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Diversity of the Global Ocean Microbiome

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News

Diversity of the Global Ocean Microbiome

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A nearly four-year expedition to sample metagenomes from plankton living in the world's waters has catalogued more than 35,000 marine denizens, more than 40 million genes belonging to them, and described interactions between the various organisms living in the topmost oceanic layer.

The Tara Oceans consortium set out on a 110-foot research schooner in 2009 to sample plankton from 210 sites around the globe and presented the results from its November 2013 data freeze in five Science papers today. As the researchers reported, they generated more than 7 trillion basepairs from 243 samples enriched for viruses, prokaryotes, and picoeukaryotes. They found more than 5,000 viral populations and about 150,000 genetic types of eukaryotes, and described how these various components of the oceanic ecosystem come together.

"Plankton, in fact, is much more than just food for the whales," noted Chris Bowler, research director at the French National Center for Scientific Research (CNRS) and an author on the set of studies, during a press teleconference this week. "Although tiny, these organisms are a vital part of the Earth's life support system providing half for the oxygen generated each year on Earth by photosynthesis and lying at the base of marine food chains on which all other ocean life depends."

As they sailed around the world — through the Mediterranean Sea to Indian Ocean and over to the Atlantic, Southern, and Pacific Oceans — consortium researchers collected plankton ranging in size from 0.02 micrometers to a few millimeters, along with physical and chemical data from the 210 sampling sites. The researchers focused on the sunlit upper layer of the ocean, down to about 200 meters, though they did collect some samples from the twilight zone. The data freeze covered by this suite of papers includes 579 samples collected at 75 different stations.

By drawing on a subset of the Tara Oceans data, researchers led by the European Molecular Biology Laboratory's Peer Bork generated a global Ocean Microbial Reference Gene Catalog with more than 40 million representative genes from a wide swathe of viruses, prokaryotes, and picoeukaryotes.

This catalog, Bork and his colleagues noted, includes more than four times the number of genes than the human gut microbial reference gene catalog contains.

Most of the genes in the ocean catalog appear to be prokaryotic in origin and the eukaryotic genes that are present hail mainly from protists.

Some 81 percent of the genes Bork and his colleagues identified were unique to the Tara Ocean samples, underscoring, they said, how much of ocean life remains to be studied. Gene novelty, they noted, increased as the ocean depth at which their samples were obtained increased, as did taxonomic and functional richness.

Temperature also appeared to be a key environmental driver of community composition, as the researchers estimated it could account for some 86 percent of variance.

"That means that at the surface layer, for example, geographic distance has less impact on the community composition than temperature, and that has implications … given the rise of water temperature and climate, et cetera," Bork said.

Surprisingly to the researchers, when they compared the core functions of the genes making up the ocean microbiome to those in the human gut microbiome — one of the few widely studied microbiomes — they found that the most of prokaryotic gene abundance in the ocean and in the human gut could be ascribed to a shared functional core.

Viruses are one oft-overlooked source of biological diversity in the oceans, and the University of Arizona's Matthew Sullivan and his colleagues developed the Tara Oceans Viromes dataset based on 43 samples from 26 locations in the upper ocean.

While this dataset is restricted to dsDNA viruses lurking in the waters, they uncovered more than 5,000 viral populations. Only 39 of those populations were similar to known viruses.

"This means that the most abundant and widespread viral populations in the oceans have yet to be characterized, but now we have an idea of what viruses are important targets for future investigations, " Arizona's Jennifer Brum, first author of the ocean viral community paper, said.

She and her colleagues also found that viral genetic diversity at any given location is high, but that the global diversity of ocean-dwelling viruses is about the same as what's seen in any individual sample.

This suggested to the researchers that viruses that widely distributed throughout the global oceans — likely by major ocean currents — and then local environmental conditions influence community composition.

Meanwhile, researchers led by Eric Karsenti at CNRS focused on the taxonomic and ecological diversity of medium-sized eukaryotes. They generated about 766 million raw rDNA reads from 334 plankton samples obtained at 47 sites at two water-column depths. Using a meta-barcode-based approach, they grouped those reads, once filtered, into about 110,000 operational taxonomic units.

This, Karsenti and his colleagues found, was enough to approach saturation at both a local and global scale.  Based on this, they extrapolated that there are some 150,000 OTUs making up the ocean microbiome, vastly more than the 11,200 or so formally described marine eukaryotic species.

In addition, about a third of these OTUs couldn’t be assigned to any known eukaryotic group, and they found that a significant portion of the biodiversity they captured belongs to heterotrophic protists, especially parasites or symbiotic hosts, which, they said highlights the interconnections among ocean life.

Indeed, environmental factors like temperature, phosphate, and nitrogen dioxide don't fully explain plankton community structure, according to KU Leuven's Jeroen Raes and colleagues.

Based on 313 plankton samples collected at various depths at 68 stations across the global oceans as well as environmental data taken at those sites, Raes and colleagues constructed a global network of taxon-taxon and taxon-environment interactions.

"So essentially what we did in our [paper] was to derive the social network of the oceans, who is living with whom and how the environment shapes these connections," first author Gipsi Lima-Mendez from Leuven said.

These interactions are marked by competition, collaboration, parasitism, and predation, she noted, and are just as important as environmental influences.

For instance, based on their interactome data, she and her colleagues predicted a photosymbiotic interaction between an acoel flatworm and a green microalga, a prediction they were able to confirm using microscopy and other tools.

Finally, consortium researchers showed that when plankton communities mix — such as in the Agulhas rings that form when Indian Ocean waters leak into the South Atlantic and that play an important role in climate regulation — there appears to be a broad similarity among the populations. However, they noted that there is a restructuring of the community at a finer scale, especially based on organism size, as they travel from the Indian to South Atlantic Ocean.

Environmental selection at this chokepoint, Daniele Iudicone from Stazione Zoologica in Naples and his colleagues said, may thus block plankton dispersal.

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