An ocean odyssey

Single droplets of sea water are teeming with improbable forms of lifePHOTO: C. Guiguand/Tara Expeditions

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A journalist who spent six weeks chronicling life on board Tara reflects on the extraordinary outcomes from the expedition.

By Andres Peyrot

October 2011. I’m on night duty aboard the 36-metre schooner Tara as it glides across the Pacific Ocean, a black mirror that reflects the star-riddled sky above and hides everything that lies beneath its surface. For the next six weeks, I am here to observe the life and times of this unique research vessel as it explores some of the most mysterious parts of our planet. Tomorrow seems a long time away, but two things keep me awake: the smell of salt hanging in the air and a line from the song A Horse With No Name that keeps looping through my mind – “The ocean is a desert with its life underground and a perfect disguise above…”

EMBL's Eric Karsenti (far left) joins UN Secretary General Ban Ki-Moon on Tara's bow. PHOTO: J. Girardot/Tara Expeditions

Eric Karsenti (far left) joins UN Secretary General Ban Ki-Moon on Tara’s bow. PHOTO: J. Girardot/Tara Expeditions

Beneath the surface

At dawn, the deck is buzzing with scientists who comb through the upper ocean with thin nets, water pumps and a ‘rosette’, which traps water at different depths and measures its physical and chemical properties. I descend into the ‘dry lab’ cabin filled with microscopes and computer screens and find Jérémie Capoulade, an imaging expert then working as a postdoc at EMBL, who delicately places a drop of sampled water under a microscope.

Suddenly, the boat is caught in waves that turn the entire lab into a swinging pendulum. I look for the edge of a table, anything, to keep my balance, while Capoulade, seemingly unaware of the complete havoc around us, sways in time with his microscope, captivated by what he sees beneath the lens.

This single droplet is teeming with improbable forms of life: plankton, some so strange-looking that they were the inspiration for the creatures in the 1979 Hollywood film Alien. And as tiny and bizarre as they may seem, plankton represent nine-tenths of the living mass in the oceans and form the base of the food chain. Through photosynthesis, they generate half of the oxygen we breathe, draw carbon from the atmosphere to the deep sea, and play a crucial role in the global nitrogen cycle. Yet, despite their immense impact on the world’s environment, we know very little about these microorganisms.

Platynereis dumerilii, imaged during the expedition. IMAGE: Eric Roettinger/Tara Expeditions

Platynereis dumerilii, imaged during the expedition. IMAGE: Eric Roettinger/Tara Expeditions

The Tara Oceans project (2009–2013), unprecedented both in scale and ambition, set out to change this forever. While navigating seven seas and oceans, evading pirates, weathering storms and hand-fixing complex equipment, the scientists on board sampled all types of plankton and have thus generated a bounty of data for comprehensive studies of these tiny creatures. I knew that what we were doing on Tara was important. It is only recently, though, that I have come to realise just how important.

In May, researchers from EMBL and partner institutions reported the first findings from the analysis of these data in a package of five papers published in a special edition of Science, as well as publications in other journals cutting across many different fields. Their interdisciplinary work involved high-throughput sequencing, advanced imaging, big data storage management, bioinformatics and the very latest physical modelling technologies. “The data we collected enables researchers to look in unprecedented detail at the populations, environments and dynamics of the oceans’ vital life support system,” says EMBL’s Eric Karsenti, Tara Oceans’ Scientific Director and a senior author on the papers. “This is the first global description of the complete ecosystems.”

Five years ago, this was science fiction!

Shotgun DNA sequencing on the samples has provided the scientific community with a staggering 7.2 trillion bases of genetic code from entire populations of plankton – from tiny viruses 0.02 micrometers in size to animals measuring up to two millimeters, roughly the ratio of a golf ball to ten Olympic-sized swimming pools. “These organisms aren’t usually studied together and the techniques we’ve used aren’t usually combined together – our approach allows us to bridge the molecular to the planetary scale,” says Chris Bowler from the CNRS and another senior author on the papers. “This is the emergence of a new type of research in life sciences,” Karsenti adds, smiling, with an excited glint in his eyes. “Five years ago, this was science fiction!”

Tales from the high seas

“Together with a few adventurous colleagues, the first scientific meeting to plan the expedition was organised in Villefranche-sur-Mer in fall 2008. Inspired by the structure and functioning of EMBL, coordinators for various specialties were appointed. Specialists for the main domains of life (viruses, bacteria, archaea, protists and metazoans) were needed, as well as oceanographers, ecologists, molecular and cellular biologists, physicists and bioinformaticians, including experts on imaging, databases and sequencing.

“Each of the scientists involved in this early phase recruited additional colleagues in a wonderfully self-organised process. With input from the different disciplines, we determined sampling zones, organisms’ size fractions to be collected, and strategies for sample storage, handling and dispatching. Using a sophisticated bar coding system, high-quality environmental data were linked to biological samples.

“The early discussions were passionate and robust debates ensued. At times, we wondered whether we would make it. But with the increasing awareness of the exceptional scope of this project dedicated to the study, an entire biome at a planetary scale, a sense of great excitement and uniqueness started to diffuse throughout the growing consortium. In the end, it was only the collective enthusiasm and commitment of the individual participants that made Tara Oceans possible.”

Eric Karsenti, Tara Oceans’ Scientific Director

From this massive census of the sea, researchers have begun to tackle questions that explorers of yesteryear would not have even dreamed of asking: What types of plankton populate our oceans? How do they interact with one another and their environment? How will they react to climate change? How will all this affect us?

Charting millions of genes

At first glance, the labs at EMBL Heidelberg, a six-hour drive from the nearest coastline, might seem an unlikely place to take forward this endeavour. Yet it was here that Shinichi Sunagawa, a researcher in Peer Bork’s group, led a project to develop an Ocean Microbial Gene Catalogue – more than 40 million genes from microbial plankton, 80% of which are new to science. Pointing towards a huge diversity of unknown plankton found in different parts of the ocean, this genetic catalogue led to an important observation: temperature is the main environmental factor shaping microbial communities. Scientists can now begin to consider wider issues connected to this striking finding, such as the potential impact rising temperatures could have on these sensitive ecosystems, how this will affect the planet’s environment, and what might be done to better protect them.

It’s like a treasure box

Researchers are also aiming to assign functions to the genes in the catalogue. “It’s like a treasure box in which you may find further variants of genes that produce bioactive substances or antibiotic effects,” says Sunagawa. Some plankton have properties that exceed our own abilities. Diatoms, for example, are single-celled organisms that synthesise a protective layer of glass in the chilly temperatures of the deep, a material that humans are only capable of producing using extreme heat. It would be exciting to identify which genes are responsible for such an astonishing ability!

Learning from life

Diatoms belong to the most diverse kingdom of life, eukaryotes, which are organisms whose DNA is coiled within a nucleus. This complex and stable cell structure enabled the evolution of multicellular beings, like us, to form. It is perhaps this legacy that inspired Colomban de Vargas, a scientist at the Roscoff Marine Biological Station in Brittany, France, to focus his research on ocean eukaryotes. The incredible diversity he observed with his team – one hundred times more than previously known – challenges the classical division of plankton into phyto- and zooplankton.

“Protists, which account for two-thirds of the eukaryotes discovered, don’t belong to either plants or animals,” explains de Vargas. Researchers have identified a total of 150 000 genetic types of protists from groups that had no match in a family tree of previously catalogued eukaryotes, a third of which could not even be classified. And one of the most fascinating discoveries for me is that underlying this hyper-diversification in marine plankton is their complex interactions.

The expedition uncovered an incredible diversity of planktonic beings. IMAGES: Christian Sardet/Tara Expeditions

The expedition uncovered an incredible diversity of planktonic beings. IMAGES: Christian Sardet/Plankton Chronicles

Community dynamics

On Tara, scientists nicknamed the specimens they found under the microscope with titles such as Hubert the protist and Dana the diatom. Behind their humour, I did not suspect the full extent of ‘social’ interactions that occur in our oceans. Step forward the Oceanic Interactome, a sort of planktonic Facebook that tells us which plankton are ‘friends’ and are always found together and which are not. Developed by a team led by Gipsi Lima-Mendez, a postdoc in Jeroen Raes’ group at the University of Leuven, researchers were able to reveal the remarkable impacts that some organisms have on community structures.

One particularly astonishing interaction came from an unlikely partnership between a photosynthetic microalgae living inside a flatworm. Using computer-generated models and advanced microscopy, the team were able to predict and confirm that the microalgae, in order to hide from predators, takes up residence inside the flatworm – and in exchange synthesises nutrients to feed its host. “Ocean interaction is far from ‘survival of the fittest’,” explains Karsenti. “Eighty percent of interactions between organisms in the ocean are positive: most organisms help one another thrive. It can change the way we look at evolution.”

Mapping new viruses

The most elusive plankton in the Interactome are also the most abundant – viruses, which are so small that we could not actually see them with the microscopes on board Tara. Ten million of them can squeeze into a single drop of seawater but their impact is enormous: they shape the populations they infect, drive evolution by transferring genes to different species, and influence the global cycling of nutrients, organic matter and atmospheric gases. Remarkably, a study led by Jennifer Brum, a postdoc in Matthew Sullivan’s group at the University of Arizona, identified more than 5000 viral populations, of which only 1% could be found in existing databases. Put another way, it’s as if 800 new planets were discovered in our Solar System, beyond the eight we already know.

“The challenges ahead will be to determine which organisms each of these viruses infects,” explains Patrick Wincker, Head of the Genoscope, the French National Sequencing Center that collaborated on the research. Importantly, the team also observed comparable local and global viral diversity, supporting the ‘seed-bank’ theory whereby viral communities are passively transported via oceanic currents and reshaped locally.

It can change the way we look at evolution

Such an understanding of oceanic currents is essential to the study of plankton distribution in our oceans. For some time, scientists hypothesised that plankton communities from the Indian Ocean were injected into the South Pacific by a peculiar current called the Aghulas rings – gigantic eddies that swirl around the tip of South Africa and transport plankton communities towards Brazil.

Not so, found a team lead by Emilie Villar, a postdoc in Pascal Hingamp’s group at the CNRS, after studying the fate of the microorganisms trapped inside these rings. “Plankton are subject to five degrees cooling and intense vertical mixing, thus limiting the species that manage to cross,” explains Daniele Iudicone, from the Stazione Zoologica Anton Dohrn in Naples, Italy. This ‘cold-wash cycle’ constitutes a fascinating case study of how planktonic ecosystems evolve in response to variations in their environment.

Navigating data

“Collectively, these studies give us a time zero reference point from which to monitor the health of our oceans in the future,” Guy Cochrane, Head of the European Nucleotide Archive at EMBL-EBI explains. “The data we have available represents 11.5 Terabytes, which is larger than the Wikipedia footprint.” The Tara Oceans consortium now invites the international scientific community to jump on board and tap into these huge reserves of data that will remain available as Cochrane notes, to “researchers working in different fields, for decades to come, when they think to ask questions that we didn’t think to ask now.” To some involved in the expedition this will come as little surprise: after all, scientists are still working with samples that Charles Darwin collected during his 1823 expedition on board the HMS Beagle!

The data we have available is larger than the Wikipedia footprint

With such a dizzying amount of samples, information and observations, one might think that grand scientific projects such as this are the product of a highly rationalised structure. But for Karsenti, “it usually starts with a hazy idea, a dream.” Stefanie Kandels-Lewis, in charge of scientific operations and logistics for Tara Oceans, adds, “It’s the dedication and the adrenaline that made it happen and kept us going.” Tara’s oceanic odyssey started with uncertainties and ended up revolutionising the way researchers think about plankton, allowing these tiny creatures to be studied on a planetary scale.

Tales from the high seas

“Working on Tara Oceans required you to be very flexible and creative. At each stopover, there was a new hurdle and throughout the expedition there was just about as much planning to do, as it is possible to imagine! One of the best aspects for me was working directly with the unique group of people involved – there was a fantastic energy, people were highly motivated and we were all riding on a wave of adrenaline.

“Looking back, the biggest achievement of Tara Oceans is the integration of all the data collected: scientists from such a broad range of disciplines trying to make sense of the information and interpret the results. It brought together people from very different fields that often work in very different ways. They had to somehow find a common language to communicate, and that’s the beauty of this – they did it!

“Researchers have seen their discipline from new angles, asking new questions they would not have thought about before. The team has spent a lot of time at sea together, as well as convening at many different meetings around the world – we are friends as well as colleagues, and a great community has built up around this dream. I’m incredibly proud of what we’ve achieved together.”

Steffi Kandels-Lewis, Scientific Operations Manager