The University of Â鶹´«Ã½ at Mānoa’s celebrated its 15th anniversary on October 25, marking a decade and a half of cutting-edge discovery and sustainable design.

Opened in 2010, the 26,997-square-foot facility has become a hub for groundbreaking research on marine microbes—organisms that play a vital role in the health of the planet’s oceans and climate. The state-of-the-art building houses laboratories, offices and a conference center designed to foster collaboration among scientists across disciplines and time zones. Its 50-seat auditorium supports video conferencing and live webcasting, connecting researchers around the world.

In 2012, C-MORE Hale was the first research laboratory building in Â鶹´«Ã½ to achieve LEED Platinum certification for environmental design. The facility incorporates energy-efficient systems and low-flow plumbing. It also features smart lighting controls and water recycling technologies that reduce potable water use by nearly half. The building’s innovative design earned multiple awards, including the Kukulu Hale Award for new commercial projects in 2011.

Leading research in microbial oceanography

David M. Karl, C-MORE’s founding director, member of the National Academy of Sciences and a professor of at UH Mānoa, was instrumental in securing the 10-year, $36.8 million National Science Foundation (NSF) grant in 2006 that led to its establishment as an NSF Science and Technology Center. The center unites specialists in biology, chemistry, oceanography and engineering from six partner institutions. Together, these teams investigate the structure, diversity and metabolic function of marine microbes—from those that use sunlight to generate energy to others that recycle organic matter and drive global nutrient cycles.

Beyond the facility itself, Karl and C-MORE have positioned UH Mānoa as a global leader in microbial oceanography by successfully establishing a link between molecular-level biology and large-scale ocean processes. His pioneering research on marine microbes and their role in global biogeochemical cycles has shaped modern understanding of how ocean life regulates Earth’s climate. Today, Karl continues to play a key role in advancing microbial oceanography worldwide.

“The opportunities that have been sustained by the investment in C-MORE Hale have put Â鶹´«Ã½ on the map of ocean research,” Karl said. “UH is now recognized as one of the top institutions in the world to study microbial oceanography, and we are also training the next generation of leaders. The future is today.”

Modeling the future of Earth’s oceans

C-MORE’s integrated research program is organized around four themes: microbial biodiversity, metabolism and nutrient flow, remote and continuous sensing of ocean processes, and ecosystem modeling and prediction. This approach allows scientists to explore how marine microorganisms influence climate, carbon storage and energy transfer within ocean ecosystems. The center’s work has advanced predictive models of how marine environments respond to environmental change, establishing UH Mānoa as a key contributor to global ocean science.

“C-MORE Hale encompasses all the success in microbial oceanography and David Karl is the founder for microbial oceanography,” UH Mānoa Interim Provost Vassilis L. Syrmos said. “He has brought funding—tens of millions of dollars to support this from the National Science Foundation, from the Moore Foundation, so private, public, federal, state, you name it. It is an unbelievable project. He has created a program that is second to none, not only here in Â鶹´«Ã½ and in the continent, but in the world.”

Karl was instrumental in the establishment of an open ocean time-series, called the Â鶹´«Ã½ Ocean Time-Series, as a sentinel for observing the effects of climate on the structure and function of microbial communities. C-MORE’s long-term research station, , located about 60 miles north of Oʻahu, was designated a Milestones in Microbiology Site by the American Society for Microbiology in 2015. The recognition honored UH’s historic contributions to understanding marine microbial life and its role in maintaining planetary habitability.

Building Â鶹´«Ã½â€™s future in ocean science

In addition to its research mission, C-MORE supports education and outreach programs that inspire future ocean scientists and engage the public in microbial ecology. These efforts span from pre-college curricula and teacher training to graduate and postdoctoral research opportunities, helping to strengthen the next generation of oceanographers.

C-MORE Hale’s naming under the Daniel K. Inouye Legacy Program honors the late senator’s lifelong commitment to advancing science and education in Â鶹´«Ã½.

During C-MORE Hale’s 15th anniversary, many students and staff are aboard the R/V Kilo Moana, a 186-foot UH Mānoa research vessel that supports the center’s oceanographic missions by serving as a mobile platform for sampling, experiments and data collection at sea. Karl said a formal celebration to mark the milestone is planned for later this fall.

A team of researchers have spent years taming mysterious marine microbes from the open ocean to grow in a lab, to investigate their feeding habits. The group’s latest discoveries, led by University of Â鶹´«Ã½ at Mānoa professors Grieg Steward and Kyle Edwards and supported by funding from the National Science Foundation, revealed that a wide variety of phytoplankton in their collection are not just photosynthesizing; in many cases they are also voracious predators. The study was published in .

Phytoplankton use light from the sun to photosynthesize and grow, and some photosynthesize and eat prey, just like a Venus flytrap. But, unlike carnivorous land plants, these dual-function phytoplankton are microscopic—each is a single cell less than one-tenth the width of a human hair—and they swim using flagella to catch bacterial prey. Because these phytoplankton mix two different feeding modes (photosynthesis and predation), they are referred to as mixotrophs (from mix plus the Greek trophikós pertaining to food).

“Oceanographers have known about mixotrophs for a long time, but interest in them has really been growing over the past decade as we learn just how prevalent and important they are in the ocean’s ecosystem,” said Qian Li, the lead author of the study and former post-doctoral researcher in the (C-MORE) at the UH Mānoa (SOEST). Li is now a faculty member at Shanghai Jiao Tong University in China.

• Related Â鶹´«Ã½News story: New marine phytoplankton species have symbiont that produces their ‘fertilizer’, February 15, 2022

Isolating and growing phytoplankton

One of the major contributions of the research, and the foundation of the current study, was the cultivation of a large collection of diverse mixotrophs from the open ocean, a process carried out by Christopher Schvarcz while a graduate student and then post-doctoral researcher in C-MORE.

“Many of these species in our collection had been detected in seawater using trendy molecular identification methods, but they had never been grown in culture before,” said Schvarcz. “As a result, enormous amounts of data have been accumulating on who is living out there in the open ocean, but we didn’t know what they were doing or how fast they were doing it.”

“Having this unprecedented collection of species in culture is very exciting, and it completely changes the kinds of questions we can ask,” said Edwards, study co-author and professor in SOEST.

Filling a gap in knowledge

One of those questions was “just how quickly do these mixotrophs eat Prochlorococcus?”—a photosynthetic bacterium and one of the single biggest contributors to photosynthesis in the open ocean. Figuring out who eats these tiny cells is fundamental to understanding the ocean ecosystem.

Mixotrophs appear to be major consumers of bacteria, and that would include photosynthetic bacteria such as Prochlorococcus, but until now there has been no direct observation that any mixotroph eats this key player of the marine food web, and no data on the rates at which they do so. That situation has dramatically changed with this new study that compared the feeding rates of dozens of unique phytoplankton isolates and quantified how feeding rates are affected by food availability.

“Dr. Li did an impressive amount of careful experimental work for this study,” said Steward, study co-author and SOEST professor. “The number of new oceanic phytoplankton she characterized is extraordinary, and it revealed that different species of mixotrophs vary widely in their feeding rates. These data help fill a large gap in our knowledge about how different mixotrophs fit into the marine food web.”

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An international group of leading microbiologists, including Professor David Karl, has issued a warning: Not including microbes, considered the support system of the biosphere, in any climate equation will lead to incomplete predictions of the environmental consequences of global climate change.

More than 30 microbiologists from nine countries are calling for the world to stop ignoring an “unseen majority” in Earth’s biodiversity and metabolism when addressing climate change. The , was published in the journal .

“Microorganisms controls the pulse of our planet,” said Karl, director of the UH Mānoa in the (SOEST). “They harvest solar energy, recycle organic matter, sequester carbon dioxide, and detoxify many human-made pollutants. In other words, microbes make things happen.”

With their statement, the researchers hope to raise awareness for how microbes can influence climate change and how microbes will be impacted by it. They urge the inclusion of microbes in climate change research, increasing the use of research involving innovative technologies and improving education in classrooms.

Microbes dominate the life on Earth and perform critical functions in animal and human health, agriculture, the global food web and industry.

Said Rick Cavicchioli, a professor and microbiologist at the School of Biotechnology and Biomolecular Sciences at the University of New South Wales Sydney who led the global effort, “Micro-organisms, which include bacteria and viruses, are the lifeforms that you don’t see on the conservation websites. They support the existence of all higher lifeforms and are critically important in regulating climate change. However, they are rarely the focus of climate change studies and not considered in policy development.”

See the on the SOEST website.

—By Marcie Grabowski

, professor and director of the , is the only woman at the University of Â鶹´«Ã½ who is a member of the . In her , commemorating her induction into one of the country’s most distinguished scientific groups, she and a team of researchers reveal a newly discovered mechanism by which organisms select beneficial microbes and reject harmful ones.

The internal microbial communities, or consortia, of mammals, such as humans, are complex in that they require many bacterial types for healthy function. Tissues in the respiratory system, the Fallopian tubes, and the Eustachian tubes are lined with cilia—microscopic hair-like structures that extend out from the surface of many animal cells. A central role attributed to these ciliated tissues is to effectively clear out toxic molecules and undesirable microbes; in work performed largely by Janna Nawroth (now at Emulate, Inc., Boston) and co-led by McFall-Ngai and Eva Kanso, a mathematical modeler at the University of Southern California, these ciliated tissues are shown to also selectively recruit beneficial microbes, called symbionts.

“A few years ago, when the biomedical community discovered that all of these surfaces of mammals have a rich co-evolved microbial consortium, a microbiome, that promotes the health of those systems, the question became: how do they do it—that is, by what mechanisms do they select the good microbes and reject the harmful ones?” explained McFall-Ngai.

Model system offers window into microscopic world

The ciliated tissues of most animals are inaccessible to observation and study. Using the Hawaiian bobtail squid and its single bacterial symbiont, Vibrio fischeri, as a model biological system, the collaborative research team—comprised of a biomechanicist/bioengineer, an applied physicist, mathematicians, an imager, a microbiologist and McFall-Ngai, a developmental biologist and biochemist—investigated the process by which an appropriate symbiont species is recruited into a host animal’s microbiome at the exclusion of all other bacteria. 

This model system provides a special window into such complex problems because the squid partners up with only one symbiont species, which it selects using the activity of a complex ciliated surface. In addition, the body plan of this animal is such that researchers can use microscopy to watch the process happen along this highly accessible tissue surface.

“We were surprised to find two different cilia behaviors,” said McFall-Ngai. “One behavior is typical of long cilia—very organized, with waves of cilia groups beating together. These fields of cilia serve to concentrate the bacterial partner into the areas where colonization will occur. We also found fields of short cilia that were beating, but each independently. The mathematical modeling and visualization showed that these shorter cilia serve to mix the chemical signals of the host cell so as to attract the partnering bacteria.”

From micro- to macro-scale

Because the structure and function of cilia are conserved throughout the evolution of animals, this study provides insight into the very basic function of ciliated surfaces.

“With this starting point, we can begin to determine how the whole system, host cells, their secretions and their bacterial partners, work to dissuade the colonization of these tissues by deadly pathogens, such as those that cause whooping cough, strep throat/ rheumatic fever, and two different types of pneumonia,” said McFall-Ngai. “This information may also aid development of ways to foster the acquisition and growth of beneficial bacterial partners along human respiratory, reproductive, and excretory tracts.”

For nearly three decades, McFall-Ngai and researcher at the UH ²ÑÄå²Ô´Ç²¹ School of Ocean and Earth Science and Technology’s Pacific Biosciences Research Center, have used the squid bacterial symbiosis system to characterize animal microbiomes. They discovered bacteria affecting animal development and bacterial partners driving circadian (daily) rhythms of their host.

• Related UH News story and video: , February 5, 2017

These and other insights have contributed to expanding the once narrow view of the microbial world. Based on her distinguished and continuing achievements in original research, McFall-Ngai, was elected to the National Academy of Sciences in 2015. Election to the academy is one of the highest honors in the field of science.

The work was funded by the National Science Foundation INSPIRE (Integrated NSF Support Promoting Interdisciplinary Research and Education) grant to Eva Kanso; and National Institutes of Health grants to McFall-Ngai and Ruby.

—By Marcie Grabowski

Microbes dominate the planet, especially the ocean, and help support the entire marine food web. In , University of Â鶹´«Ã½ at ²ÑÄå²Ô´Ç²¹ oceanography professor and his team report the largest single-site microbiome gene catalog constructed to date. With this new information, the team discovered nutrient limitation is a central driver in the evolution of ocean microbe genomes.

As a group, marine microbes are extremely diverse and versatile with respect to their metabolic capabilities. All of this variability is encoded in their genes. Some marine microorganisms have genetic instructions that allow them to use the energy derived from sunlight to turn carbon dioxide into organic matter. Others use organic matter as a carbon and energy source and produce carbon dioxide as a respiration end-product. Other, more exotic pathways have also been discovered.

“But how do we characterize all these diverse traits and functions in virtually invisible organisms, whose numbers approach a million cells per teaspoon of seawater?” asked DeLong, senior author on the paper. “This newly constructed, comprehensive gene catalog of microbes inhabiting the ocean waters north of the Hawaiian Islands addresses this challenge.”

Transition zone reveals influence of nutrients

Water samples were collected over two years, and modern genome sequencing technologies were used to decode the genes and genomes of the most abundant microbial species in the upper 3,000 feet of water at the (HOT) Program open ocean field site, Station ALOHA.

Just below the depth of sunlit layer, the team observed a sharp transition in the microbial communities present. They reported that the fundamental building blocks of microbes, their genomes and proteins, changed drastically between depths of about 250-650 feet.

“In surface waters, microbial genomes are much smaller, and their proteins contain less nitrogen<—a logical adaptation in this nitrogen-starved environment,” said Daniel Mende, post-doctoral researcher at the UH ²ÑÄå²Ô´Ç²¹ (SOEST) and lead author on the paper. “In deeper waters, between 400–650 feet, microbial genomes become much larger, and their proteins contain more nitrogen, in tandem with increasing nitrogen availability with depth.”

“These results suggest that the availability of nutrients in the environment may actually shape how microbial genomes and proteins evolve in the wild,” said DeLong. “Another surprising finding of the study is that the microbial ‘genomic transition zone’ observed occurs over a very narrow depth range, just beneath the sunlit layer. Below about 650 feet deep, the fundamental properties of microbial genomes and proteins are relatively constant, all the way down to the seafloor.”

Making data widely available

In collaboration with a computer science group led by professor Bonnie Hurwitz at the University of Arizona, who are seeking to describe the nature and function of microbes in the global oceans.

“These new data will provide an important tool for understanding the nature and function of the ocean’s microbiome today, as well as help predict its trajectory into the future,” said DeLong.

This effort was the result of a collaboration between three major programs at UH ²ÑÄå²Ô´Ç²¹—the Program, the National Science Foundation Science and Technology (C-MORE), and the (SCOPE). These programs are operated out of UH ²ÑÄå²Ô´Ç²¹ Daniel K. Inoue C-MORE Hale. The work was funded by the National Science Foundation, the Gordon and Betty Moore Foundation and the Simons Foundation.

—By Marcie Grabowski

A team of scientists from the University of Â鶹´«Ã½ at Mānoa showed for the first time that many novel viruses are present in the fluids circulating deep in the rocky crust of the seafloor known as the ocean basement. Their also provides evidence that the viruses are actively infecting the many unusual microorganisms that live in the basement.

Viruses are often thought of as a nuisance because of the familiar diseases they cause—common colds and the flu, for example. However, viruses infect every living thing on earth and viral infections have been one of the major creative forces that shape the nature of life on our planet. The first viruses likely originated at the dawn of life billions of years ago. Through relentless cycles of infections, viruses have helped drive the evolution of the diverse life found on our planet and their influence continues to this day.

Exploring the deep frontier

“The ocean basement was one of the last major habitats on Earth for which we had no information on the number and types of viruses present,” said lead author Olivia Nigro, a post-doctoral researcher of . “The volume of water that moves under the seafloor through the ocean basement is enormous. Annually, it is equivalent to the flow of all the rivers on the planet combined.”

Hydrothermal vents and plumes, like those found in Â鶹´«Ã½ at Lōʻihi seamount, are the most spectacular evidence of that flow.

“Despite the massive scale of flow through the seafloor and its importance for understanding the chemical balance of our oceans, our view of the unusual microorganisms that live in this fluid and how they interact is still very sketchy,” said , oceanography professor and lead investigator for the project.

It is very challenging to get a clean sample of water from rocks buried under hundreds of feet of sediment at the bottom of the Pacific Ocean. To do this, the team took advantage of devices designed to plug holes drilled deep into the seafloor called Circulation Obviation Retrofit Kits, or CORKs. The bottom of the CORKs seal off the fluids in the basement and transport samples of that fluid to a sampling port that extends a few meters above the seafloor. The CORKs sampled were over one-and-half miles under the ocean and required an autonomous underwater vehicle to connect the sample vessels, open and close the valves, and return the samples to the surface.

The researchers used microscope and DNA analyses to count and characterize the viruses in the fluids and to detect viral DNA inside of cells. This pioneering work provided the first look at the diverse and unusual viruses infecting the microorganisms in warm basaltic crust, which forms the very foundation of the Hawaiian Islands. Surprisingly, many of them resemble the lemon- and rod-shaped viruses found in hot springs on land, like those in Yellowstone National Park, even though these two habitats are very far apart.

Looking deep, deep into the past

“One of the likely places for the origin of the first living cells and viruses was in hydrothermally active seafloor,” said Nigro. “Analyzing viruses from this remote habitat helps us flesh out the deep branches on the virus family tree so we can better understand their origins, their contributions to the history of life, and how they influence the activities of microbial life in the crust.”

“The data we obtained provides clues about the nature of a microbial world that lies hidden deep in the roots of these volcanic islands,” said Steward. “Through their interactions with rock and water, these deep-dwelling communities of microbes and their viruses are invisible engineers contributing to the chemical balance of our oceans.”

New funding from the (NSF) will allow the researchers to collect additional samples in the Atlantic Ocean. The conditions in the crust there are very different from those in the Pacific oceanic basement, and the team hopes to determine how these different conditions influence the community of the microbes and their viruses.

Inspiration and support

This work was inspired by and was made possible in part by the pioneering work of the late James P. Cowen, an esteemed and long-serving faculty member in the Department of Oceanography at UH Mānoa. The researchers dedicated the paper to him in recognition of the encouragement and support that he provided to the team that was instrumental to the success of the project.

The NSF funded this work through two of its Science and Technology Centers, the located at the University of Southern California and the at UH Mānoa.

—By Marcie Grabowski

Researchers from laboratory at the and from Professor laboratory at in Göteborg, Sweden, developed a computer model which takes into account hundreds of genes, chemical reactions and compounds required for the survival of Prochlorococcus, the most abundant photosynthetic microbe on the planet. They found that Prochlorococcus has made extensive alterations to its metabolism as a way to reduce its dependence on phosphorus, an element that is essential and often growth-limiting in the ocean.

Revolutionary developments in gene sequencing technology have allowed scientists to catalog and investigate the genetic diversity and metabolic capability of life on Earth—from E. coli bacteria to humans, and much in between. Ocean monitoring and advances in oceanographic sensors have enabled a more detailed look than ever before at the environmental conditions that are both the consequence of microbial activity and act as stressors on the growth of microbes in the ocean.

This new metabolic model, , represents a window to the inner workings that enable microbes to dominate Earth’s chemical and biological cycles, thrive in the harshest conditions and make the planet habitable—a black box, in a sense.

A previously unknown survival strategy

Microbes are known to employ three basic strategies to compete for limiting elemental resources: cell quotas may be adjusted, stressed cells may synthesize molecules to make more efficient use of available resources and cells may access alternatives or more costly sources of the nutrient.

In the case of phosphorus, a limiting resource in vast oceanic regions, the cosmopolitan Prochlorococcus thrives by adopting all three strategies and a fourth, previously unknown strategy.

“By generating the first detailed model of metabolism for an ecologically important marine microbe, we found that Prochlorococcus has evolved a way to reduce its dependence on phosphate by minimizing the number of enzymes involved in phosphate transformations, thus relieving intracellular demands” said , an oceanography doctoral candidate at the UH Mānoa and lead author of the recently published study.

Prochlorococcus has an extremely minimal genome. If it were to lose the function of any one metabolic gene, its survival would be nearly a coin toss. To their surprise, Casey and co-authors discovered that the world’s most abundant microbe has performed, through a process called “genome streamlining”—the concerted loss of frivolous genes over evolutionary time—a comprehensive re-design of the core metabolic pathways in response to the persistent limitation of phosphorus.

“The dramatic and widespread change in the metabolic network is really a shock,” said Casey. “However, we’re seeing that these changes provide a substantial growth advantage for this ubiquitous microbe in phosphorus-limited regions of the ocean, so it seems that where there’s a will there’s a way.”

Creating the model

The computer model is built from an enormous library of genetic data compiled from researchers around the world, and the results are validated with data from numerous laboratory culture experiments and field studies.

“We’re interested in the underlying principles guiding metabolism and physiology in marine microbes, and that is going to require a deep understanding of not only the 1-dimensional genetic code, but also the 4-dimensional product it codes for,” said Casey. “So we’re looking to a systems-level approach to incorporate a great variety of physiological and ’omics studies all in one computational structure, with the hope that we can start to learn from the design and interactions of these complex systems.”

In the future, the researchers plan to expand the model to include more representatives of the marine microbial community and to look deeper into micro-diversity within the Prochloroccocus genus.

“This will allow us to simulate marine microbial community metabolism at an unprecedented level of detail; embedding these fine-scale simulations within global ocean circulation models promises to deliver insights into how microbial assemblages interact with their environment and amongst each other,” said Casey.

Opportunities for an outstanding graduate student

This work was funded by the (NSF) through the competitive which provided Casey with three years of research support. A portion of this work was made possible through Casey’s acceptance into NSF’s (GROW) program which expands opportunities for U.S. graduate students to engage in international research collaboration. GROW is open to only active awardees of the Graduate Research Fellowship Program. Additional funding was provided by the Simons Foundation, the Swedish Research Council, and the Gordon and Betty Moore Foundation.

—By Marcie Grabowski

On May 13, the White House announced a new (NMI), a coordinated effort to better understand microbiomes—communities of microorganisms that live on and in people, plants, soil, oceans and the atmosphere—and to develop tools to protect and restore healthy microbiome function. This initiative represents a combined federal agency investment of more than $121 million.

For years, the has been making substantial investments—through faculty hires, endowments and facilities—and plans to continue to build capacity in the emerging field of microbiome research.

“UH Mānoa is a powerhouse in the realm of microbiome research,” said UH Mānoa Vice Chancellor for Research Michael Bruno. “There are few, if any, universities with the number of world leaders in this domain—UH Mānoa has three members of the (NAS) who specialize in this field.”

Along with long-established UH Mānoa scientists, recent and upcoming hires of faculty will support the NMI and advance related research discoveries. In the past two years, and with an allocation of $2.2 million, UH Mānoa has hired three professors, two junior faculty, and two related positions—all of whom address microbiomes. Further, the UH Mānoa (PBRC) will invest $1 million in hiring two additional faculty to explore complex microbial ecosystems.

“Major challenges facing mankind, including sustainability of the environment, human health, and energy and food production, have the microbial world as a principal driving force in both the creation of the problems as well as strategies for the development of solutions. We have a great opportunity here in Â鶹´«Ã½ to participate as pioneers in the research of our microbial biosphere,” said , NAS member and director of PBRC.

More investment in the microbiome future

In 2014, the Pavel family announced an endowment of $2 million to the (C-MORE). Professor , co-founder of the program and C-MORE director, is the inaugural recipient of the Victor and Peggy Brandstrom Pavel chair in Oceanography.

UH Mānoa has invested nearly $37 million in construction and renovation of facilities that primarily support microbiome research. The majority of this ($22.5 million) went toward construction of the Daniel K. Inouye C-MORE Hale, a state-of-the-art LEED Platinum building, which was dedicated in 2010. C-MORE, as a National Science Foundation Science and Technology Center, required a cost share from UH—a contribution of approximately $9 million as cash or in-kind support. The university will continue to support shorefront and ocean-going assets that provide unparalleled access to the coastal and deep-water environments in which many microbiome researchers work. These additional future investments are expected to be greater than $5 million over the next 5 years.

Microbiomes maintain healthy function of diverse ecosystems, influencing diverse features of the planet—human health, climate change, and food security. UH Mānoa, as a partner in the NMI, will advance the understanding of microbiome behavior and enable protection and restoration of healthy microbiome function. From medicine to global climate change to deep sea mining, microbiome research is proving to be the next frontier—an area of research that is yielding new understanding and paradigm-shifting discoveries about the world around, and in, us.

UH projects and expertise

Numerous internationally recognized faculty at ²ÑÄå²Ô´Ç²¹ actively contribute to this field of discovery. A sampling of some of these faculty and their research emphasis are listed below:

• (C-MORE):  Influence of bacteria on animal origins
• (): Environmental and biogeographic processes that shape the composition of symbiotic microbial communities and how differences impact hosts 
• Gordon Bennett (Plant and Environmental Protection Sciences): Microbe-insect symbioses in native Hawaiian and pest insect systems
• (C-MORE): Develops and applies advanced genomic and robotic technologies to study dynamics of marine microbial communities from surface waters to the deep-sea
• (Â鶹´«Ã½ Institute of Marine Biology): Microbiomes of reef corals and their contribution to coral health and response to environmental stress
• (PBRC): Mechanisms by which surface microbial films induce the settlement of invertebrate larvae and thus strongly influence sea floor ecosystems
• (): Microbe-host interactions in the human gut microbiome that underlie the development of gastrointestinal cancer and metabolic disorders such as diabetes
• Dave Karl (C-MORE): Microbial processes that determine how energy, nutrients and chemicals cycle through the open ocean
• Margaret McFall-Ngai (PBRC): Uses simple invertebrate model systems to study how microbiomes colonize the surfaces of animal epithelia, the most common type of host-microbe interaction
• (PBRC): Mechanisms underlying microbe-microbe and microbe-host communication 

—By Marcie Grabowski

In the microscopic life that thrives around coral reefs, a team of researchers, including , postdoctoral researcher at the University of Â鶹´«Ã½ at Mānoa’s Â鶹´«Ã½ Institute of Marine Biology, have discovered an interplay between viruses and microbes that defies conventional wisdom. As the density of microbes rises in an ecosystem, the number of viruses infecting those microbes rises with it. It has generally been assumed that this growing population of viruses, in turn, kills more and more microbes, keeping the microbial population in check. It’s a model known as “kill-the-winner”—the winners being the blooming microbial cells and the killers being the viruses (mostly bacteria-killing viruses known as bacteriophages) that infect them.

However, previous research has suggested that, under certain conditions, viruses can change their infection strategy. As potential host microbes become more numerous, some viruses forego rapid replication and opt instead to reside peaceably inside their host, thereby reducing the viruses’ numbers. In a study Barott, along with lead authors Ben Knowles and Cynthia Silveira, both in at , and co-authors refer to this alternative model as “piggyback-the-winner,” and it could have implications for phage-based medicine and ecosystem resilience in the face of environmental disturbances that promote microbial blooms.

Microbial population explosions can take many forms—algal blooms in the ocean and in lakes, fungal blights in soil and bacterial infection in humans are just a few examples—and how viruses respond to this rapid microbial growth has long interested ecologists. Many viruses can make the switch between rapid replication and dormant coexistence. For decades, most researchers have assumed that during microbial population booms, their viruses take advantage of the opportunity to multiply by killing the abundant microbial winners.

“Kill-the-winner seems to make sense,” said Knowles. “The logic behind it has been around for a while. The reasoning is very seductive.”

And the winner is…

The international team of collaborators—with expertise ranging from mathematics, physics and statistics to ecology and molecular biology—decided to put this model to the test. They collected samples of microbe-rich seawater near coral reefs in both the Pacific and Atlantic Oceans. Then, using a combination of microscopic and genomic techniques, they analyzed those samples for the abundance and nature of both microbes and the viruses that infect them.

Under the kill-the-winner model, researchers would expect to find more viruses per microbe in samples with a high microbial density and growth rates. What the team found, however, was just the opposite—as microbial abundance increased, the virus-to-microbe ratio decreased significantly.

Next, the team ran an experiment in which they incubated seawater from a pristine coral reef location and from Mission Bay in San Diego for several days, during which they monitored the viral and microbial abundance. The results matched their field sampling, with virus numbers staying relatively low even as microbial populations bloomed.

Why weren’t the viruses exploiting the increasing population of hosts by infecting them and multiplying rapidly? Why weren’t they killing the winner? Exploring this phenomenon further, the researchers used metagenomic analysis to determine whether the viruses in the sample showed virulent, predatory traits or the hallmarks of non-predatory lifestyles. Intriguingly, they found that in samples with a higher microbe count, viral communities became less virulent.

Better living through integration

Instead of multiplying and killing off their booming host population, more of the viruses instead integrate themselves into their host. The viruses replicate more slowly, but they also avoid competing with other viruses and having to navigate with the host’s own immunity defenses. This piggyback-the-winner model better explains virus-host dynamics during periods of fast microbial growth than the established kill-the-winner model, the researchers said.

“When you have a fast-growing host, if you’re a virus, you profit more from integration,” Knowles said. “It’s just intelligent parasitism.”

A better understanding of these dynamics holds promise for improving human health. For example, specially targeted phages have been suggested as a possible therapy for conditions like cystic fibrosis, which is caused by frequent bacterial lung infections. This discovery also could help improve marine ecologists’ understanding of the microbiological forces that influence coral reef health.

—By Marcie Grabowski

The biological carbon pump is the process by which carbon dioxide (CO2) is transformed to organic carbon via photosynthesis, exported from the surface ocean as sinking particles and finally sequestered in the deep sea. While the intensity of the pump is directly correlated to the abundance of certain plankton species—free-floating micro-organisms—the underlying ecosystem structure driving the process has remained poorly understood.

By analyzing samples collected by the expedition (2009–2013), an interdisciplinary team of biologists, computer scientists and oceanographers, led by Lionel Guidi, affiliated researcher of oceanography at the University of Â鶹´«Ã½ at Mānoa and CNRS researcher at Laboratoire d’Océanographie de Villefranche (France), has shed new light on these microbes, their interactions and the main functions associated with the biological pump in nutrient-poor ocean regions—areas which represent more than 70 percent of the surface ocean.

The ‘planktonic social network’

Ocean microbes are extraordinarily varied, produce half the world's oxygen from photosynthesis, and form the base of the oceanic food chain that feeds fish and marine mammals.

In , Guidi and co-authors (see complete list below) made use of articles previously published in Science, and especially . They used computer analyses to describe the first ‘planktonic social network’ associated with carbon export in nutrient-poor regions. Many of the players involved, such as certain photosynthesizing algae (especially diatoms) and copepods (tiny shrimp-like organisms) were already known. However, the role played by certain microorganisms (single-celled parasites, cyanobacteria and viruses) in carbon export was previously grossly underestimated.

The genetics tell a deeper story

Going further, the researchers then characterized a network of functions, based this time on the analysis of the genes of bacteria and viruses. The Tara Oceans database enabled them to establish that the relative abundance of a small number of bacterial and viral genes can predict a significant proportion of variations in carbon export from the upper layers of the ocean to the deep ocean. Some of these genes are involved in photosynthesis and membrane transport, promoting among other things the formation of sediments and breakdown of organic aggregated material. However, the function of most of these genes is still unknown.

Taking a global view

One future objective for the team is to repeat this work for nutrient-rich oceanic regions, to determine whether the planktonic networks are different in various marine environments.

The ocean is the largest carbon sink on the planet. The recent findings will enable researchers to better understand the sensitivity of this network to a changing ocean and to better predict the effects that climate change will have on the functioning of the biological carbon pump, which is a key process for removing carbon from the atmosphere and sequestering it into the deep sea at global scale. This work highlights the important role played by plankton in the climate system.

Principal laboratories involved in the study

• CEA–Genoscope, Institut de Génomique
• Center for the Biology of Disease, VIB (Belgium)
• Department of Earth, Atmospheric and Planetary Sciences, Massachusetts Institute of Technology (USA)
• Department of Microbiology, The Ohio State University (USA)
• Department of Oceanography, University of Â鶹´«Ã½ School of Ocean and Earth Science and Technology (USA)
• EMBL (European Molecular Biology Laboratory) (Germany)
• Laboratoire d’Océanographie de Villefranche (CNRS/UPMC)
• Laboratoire “Evolution Paris Seine” (CNRS/UPMC), part of the Institut de Biologie Paris-Seine
• Laboratoire d’Informatique de Nantes Atlantique (CNRS/Université de Nantes/École des Mines de Nantes)
• Institut de Biologie, Ecole Normale Supérieure (CNRS/ENS Paris/INSERM)
• Institute for Chemical Research, Kyoto University (Japan)
• Institute of Marine Sciences (Spain)
• Laboratoire “Adaptation et Diversité en Milieu Marin” (CNRS/UPMC), Roscoff Biological Station
• Laboratoire “Génomique Métabolique” (CNRS/CEA/Université Evry-Val-d’Essonne)
• Laboratoire “Information Génomique et Structurale” (CNRS/AMU)
• Laboratoire de Météorologie Dynamique (CNRS/UPMC/Ecole Polytechnique/ENS Paris), part of IPSL
• Stazione Zoologica Anton Dohrn (Italy)
• University of Bremen (Germany)
• University of Maine (USA)

—By Marcie Grabowski