Sold on Symbiosis

A love of the ocean lured Nicole Dubilier into science; gutless sea worms and their nurturing bacterial symbionts keep her at the leading edge of marine microbiology.

By | July 1, 2015

NICOLE DUBILIER
Professor, Marine Biology, University of Bremen Director, Symbiosis Department
Max Planck Institute for Marine Microbiology Bremen, Germany
COURTESY OF NICOLE DUBILIER
Nicole Dubilier doesn’t have fond memories of her high school science classes. “Unlike many scientists who say they loved to dissect frogs and insects, I was not interested in science when I was young,” says Dubilier, director of the Symbiosis Department at the Max Planck Institute for Marine Microbiology in Bremen, Germany.

Dubilier grew up in Manhattan, where her exposure to nature was limited to Central Park. But, vacationing on Fire Island in the summer, she fell in love with the ocean and decided to become a marine biologist. “It wasn’t so much the biology,” she says. “There was absolutely nothing I found inspiring or interesting about biology class. It was my worst subject in school; it was about learning without understanding.”

Dubilier is unapologetic about her early science experience and emphasizes that an early and vivid interest in chemistry, physics, or biology is not a necessary prelude to a successful science career. “I actually don’t think it’s that important,” she says.

“I am just really interested in how two species come together: Why are they associated? What is the benefit?”

Her love of the ocean and its marine inhabitants led Dubilier to pursue a PhD in marine biology at the University of Hamburg. After completing her doctoral studies, she was still not sure she had the passion and stamina required to be an independent researcher. Dubilier says she was jealous of colleagues who said they thought of project ideas in the shower. “I thought of everything else but my research!” But a postdoc year spent in the lab of Harvard professor Colleen Cavanaugh studying symbiosis in gutless marine oligochaetes—a type of worm—cemented her love for research. “It was the first time I started to work in depth on marine symbiosis, and this topic evoked a deep, deep interest that is emotionally right next to marine biology for me. I am just really interested in how two species come together: Why are they associated? What is the benefit? And why these two species and not another two? Simple questions, really.”

Here, Dubilier talks about the research cruises that add elements of beauty and adventure to her work, how diving in Bermuda beats wading in freezing German waters, and how sheer persistence first landed her a coveted position at the Max Planck Institute.

Dubilier Discovers

Romantic notions. Growing up, ballet and the ocean were Dubilier’s two loves. At age 14, she chose not to continue with ballet because it would have meant quitting formal schooling. But the sea continued to draw her. “I had this unrealistic concept that I would spend half of my day diving, one-third doing research, and then the rest with the beautiful men I imagined on Jacques Cousteau’s ships! That was the concept of marine biology I had in my head.”

Back and forth. After her parents divorced when she was 13, Dubilier and her siblings were moved by her mother, a native of Berlin, to Wiesbaden, Germany. Every summer, she came back to New York to visit her father and developed what she calls “trans-Atlantic schizophrenia.” “A more positive way to put it is we had the best of both sides of the Atlantic,” she says.

Starting from the bottom. After graduating high school, Dubilier worked at a marine station on Helgoland, Germany’s only deep-sea island. “This was pivotal in my decision to pursue marine biology. Even though I had a menial job of cleaning fish tanks, there was something about the physical closeness of the ocean around me and working with marine organisms that inspired me. I got a basic, emotional satisfaction from it,” she says, and she immersed herself in learning the Latin names of marine species and understanding their taxonomy.

Butt bacteria. Dubilier received a bachelor’s degree in zoology from the University of Hamburg and then—always seeking travel opportunities—took a summer course in tropical marine ecology at a biological station in Bermuda. She went on to pursue a master’s degree in the University of Hamburg laboratory of Olav Giere, who studied the biology and ecology of marine oligochaete worms. Giere suggested that Dubilier study how a marine oligochaete from mud flats off the coast of Germany lives at low oxygen and high sulfide concentrations. Then Dubilier discovered that long, filamentous bacteria grew on the tail end of these worms, and became really excited. “For no reason, really,” she says, laughing. The observation turned into her first (single-author) publication. “Twenty years later I went back and looked at these funny bacteria [the worms] had on their tail ends, and we made fun of this and called it their butt bacteria.” Those bacteria are similar to the ones she studies now, found on and in invertebrates living in hydrothermal vents.

Researchers discovered deep-sea hydrothermal vents in 1977 in the Pacific Ocean off the coast of the Galapagos Islands, just a few years before Dubilier became interested in chemosynthetic symbiosis. “Suddenly there was a lot of interest in bacteria associated with invertebrates, and particularly those bacteria that use reduced sulfur compounds as an energy source, because the hydrothermal vent worms didn’t have a mouth or a gut and were being fed by their symbiotic bacteria that use hydrogen sulfide as a source of energy.”

Mucking around. For her graduate work at Hamburg, Dubilier spent a lot of time on the German coast, “freezing to death” she says. The silt and sand sediments off the coast exuded a rotten-egg smell from hydrogen sulfide, used by the bacteria living on the tail end of Tubificoides benedii, the inch-long marine oligochaete she studied for her PhD. Wading into the muddy water, Dubilier used a sieve to collect worms to bring back to the lab for analysis. “This was not the glorious image of diving I had envisioned. The sediments were so muddy that you could lose your rubber boots if you were not careful. The mud would end up in almost every opening in your body. That was where I swore that, after finishing my PhD, the next group of animals I would work on would live in warmer climates!”

Dubilier Dives In

Molecular biology for dummies. After completing her PhD in 1992, Dubilier was still not convinced research was for her. “It was clear to me that if you are not absolutely dedicated to your research, you are going to be very miserable. I had realized that I could not continue in this profession without being dedicated and excited about it.” To help her decide, Dubilier took a molecular biology course for marine biologists offered by the University of Southern California on Catalina Island. “It could have been molecular biology for dummies for all I knew about molecular biology! But it was taught by some of the best marine microbiologists who were just starting to use the newly developed molecular biology methods, including PCR.”

Warmer climes. When Dubilier was still a grad student, she met Colleen Cavanaugh at a Woods Hole course, and the Harvard professor, who had been among the first to characterize hydrothermal vent symbioses, suggested postdoctoral work in her lab. There Dubilier sequenced the 16S RNA genes—used as phylogenetic markers—of bacteria found on gutless marine worms, concluding that the worms harbored two symbionts. The two-to-three-centimeter-long worms Dubilier characterized are found in coral reef sediments in tropical environments such as Belize, Bermuda, and Australia. “The fieldwork was much better than during my PhD. These trips alone were magnificent.” With better tools, Dubilier’s lab later identified an additional three symbionts in these worms.

Back to Germany. After her postdoc, Dubilier returned to Germany along with her husband, an orthopedic surgeon. In 1995, she had funding from both Harvard and the University of Hamburg and began to knock on the door of the Max Planck Institute. In 1996, the Molecular Ecology Group welcomed Dubilier as a postdoctoral fellow. “They finally broke down and gave me a contract,” she says. “I was persistent to the point that they later told me they were worried I was going to be this super-annoying person once I arrived.” Dubilier decided to continue to work on the gutless oligochaetes because no one else in the world of marine symbiosis was working on their molecular biology and ecology. “They were small and difficult to work with because everything was complicated, including that they had more than one symbiont. So it was great not to have any competition, although for the first 5 to 10 years, almost no one cited my papers.”

Her own cheerleader. By 2001, Dubilier transitioned to a research associate position at the institute. That year, her laboratory published a paper describing the first example of two symbiotic bacteria that, rather than competing, provide each other with a growth advantage. In the gutless oligochaete Olavius algarvensis, the primary bacterial symbiont is a sulfur oxidizer that uses hydrogen sulfide as an energy source to fix carbon dioxide and provide organic carbon compounds to its host. Surprisingly, Dubilier could never measure hydrogen sulfide in the worm’s environment. This puzzle was solved when she discovered a second symbiont in the worms, a sulfate reducer. The sulfate reducer produces the hydrogen sulfide used by the primary symbiont, which in turn produces oxidized sulfur compounds for the sulfate reducer.

To prove that the second symbiont was producing hydrogen sulfide, Dubilier collaborated with Max Planck colleagues Dirk de Beer and Tim Ferdelman to design a laboratory experiment in which the bacteria were incubated with radiolabeled sulfate, which was then converted to radiolabeled sulfide by the bacteria. Because sulfide precipitates on silver, the team stuck silver needles into live worms and then observed if radiolabeled sulfide had precipitated on the needles by exposing the needles to autoradiography film. The New York Times covered the work because Dubilier had written to one of paper’s science writers. “I told him that my dad is a businessman and a golfer and does not understand my work and how cool would it be for him to read about it in The New York Times? And he said that had to be the best plug he had ever read.”

Evolution driver. In 2006, Dubilier’s lab produced the first detailed metagenomic analysis of a marine animal–microbe symbiotic community. The analysis demonstrated that four bacterial symbionts of O. algarvensis act as the energy source and excretory system for the invertebrate—the first example of such an adaptation among free-living marine animals. The work provided evidence of the worm’s evolution to a gutless animal that relies solely on its symbiotic relationships for both digestion and waste functions.

An unexpected finding. On a 2005 research cruise to the Mid-Atlantic Ridge to study hydrothermal vents that emitted high concentrations of hydrogen, Dubilier thought that the bacteria living on mussels in these vents might be using hydrogen as an energy source. Up until that point, there were only two known energy sources for chemosynthetic symbioses in hydrothermal vents: hydrogen sulfide and methane. Both gases, as well as hydrogen, are produced by geochemical processes in the hot hydrothermal vents. “Naively, I was not aware of the negative results on this. Thomas Pape from the MARUM in Bremen, also on the cruise, conducted a 24-hour experiment to measure hydrogen concentrations of the symbiosis community that suggested that hydrogen indeed was being consumed by these symbiotic bacteria. It took another five years to really piece the data together,” says Dubilier. The study, published in 2011, made the cover of Nature, and showed that hydrogen provides energy for symbioses in mussels and other hydrothermal vent animals. “Our work is at the crossroads of environmental microbiology and molecular microbiology. We use omics methods to form hypotheses but then validate them using physiology and imaging methods.” Using metaproteomics, the lab has also found evidence that carbon monoxide is used as an energy molecule in marine invertebrate symbioses. The lab has since uncovered physiological evidence that this is the case, and this study has just been accepted for publication.

Dubilier Divulges

Career-life balance. Dubilier says that she rarely mixes her work with her family. Her son and husband have come with her on several research expeditions to collect gutless worms in the Bahamas, Belize, and Australia, but research cruises—typically six weeks long—are restricted to scientists only. “I am not sure it’s a good thing for meetings or excursions to bring your kids along. If you’re there with a partner and kids at a meeting, you’re usually rushing home to take care of kids, and you don’t have time for some of the most important parts of a conference—the socializing. For myself, I question the integration of family with work, and whether it benefits your family or your work.”

Improv. “I loved and still love fieldwork. It’s completely independent work where you have to adjust to a situation immediately and to improvise. You need to be clear about what you want and to be able to deal with going out three times when things don’t work, and then if you’re lucky, on the fourth try, it might work out. I was also on the ocean, which was immensely satisfying. That mix of feeling that with a little forethought, afterthought, and engagement, that I could bring my work to a productive level, I always enjoyed.”

An American at heart. After her postdoc at Harvard, Dubilier and her husband, who had completed a research fellowship in orthopedic surgery during their stay in Boston, made a two-body decision to return to Germany. “I would like to have stayed, and that was when I really realized that I am an American at heart. But my husband is a German at heart, and he made the point, which I agreed with, that he would rather live in Europe and vacation in the U.S. than the other way around.”

Greatest Hits

  • Identified the first sulfate-reducing bacterial species as an obligate animal endosymbiont, as well as the first example of a symbiotic, syntrophic relationship that includes multiple symbionts within a marine host—two species, both living in O. algarvensis
  • Conducted the first detailed metagenomic analysis of an endosymbiotic microbial community in a eukaryotic marine host—a gutless worm (O. algarvensis) associated with four bacterial species that provide the animal with energy and waste clearance
  • Identified hydrogen as a third, previously unknown energy source for bacterium–animal symbioses, providing energy for mussels within deep-sea hydrothermal vents—the first new symbiotic chemical energy source discovered in 25 years
  • Provided the first combined metaproteomic and metabolomic analysis examining a host with multiple symbionts—the gutless marine worm O. algarvensis and four of its bacterial symbionts. The study also identified carbon monoxide as a previously unknown energy source for marine invertebrate symbiosis.
  • Organized the first Gordon conference on animal-microbe symbioses, which took place last month

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