An international team has conducted the first-ever global survey of the ecological diversity of viruses in the oceans during expeditions aboard a single sailboat, the Tara. They identified nearly 200,000 marine viral species, which vastly exceeds the 15,000 known from prior ocean surveys of these waters and the approximately 2,000 genomes available from cultured viruses of microbes. Their findings, appearing April 25 in the journal Cell, have implications for understanding issues ranging from evolution to climate change, because they help create a new picture of our planet and how it may be impacted by interactions among organisms.

“Viruses are these tiny things that you can’t even see, but because they’re present in such huge numbers, they really matter,” says senior author Matthew Sullivan (@Lab_Sullivan), a microbiologist at the Ohio State University. “We’ve developed a distribution map that is foundational for anyone who wants to study how viruses manipulate the ecosystem. There were many things that surprised us about our findings.”

Among the surprises was the existence of these nearly 200,000 marine viral species. Additionally, meta-community analysis showed that the viruses were organized into five distinct ecological zones throughout the entire ocean, which was unexpected given the fluid nature of the oceans and the complexity of many of the marine regions. Also, despite the paradigm from larger organisms that species diversity is highest near the equator and lowest near the poles, the researchers collected an extensive number of samples in the Arctic compared to previous studies of ocean life and found a biodiversity hotspot in the Arctic Ocean.

The samples were collected between 2009 and 2013 on the Tara as part of the Tara Oceans effort. Begun in 2006, the Tara project aims to conduct unique and innovative ocean science with the goal of predicting and better anticipating the impacts of climate change. In the current effort, a rotating team of scientists spent time on the boat collecting ocean water samples from different depths across many geographical regions. After being collected, the samples for this study were filtered and shipped back to about a dozen different labs for analysis.

The investigators studied not only the water samples for viruses, but also other microbes and other living creatures. “We filtered the samples to analyze organisms ranging in size from viruses to fish eggs,” Sullivan says. He adds that papers reporting some of the other microbial components from the samples are forthcoming.

Another noteworthy aspect of the project was the extensive number of samples collected in the Arctic, a highlight that has not been part of earlier studies of ocean life.

This research has significant implications for understanding how ocean microorganisms affect the earth’s atmosphere. “In the last 20 years or so, we’ve learned that half of the oxygen that we breathe comes from marine organisms,” Sullivan notes. “Additionally, the oceans soak up half of the carbon dioxide from the atmosphere.”

“Because of complex chemistry, increased levels of carbon dioxide at the surface acidify the oceans,” Sullivan adds. “However, if carbon dioxide instead is converted to organic carbon and biomass, then it can become particulate and sink into the deep oceans. That’s a good result for helping mitigate human-induced climate change–and we’re learning that viruses can help facilitate this sinking. Having a new map of where these viruses are located can help us understand this ocean carbon “pump” and, more broadly, biogeochemistry that impacts the planet.”

The investigators say that having a more complete picture of marine viral distribution and abundance will help them to determine which viruses they should be focusing on for further studies. Additionally, the maps based on this research establish a baseline for other collection efforts going forward, which can help to answer questions about how levels of microorganisms change over time, in response to both seasonal variation and climate change.

“Previous ocean ecosystem models have commonly ignored microbes, and rarely included viruses, but we now know they are a vital component to include,” Sullivan concludes.

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The study’s two first authors were Ohio State graduate students Ann C. Gregory and Ahmed Zayed. This research was made possible by the scientists and crew who sampled aboard the Tara, as well as the leadership of the Tara Expeditions Foundation. Funding was provided by the Gordon and Betty Moore Foundation, the National Science Foundation, Oceanomics, France Genomique, ETH (the Swiss Federal Institute of Technology), the Helmut Horten Foundation, a Netherlands Organization for Scientific Research Vidi grant, and a National Institutes of Health training grant fellowship.

Cell, Gregory et al: “Marine viral macro- and micro-diversity from pole to pole.” https://www.cell.com/cell/fulltext/S0092-8674(19)30341-1

• Two papers publishing in the journal Cell use samples and data collected during the Tara Oceans Expedition to analyze current ocean diversity across the planet, providing a baseline to better understand the future impacts of climate change on the oceans.
• Ibarbalz et al. report that most planktonic groups follow a gradient of diversity along latitudes, with the lowest level of diversity closest to the poles.
• Salazar et al. find that microbial diversity and microbial gene expression play different roles in how ocean microbial communities respond to environmental change in different geographies.
• In a Perspective publishing in the journal One Earth, Claudet et al. examine the barriers that have prevented ocean sustainability policy changes so far and suggest strategies for leveraging the UN Decade of Ocean Science for Sustainable Development to overcome these challenges.

In an effort to reverse the decline in the health of the world’s oceans, the United Nations (UN) has declared 2021 to 2030 to be the Decade of Ocean Science for Sustainable Development. One key requirement for the scientific initiative is data on existing global ocean conditions. An important trove of data is already available thanks to the Tara Oceans expedition, an international, interdisciplinary enterprise that collected 35,000 samples from all the world’s oceans between 2009 and 2013. The samples were collected by researchers aboard one schooner, the Tara, at depths ranging from the surface to 1,000 meters deep.

Two papers being published November 14 in the journal Cell are the latest to use samples and data collected during the Tara Oceans expedition to analyze diversity across the entire planet of plankton, microscopic organisms that drift on oceanic currents that are key for the well-being of our oceans. One study focused on the diversity of plankton across Earth’s oceans, whereas the other study assessed gene expression among microbial communities as a way to predict how these communities might adapt to changing environmental conditions.

Plankton Diversity across Different Latitudes

“Everything in the ocean is connected, which means it has the potential to move around,” says Chris Bowler, a National Center for Scientific Research (CNRS) scientist at the Institut de Biologie de l’Ecole Normale Superieure (IBENS) in Paris and a co-senior author of the plankton study. “This makes it important to assemble everything on a global scale. Doing deep analysis also allows us to catch the rare organisms in the biosphere in addition to those that are more abundant.”

“Our study focused on plankton because it’s a major contributor to marine ecosystems in terms of biomass, abundance, and diversity,” says co-senior author Lucie Zinger of IBENS. “All types of life have representatives in the plankton–bacteria, archaea, protists, animals and plants, as well as viruses. But the large majority of this diversity is invisible to the naked eye.”

The paper reports that the large majority of planktonic groups, from giant viruses to small animals, follow a gradient of diversity along latitudes, with the lowest level of diversity closest to the poles. “Ocean temperature is mainly responsible for this pattern,” Zinger notes. “Ocean warming due to climate change is likely to lead to a ‘tropicalization,’ or increase, of plankton diversity in temperate and polar waters. The consequences of this are still unclear, but we know these geographic areas are currently very important for different ecosystem services, including fisheries and carbon sequestration.”

One innovative aspect of this study was that it combined both imaging and DNA-based techniques to assess plankton diversity. “We know a lot about how to process information from DNA sequences,” Bowler says. “But images are much more complicated. We observed many different morphologies and different behaviors of these organisms. There are many new organisms and new kinds of interactions between them still to be discovered.”

Understanding the Activity of Microbial Life at Different Ocean Depths and Geographies

The transcriptome study combined metagenomic and metatranscriptomic data, allowing the team to analyze the analyze which genes were present, as well as which genes were turned on, in ocean microbial communities across gradients of both depth and latitude. Previous studies on the diversity of marine microbial life have focused primarily on genomes. This was the first to look at transcriptomes on a global scale.

“Looking at transcriptomes is important for determining not just which microbes are present, but what those microbes are actually doing with regard to activities like photosynthesis and nutrient uptake,” says senior author Shinichi Sunagawa of the Institute of Microbiology and Swiss Institute of Bioinformatics at ETH Zurich. “One of our goals was to learn whether microbial communities adjust to environmental and temperature variations with changes in their composition relative to each other or with changes in the gene expression patterns within these communities.”

The investigators found that in terms of taxonomic, genomic, and transcriptomic composition, there are distinct ecological boundaries separating both surface water from deep water and polar from nonpolar regions. They expected to see some of these changes–such as differences in the levels of photosynthetic organisms relative to water depth. But some other observations were rather unexpected.

“We did not expect to find biogeographic patterns for the underlying mechanisms of metatranscriptomic composition variation. Specifically, we found differences in polar communities to be dominated by changes in organismal composition, while in nonpolar waters, the differences were dominated by changes in the expression of genes,” Sunagawa says. He adds that his team was also surprised to find genomic and transcriptomic evidence for a nitrogen-fixing bacterium in deep Arctic waters.

“Every drop of marine water is full of microbes, which play a central role in many processes relevant to life on Earth,” he notes. “Understanding the ecological factors that determine the diversity, composition, and activity of these organisms is essential to better model and predict future deviations, especially in light of climate change.”

One limitation of the data to come from the Tara Oceans expedition is that the samples were collected over a relatively short period of time, less than four years. This makes it difficult to observe any measurable trends in today’s oceans related to climate change. The researchers say that longer-term studies are needed to account for changes in factors like acidification, deoxygenation, and pollution.

A Call for Ocean Science in the Face of Climate Change

Researchers examine the barriers that have prevented ocean sustainability policy changes so far and suggest strategies for overcoming these challenges in a Perspective publishing November 14 in the new Cell Press journal One Earth.

“As revealed by the releases of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services global assessment and of the Special Report on the Ocean and Cryosphere of the IPCC, both in 2019, there is now an urgency to engage into sustainable pathways,” says corresponding author Joachim Claudet of the CNRS. He adds that the main threats on the ocean’s sustainability are overexploitation of fish, shellfish, and other organisms; land- and sea-based pollution; and land/sea-use change, including coastal development for infrastructure and aquaculture; and climate change.

“We need science to develop evidence that can better inform policies to implement viable solutions, as well as operational and transformative actions that can better impact societies, from local to global scales,” he says. “The Tara expeditions have multiple values. They allow us to collect local natural, chemical, and physical in situ data at the ocean scale. These data can feed into both basic and applied research. Tara’s outreach programs can also be a driver of the most needed change in perception that the ocean is both highly valuable and vulnerable.”

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This work was primarily funded by the Tara Ocean Foundation and 23 supporting institutes (https://oceans.taraexpeditions.org/). For additional funding information, please see individual papers.

Cell, Ibarbalz et al.: “Global Trends in Marine Plankton Diversity across Kingdoms of Life” https://www.cell.com/cell/fulltext/S0092-8674(19)31124-9 DOI: 10.1016/j.cell.2019.10.008