, a molecule we’ve known about for more than half a century, we’re only now realizing who’s making it in the marine ecosystem.”

The research was funded by the National Science Foundation and the Simons Foundation. Other 91±ŹÁÏ co-authors are Wei Qin, Francois Ribalet, Anthony Bertagnolli, Willow Coyote-Maestas, Laura Hmelo, Allan Devol, Virginia Armbrust and David Stahl; and James Moffett at the University of Southern California.

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For more information, contact Heal at kheal@uw.edu and Ingalls at aingalls@uw.edu or 206-221-6748.

NSF Grants: OCE1228770, OCE1046017

These are , a diverse group of organisms that includes microalgae, viruses, bacteria and archaea. They serve as the base of the marine food chain and are responsible for controlling much of the ocean’s nutrient flow and health.

But given their prevalence, very little is known about how they interact and carry out fundamental processes in the ocean, particularly in deep, low-oxygen waters where the impacts of climate change are becoming significant. In these areas, up to half of all available nitrogen — a nutrient that is essential for all ocean life — is lost due to microbial processes on overdrive because of warmer ocean water and less circulation.

Now, a 91±ŹÁÏ team has on a common but poorly understood bacteria known to live in these areas. By culturing and sequencing the microbe’s entire genome, the oceanographers found that it significantly contributes to the removal of life-supporting nitrogen from the water in new and surprising ways.

“If we want to understand how the oceans are working and be able to model them in any sort of predictive way, we need to more accurately understand what the inputs and outputs are,” said senior author , a 91±ŹÁÏ associate professor of oceanography. “This is an important organism that fixes carbon, is involved in nitrogen loss and is in parts of the ocean that are shifting due to climate change. We now have the first-ever culture in the laboratory and we can study its physiology.”

The were published July 19 in the , a Nature publication.

This organism, given the name Candidatus Thioglobus autotrophicus, is present in low-oxygen waters around the world and is one of the dominant organisms in these areas — between 40 and 60 percent of all cells in some regions.

Living things use oxygen for their metabolic activities, but in low-oxygen areas, bacteria and archaea have evolved to “breathe” other elements available in seawater. One of those is a chemical called nitrate which, when respired, produces gaseous nitrogen. That gas escapes to the atmosphere, effectively leaving the ocean and removing valuable nitrogen from the water.

The bacteria grown and sequenced by the 91±ŹÁÏ oceanographers have been pegged as playing a big role in removing nitrogen from the ocean, but until now scientists didn’t have a complete picture of how it happened.

“We are filling in the gaps by providing a full genome,” said lead author , a 91±ŹÁÏ doctoral student in oceanography. “Now we can talk about both what these organisms can and can’t do.”

The research team confirmed the bacteria are contributing to nitrogen loss, but in a different way than expected. More specifically, they are responsible for a key step — converting nitrate to a similar chemical called nitrite — which then goes on to fuel other nitrogen-removal processes. Earlier research had hypothesized that these microbes also produce ammonia, another nitrogen-containing chemical. Instead, the 91±ŹÁÏ team found that the microbes consume ammonia, essentially competing with other organisms for this nitrogen compound that is also important for growth and development.

At a global scale, the areas of the ocean where these bacteria live are getting bigger as climate change creates conditions that produce low-oxygen zones, including warmer ocean temperatures and less water circulation.

“In the very big picture, we know that different types of oxygen minimum zones that house these organisms are getting bigger and more persistent,” Shah said. “So, whatever influence these bugs have on water chemistry and the atmosphere is going to get more and more important — basically, their habitat is expanding.”

Growing this organism in the lab was no easy task. The 91±ŹÁÏ oceanographers combined several techniques to culture the bacteria in as close as possible to their native ocean environment. It took almost a year to stabilize them to the point where researchers could start doing physiological experiments.

Even the experiments, however, took more time than usual, because these organisms grow much slower than most cultures grown in the lab.

“Most experiments lasted 10 to 15 days because they were growing so slowly. But the advantage is they are actually behaving very similarly to how they do in the ocean environment,” Morris said.

Shah collected the organism from a low-oxygen fjord off the coast of British Columbia from the R/V Thomas G. Thompson during a . She then used these organisms to grow identical offspring in the lab.

The researchers will look next at the role this bacteria play in the ocean’s carbon and sulfur cycles. They also recently received National Science Foundation funding to study this organism and its relatives in other low-oxygen areas around the world, including off the coast of Mexico.

of the 91±ŹÁÏ’s Joint Institute for the Study of the Atmosphere and Ocean is a co-author on this study. The work was funded by the National Science Foundation, the 91±ŹÁÏ Royalty Research Fund and the .

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For more information, contact Morris at morrisrm@uw.edu or 206-221-7228 and Shah at vs1@uw.edu or 206-685-4118.

Grant numbers: OCE-1232840, DGE-1068839