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Science

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Microbes are dominant drivers of biogeochemical processes, yet drawing a global picture of functional diversity, microbial community structure, and their ecological determinants remains a grand challenge. We analyzed 7.2 terabases of metagenomic data from 243 Tara Oceans samples from 68 locations in epipelagic and mesopelagic waters across the globe to generate an ocean microbial reference gene catalog with >40 million nonredundant, mostly novel sequences from viruses, prokaryotes, and picoeukaryotes. Using 139 prokaryote-enriched samples, containing >35,000 species, we show vertical stratification with epipelagic community composition mostly driven by temperature rather than other environmental factors or geography. We identify ocean microbial core functionality and reveal that >73% of its abundance is shared with the human gut microbiome despite the physicochemical differences between these two ecosystems. Authors: Shinichi Sunagawa, Luis Pedro Coelho, Samuel Chaffron, Jens Roat Kultima, Karine Labadie, Guillem Salazar, Bardya Djahanschiri, Georg Zeller, Daniel R. Mende, Adriana Alberti, Francisco M. Cornejo-Castillo, Paul I. Costea, Corinne Cruaud, Francesco d'Ovidio, Stefan Engelen, Isabel Ferrera, Josep M. Gasol, Lionel Guidi, Falk Hildebrand, Florian Kokoszka, Cyrille Lepoivre, Gipsi Lima-Mendez, Julie Poulain, Bonnie T. Poulos, Marta Royo-Llonch, Hugo Sarmento, Sara Vieira-Silva, Céline Dimier, Marc Picheral, Sarah Searson, Stefanie Kandels-Lewis, , Chris Bowler, Colomban de Vargas, Gabriel Gorsky, Nigel Grimsley, Pascal Hingamp, Daniele Iudicone, Olivier Jaillon, Fabrice Not, Hiroyuki Ogata, Stephane Pesant, Sabrina Speich, Lars Stemmann, Matthew B. Sullivan, Jean Weissenbach, Patrick Wincker, Eric Karsenti, Jeroen Raes, Silvia G. Acinas, Peer Bork, Emmanuel Boss, Chris Bowler, Michael Follows, Lee Karp-Boss, Uros Krzic, Emmanuel G. Reynaud, Christian Sardet, Mike Sieracki, Didier Velayoudon

Marine plankton support global biological and geochemical processes. Surveys of their biodiversity have hitherto been geographically restricted and have not accounted for the full range of plankton size. We assessed eukaryotic diversity from 334 size-fractionated photic-zone plankton communities collected across tropical and temperate oceans during the circumglobal Tara Oceans expedition. We analyzed 18S ribosomal DNA sequences across the intermediate plankton-size spectrum from the smallest unicellular eukaryotes (protists, >0.8 micrometers) to small animals of a few millimeters. Eukaryotic ribosomal diversity saturated at ~150,000 operational taxonomic units, about one-third of which could not be assigned to known eukaryotic groups. Diversity emerged at all taxonomic levels, both within the groups comprising the ~11,200 cataloged morphospecies of eukaryotic plankton and among twice as many other deep-branching lineages of unappreciated importance in plankton ecology studies. Most eukaryotic plankton biodiversity belonged to heterotrophic protistan groups, particularly those known to be parasites or symbiotic hosts. Authors: Colomban de Vargas, Stéphane Audic, Nicolas Henry, Johan Decelle, Frédéric Mahé, Ramiro Logares, Enrique Lara, Cédric Berney, Noan Le Bescot, Ian Probert, Margaux Carmichael, Julie Poulain, Sarah Romac, Sébastien Colin, Jean-Marc Aury, Lucie Bittner, Samuel Chaffron, Micah Dunthorn, Stefan Engelen, Olga Flegontova, Lionel Guidi, Aleš Horák, Olivier Jaillon, Gipsi Lima-Mendez, Julius Lukeš, Shruti Malviya, Raphael Morard, Matthieu Mulot, Eleonora Scalco, Raffaele Siano, Flora Vincent, Adriana Zingone, Céline Dimier, Marc Picheral, Sarah Searson, Stefanie Kandels-Lewis, , Silvia G. Acinas, Peer Bork, Chris Bowler, Gabriel Gorsky, Nigel Grimsley, Pascal Hingamp, Daniele Iudicone, Fabrice Not, Hiroyuki Ogata, Stephane Pesant, Jeroen Raes, Michael E. Sieracki, Sabrina Speich, Lars Stemmann, Shinichi Sunagawa, Jean Weissenbach, Patrick Wincker, Eric Karsenti, Emmanuel Boss, Michael Follows, Lee Karp-Boss, Uros Krzic, Emmanuel G. Reynaud, Christian Sardet, Matthew B. Sullivan, Didier Velayoudon

Species interaction networks are shaped by abiotic and biotic factors. Here, as part of the Tara Oceans project, we studied the photic zone interactome using environmental factors and organismal abundance profiles and found that environmental factors are incomplete predictors of community structure. We found associations across plankton functional types and phylogenetic groups to be nonrandomly distributed on the network and driven by both local and global patterns. We identified interactions among grazers, primary producers, viruses, and (mainly parasitic) symbionts and validated network-generated hypotheses using microscopy to confirm symbiotic relationships. We have thus provided a resource to support further research on ocean food webs and integrating biological components into ocean models. Authors: Gipsi Lima-Mendez, Karoline Faust, Nicolas Henry, Johan Decelle, Sébastien Colin, Fabrizio Carcillo, Samuel Chaffron, J. Cesar Ignacio-Espinosa, Simon Roux, Flora Vincent, Lucie Bittner, Youssef Darzi, Jun Wang, Stéphane Audic, Léo Berline, Gianluca Bontempi, Ana M. Cabello, Laurent Coppola, Francisco M. Cornejo-Castillo, Francesco d'Ovidio, Luc De Meester, Isabel Ferrera, Marie-José Garet-Delmas, Lionel Guidi, Elena Lara, Stéphane Pesant, Marta Royo-Llonch, Guillem Salazar, Pablo Sánchez, Marta Sebastian, Caroline Souffreau, Céline Dimier, Marc Picheral, Sarah Searson, Stefanie Kandels-Lewis, , Gabriel Gorsky, Fabrice Not, Hiroyuki Ogata, Sabrina Speich, Lars Stemmann, Jean Weissenbach, Patrick Wincker, Silvia G. Acinas, Shinichi Sunagawa, Peer Bork, Matthew B. Sullivan, Eric Karsenti, Chris Bowler, Colomban de Vargas, Jeroen Raes

Agulhas rings provide the principal route for ocean waters to circulate from the Indo-Pacific to the Atlantic basin. Their influence on global ocean circulation is well known, but their role in plankton transport is largely unexplored. We show that, although the coarse taxonomic structure of plankton communities is continuous across the Agulhas choke point, South Atlantic plankton diversity is altered compared with Indian Ocean source populations. Modeling and in situ sampling of a young Agulhas ring indicate that strong vertical mixing drives complex nitrogen cycling, shaping community metabolism and biogeochemical signatures as the ring and associated plankton transit westward. The peculiar local environment inside Agulhas rings may provide a selective mechanism contributing to the limited dispersal of Indian Ocean plankton populations into the Atlantic. Authors: Emilie Villar, Gregory K. Farrant, Michael Follows, Laurence Garczarek, Sabrina Speich, Stéphane Audic, Lucie Bittner, Bruno Blanke, Jennifer R. Brum, Christophe Brunet, Raffaella Casotti, Alison Chase, John R. Dolan, Fabrizio d’Ortenzio, Jean-Pierre Gattuso, Nicolas Grima, Lionel Guidi, Christopher N. Hill, Oliver Jahn, Jean-Louis Jamet, Hervé Le Goff, Cyrille Lepoivre, Shruti Malviya, Eric Pelletier, Jean-Baptiste Romagnan, Simon Roux, Sébastien Santini, Eleonora Scalco, Sarah M. Schwenck, Atsuko Tanaka, Pierre Testor, Thomas Vannier, Flora Vincent, Adriana Zingone, Céline Dimier, Marc Picheral, Sarah Searson, Stefanie Kandels-Lewis, , Silvia G. Acinas, Peer Bork, Emmanuel Boss, Colomban de Vargas, Gabriel Gorsky, Hiroyuki Ogata, Stéphane Pesant, Matthew B. Sullivan, Shinichi Sunagawa, Patrick Wincker, Eric Karsenti, Chris Bowler, Fabrice Not, Pascal Hingamp, Daniele Iudicone

Viruses influence ecosystems by modulating microbial population size, diversity, metabolic outputs, and gene flow. Here, we use quantitative double-stranded DNA (dsDNA) viral-fraction metagenomes (viromes) and whole viral community morphological data sets from 43 Tara Oceans expedition samples to assess viral community patterns and structure in the upper ocean. Protein cluster cataloging defined pelagic upper-ocean viral community pan and core gene sets and suggested that this sequence space is well-sampled. Analyses of viral protein clusters, populations, and morphology revealed biogeographic patterns whereby viral communities were passively transported on oceanic currents and locally structured by environmental conditions that affect host community structure. Together, these investigations establish a global ocean dsDNA viromic data set with analyses supporting the seed-bank hypothesis to explain how oceanic viral communities maintain high local diversity. Authors: Jennifer R. Brum, J. Cesar Ignacio-Espinoza, Simon Roux, Guilhem Doulcier, Silvia G. Acinas, Adriana Alberti, Samuel Chaffron, Corinne Cruaud, Colomban de Vargas, Josep M. Gasol, Gabriel Gorsky, Ann C. Gregory, Lionel Guidi, Pascal Hingamp, Daniele Iudicone, Fabrice Not, Hiroyuki Ogata, Stéphane Pesant, Bonnie T. Poulos, Sarah M. Schwenck, Sabrina Speich, Celine Dimier, Stefanie Kandels-Lewis, Marc Picheral, Sarah Searson, , Peer Bork, Chris Bowler, Shinichi Sunagawa, Patrick Wincker, Eric Karsenti, Matthew B. Sullivan

On 8 June, the United Nations Educational, Scientific and Cultural Organization (UNESCO) celebrates World Oceans Day, a fitting occasion to remind ourselves of the essential role of the oceans in making Earth a habitable planet. We have had an official day of celebration for the oceans only since December 2008. In contrast, Earth Day has been celebrated every year since 1970. Conceived by U.S. Senator Gaylord Nelson in the aftermath of the 1969 Santa Barbara oil spill, Earth Day became a focus for the growing environmental movement (it became an international event in 1990) and the catalyst that led to the Clean Air, Clean Water, and Endangered Species Acts in the United States. Imagine what might be accomplished if World Oceans Day could similarly inspire actions for improving the state of the oceans worldwide. Author: Marcia McNutt

In science news around the world, the United States' Advanced Research Projects Agency-Energy, part of the Department of Energy, announces a slew of projects that it hopes will break the logjam in fusion research, the National Academies launches an initiative to discuss the ethically fraught topic of human embryo gene editing, and German scientists join other genetically modified (GM) foods proponents in an unusual gamble: urging the country's government to label all GM products to convince people there's nothing to be afraid of. Also, agriculturalist Cary Fowler discusses his work to protect the genetic diversity of the world's crops, featured in the upcoming documentary Seeds of Time. And researchers are closing in on a long-standing goal of engineering genes into yeast that will enable the microbes to make opiates—which, policy experts worry, could make it too easy for narcotics dealers to manufacture the drugs as well.

One of the fastest growing trees, poplars, may rely on tiny microbes in their leaves to fuel their growth. For more than a decade, a lone researcher has been building a case for nitrogen fixation by bacteria living in poplar leaves. There have been many claims of nitrogen fixation in plants outside nodules where it was known to occur for more than a century. Newly reported experiments involving rice grown on nitrogen-poor soil and poplar cuttings put in air with heavy nitrogen should help convince the skeptics. In addition, another researcher finds evidence of nitrogen fixation in the needles of limber pine and Englemann spruce. If these bacteria prove to be widespread, they could be used to boost crop production on marginal soils. Author: Elizabeth Pennisi

Vietnam's Mekong River delta—the world's third largest delta—is sinking, putting some 20 million people and vast swaths of fertile farmland at risk. Recent research has found that the delta, which covers some 55,000 square kilometers and sits about 2 meters above sea level, is subsiding at rates of 1 to 4.7 centimeters per year. Among the culprits: levees that prevent sediment from spilling out of rivers and collecting in the delta, and some 1 million wells drilled since the 1980s for drinking and agriculture. If groundwater depletion continues at present rates, researchers estimate, the delta could sink by nearly a meter by midcentury. Now, an alliance of Vietnamese and Dutch scientists is trying to get ahead of the problem. They met in Vietnam recently to launch the Rise and Fall project, a $1 million, 5-year effort to better understand what's driving Mekong delta subsidence and develop strategies to reverse it. "We know virtually nothing about what's beneath our feet," said geographer Philip Minderhoud, a co-leader of the project and doctoral candidate at Utrecht University in the Netherlands, during the 11 March gathering. New studies aim to change that. Author: Charlie Schmidt

Fifteen years after learning about the medical benefits of cannabis from patients in a sickle cell clinic in Kingston, Mark Ware is studying the drug on a grand scale. A pain management researcher at McGill University Health Centre in Montreal, Canada, he directs the Quebec Cannabis Registry, a new, one-of-a-kind database that aims to gather information on every patient prescribed marijuana in the province over the next 10 years—an estimated 3000 in all. By collecting data on symptoms, dosage, improvement, and side effects, the registry, launched on 11 May and funded by a grant from the nonprofit Canadian Consortium for the Investigation of Cannabinoids, aims to fill gaps in knowledge about the efficacy and safety of medical marijuana. Even as more and more states and countries legalize pot for medical purposes, clinical trials of smoked cannabis remain rare. "Decisions [about medical marijuana] are being made at the ballot box instead of in the laboratories," says Raul Gonzalez, a psychologist at Florida International University in Miami who studies cognitive effects of cannabis use in HIV/AIDS patients. Author: Lizzie Wade

A young man who lived in Romania 37,000 to 42,000 years inherited as much as one-tenth of his DNA from a Neandertal ancestor, according to a new study of ancient DNA. Ever since spelunkers found a robust jawbone in a cave in Romania in 2002, some paleoanthropologists have thought that its huge wisdom teeth and other features resembled those of Neandertals even though the fossil was a modern human. Now, by sequencing informative parts of the Romanian man's genome, an international team of researchers has found that he had inherited 4.8% to 11.3% of his genome from a Neandertal who lived only 200 years or so previously, according to a talk this month at Cold Spring Harbor Laboratory in New York. The finding confirms that Neandertals interbred with modern humans more than once, and it is the first evidence that the two types of humans had a liaison in Europe. Author: Ann Gibbons

Surrounded by six Nobel laureates, European Commission President Jean-Claude Juncker announced his long-awaited plan to restructure the commission's scientific advice process on 13 May. In the commission's new Science Advice Mechanism, a high-level group of seven scientists will channel the input of national academies and learned societies to give the commission the best scientific advice. When Juncker took office last November, he didn't renew the position of chief scientific adviser, which some scientists took as a sign of disregard for science. Last week's announcement provided critics with some reassurance, but many details remain to be worked out, including how the high-level group will operate effectively. Author: Tania Rabesandratana

In the 1950s, researchers observed that when the circulation of a young mouse is connected to an old mouse, the elderly animal seems to be rejuvenated. Since 2005, a handful of labs have been hotly pursuing the molecules responsible, hoping to harness them to slow or reverse aging in people. One in particular stood out: a protein found in young blood known as GDF11. In several high-profile papers, two of them published last year in Science, a Harvard University team reported that GDF11 levels decline in older animals, and that replacing it rebuilds muscles, the brain, and the heart. But work described this week in Cell Metabolism by a Novartis team challenges GDF11's rejuvenating powers. Their paper casts doubt on the assays used in the earlier research and suggests that GDF11 actually inhibits muscle regeneration. Author: Jocelyn Kaiser

Antibiotics face an unfortunate paradox: Though we desperately need new drugs to combat the growing threat of resistant bacteria, their discovery and development has ground to a crawl. A series of financial, scientific, and regulatory setbacks have driven companies out of the field, and many of the investors who could help get new drug candidates to the clinic are skeptical that such drugs can be profitable. Now, some are heralding new signs of life, including the return of a few pharmaceutical superpowers. But will desperate moves by governments to entice companies and researchers be enough to spring the next generation of antibiotics from the lab? Author: Kelly Servick

The quest for fusion energy is more than 60 years old and the current great hope, the $18 billion ITER reactor, won't hit its stride until 2027 at the earliest. Surely there is a quicker and cheaper route. Behold the spherical tokamak, a plumped-up version of the mainstream tokamak reactor shaped more like a cored apple than the traditional doughnut. That simple shape change could open the way to a fusion power plant that would match ITER's promise, without the massive scale. The world's two front-rank machines—in the United States and the United Kingdom—are both being upgraded with stronger magnets and more powerful heating systems. Soon they will switch on and heat hydrogen fuel to temperatures much closer to those needed for generating fusion energy. If they perform well, spherical tokamaks could change the shape of fusion's future. Author: Daniel Clery

Sexual dimorphism of testosterone (T) in elite athletes was at the center of a recent case at the “Supreme Court of Sport,” the Court of Arbitration for Sport in Switzerland, after teenage Indian sprinter Dutee Chand challenged a sports policy regulating competition eligibility of women with naturally high T. The idea of a “sex gap” in T is a cornerstone of this policy (1). Policymakers infer that men's higher T is the “one factor [that] makes a decisive difference” between men's and women's athletic performances (2)—so that women with naturally high T may unfairly enjoy a “massive androgenic advantage” over other women athletes (2). We report on an emerging scientific debate about whether the sex gap in T applies to elite athletes. Authors: Katrina Karkazis, Rebecca Jordan-Young

Imagine a world in which your smartphone can read your mind. Just at the moment that you decide to move your finger to delete a message, it is already gone. This sounds like science fiction, but for one human in California, this fantasy is becoming reality. On page 906 of this issue, Aflalo et al. (1) report the case of a tetraplegic individual (called “EGS”) who volunteered to have his brain implanted with two small silicon chips that allow researchers to read his intentions directly from his brain activity. The chips—initially developed at the University of Utah (2) and now commercially available and approved for human use by the U.S. Food and Drug Administration—consist of a matrix of 96 microscopic electrodes that can record the activity of about 100 nerve cells at the same time. Authors: J. Andrew Pruszynski, Jörn Diedrichsen

Lanthanides are used in items such as hybrid-car and smartphone batteries, magnets, and catalytic converters. Deceptively referred to as rare-earth elements (REEs), they are relatively abundant in Earth's crust but highly insoluble and scarce in pure form, requiring harsh extraction methods for purification. In China, lanthanides have been added to fertilizers and animal feed stocks to promote growth, although the growth of some crops is inhibited by lanthanides (1). Increased exposure to lanthanides has raised concerns that consumption of these elements in food or polluted water may have a negative impact on animals, including humans (2). However, recent studies have discovered that lanthanides are very important to a specialized group of bacteria that play a vital role in global carbon cycling. Authors: Elizabeth Skovran, Norma Cecilia Martinez-Gomez

Amines, a collective name for compounds that contain one or more nitrogen atoms, and their derivatives make up the overwhelming majority of drug molecules and agrochemicals, as well as many compounds that are produced by plants and living organisms (i.e., natural products) (1, 2). Not surprisingly, organic chemists spend a considerable amount of time with the synthesis and late-stage functionalization of amines. On page 886 of this issue, Gui et al. (3) report a highly innovative iron-catalyzed cross-coupling of olefins with nitroarenes, both of which are readily available and inexpensive, to afford bulky secondary arylamines that are either very difficult to obtain or inaccessible with existing methods. Author: László Kürti

A bewildering swirl of tiny creatures dominates life in the oceans. More numerous than the stars in the universe, these organisms serve as the foundation of all marine food webs, recycling major elements and producing and consuming about half the organic matter generated on Earth each year (1). In this issue, five research articles from the Tara Oceans expedition (2–6) provide a vivid, potentially transformative view of the genetic diversity and interconnectivity of these unseen marine communities of viruses, bacteria, archaea, single-celled eukaryotes, and small planktonic animals (see the figure). Together, these studies deliver compelling evidence for extensive networks of previously hidden biological interactions in the sea. Authors: E. Virginia Armbrust, Stephen R. Palumbi

Tumors have a life history (1, 2). A tumor consists of a dominant cell clone containing mutations in key cancer genes called “drivers,” together with smaller clones that descended from it but then diverged by accumulating different drivers. Other mutant clones appeared and vanished according to the selection pressures acting upon them or by neutral drift; the resulting diversity confers the means to escape clinical treatment (3). The stepwise accumulation of genetic and epigenetic alterations roughly parallels the clinical progression from normal tissue to precancer, cancer, and metastasis. It is widely assumed that driver mutations occur infrequently in long-lived lineages of cells (2), and that most arise in cancerous tissue that is too small to be clinically detectable. On page 880 of this issue, Martincorena et al. (4) overthrow both assumptions and reveal that sun-exposed normal skin is already a polyclonal quilt of driver mutations subjected to selection—a field of preprocancers, as it were—that nevertheless functions as a skin. Author: Douglas E. Brash

In August 2003, hundreds of Parisians returned from their summer holidays to an unholy smell. Ascending the stairs in their apartment buildings, they found the source: dead bodies. Between August 1st and 20th, a heat wave baked Europe, and nearly 15,000 people died in France alone. Fatal Isolation is a social autopsy of those deaths. Author: Laura Stark

Reviewer Michael Koeris is an unabashed proponent of bacteriophages and self-confessed "phage fanboy". As such, he welcomes this this "guide to the (phage) universe," which traces the infection strategies, replication mechanisms, and recent findings related to representative phages from a wide range of classes. Author: Michael Koeris

Striking close-up photos and micrographs take center stage in this striking book, revealing the dazzling diversity of these tiny creatures.

A listing of books received at Science during the week ending 15 May 2015.

Author: Robert Pollack

Authors: José Vicente López-Bao, Petra Kaczensky, John D. C. Linnell, Luigi Boitani, Guillaume Chapron

Author: Bing Xue

Chen et al. (Reports, 16 January 2015, p. 248) argued that early Tibetan agriculturalists pushed the limits of farming up to 4000 meters above sea level. We contend that this argument is incompatible with the growing requirements of barley. It is necessary to clearly define past crop niches to create better models for the complex history of the occupation of the plateau. Authors: Jade d’Alpoim Guedes, R. Kyle Bocinsky, Ethan E. Butler

Guedes et al. have drawn attention to a mismatch between the predictions of their “thermal niche model” and the records we have published of early barley finds in the northeastern Tibetan Plateau. Here, we consider how that mismatch usefully draws our attention to the additional variables that may account for it—namely, variations in genetic expression and agricultural practice. Authors: Guanghui Dong, Dongju Zhang, Xinyi Liu, Fengwen Liu, Fahu Chen, Martin Jones

Authors: P. Bork, C. Bowler, C. de Vargas, G. Gorsky, E. Karsenti, P. Wincker

Author: H. Jesse Smith

Author: Paula A. Kiberstis

Author: Leslie K. Ferrarelli

Author: Jake Yeston

Author: Gilbert Chin

Author: Angela Colmone

Author: Brent Grocholski

Author: Peter Stern

Author: Guy Riddihough

Author: Kristen L. Mueller

Author: H. Jesse Smith

Author: Julia Fahrenkamp-Uppenbrink

Author: Laura M. Zahn

Author: Guy Riddihough

Author: Valda Vinson

Author: Beverly A. Purnell

Author: Caroline Ash

Author: Ian S. Osborne