Plankton networks driving carbon export in the oligotrophic ocean

Abstract

The biological carbon pump is the process by which CO 2 is transformed to organic carbon via photosynthesis, exported through sinking particles, and finally sequestered in the deep ocean. While the intensity of the pump correlates with plankton community composition, the underlying ecosystem structure driving the process remains largely uncharacterised. Here we use environmental and metagenomic data gathered during the Tara Oceans expedition to improve our understanding of carbon export in the oligotrophic ocean. We show that specific plankton communities, from the surface and deep chlorophyll maximum, correlate with carbon export at 150 m and highlight unexpected taxa such as Radiolaria, alveolate parasites, as well as Synechococcus and their phages, as lineages most strongly associated with carbon export in the subtropical, nutrient-depleted, oligotrophic ocean. Additionally, we show that the relative abundance of just a few bacterial and viral genes can predict most of the variability in carbon export in these regions. Guidi et al. Page 2 Nature. Author manuscript; available in PMC 2016 September 22. Europe PMC Funders Author Manuscripts Europe PMC Funders Author ManuscriptsMarine planktonic photosynthetic organisms are responsible for approximately fifty percent of Earth's primary production and fuel the global ocean biological carbon pump 1 . The intensity of the pump is correlated to plankton community composition 2,3 , and controlled by the relative rates of primary production and carbon remineralisation 4 . About 10% of this newly produced organic carbon in the surface ocean is exported through gravitational sinking of particles. Finally, after multiple transformations, a fraction of the exported material reaches the deep ocean where it is sequestered over thousand-year timescales 5 .Like most biological systems, marine ecosystems in the sunlit upper layer of the ocean (denoted the euphotic zone) are complex 6,7 , characterised by a wide range of biotic and abiotic interactions [8][9][10] and in constant balance between carbon production, transfer to higher trophic levels, remineralisation, and export to the deep layers 11 . The marine ecosystem structure and its taxonomic and functional composition likely evolved to comply with this loss of energy by modifying organism turnover times and by the establishment of complex feedbacks between them 6 and the substrates they can exploit for metabolism 12 .Decades of groundbreaking research have focused on identifying independently the key players involved in the biological carbon pump. Among autotrophs, diatoms are commonly attributed to being important in carbon flux because of their large size and fast sinking rates 13-15 while small autotrophic picoplankton may contribute directly through subduction of surface water 16 or indirectly by aggregating with larger settling particles or consumption by organisms at higher trophic levels 17 . Among heterotrophs, zooplankton such as crustaceans impact carbon flux via production of fast-sinking fecal pellets...

Mare Incognitum: A Glimpse into Future Plankton Diversity and Ecology Research

“…High-throughput omics data offer great potential to reveal the global structure of transient marine planktonic ecosystems, since genetic methods compare favorably to traditional observational methods such as microscopy or flow cytometry in terms of the time expenditure, expert knowledge required to identify organisms, and the cost of equipment and analysis. The growing spatial coverage of data enables researchers to estimate global-scale taxonomic diversity of unicellular eukaryotes (de Vargas et al, 2015), to identify the main environmental drivers of community structure in marine prokaryotes (Sunagawa et al, 2015), and to delve into the complexity of biotic interactions between plankton species spanning multiple domains of life, as well as their link to global biogeochemical cycling (Lima-Mendez et al, 2015;Guidi et al, 2016). Complementary to a "bulk" screening of marine biodiversity, single-cell genomics approaches allow matching of phenotype and genotype, and have been used to investigate the phylogenetic affinities of microbial dark matter (i.e., currently unculturable microbial organisms; Rinke et al, 2013;Hug et al, 2016) and to uncover niche partitioning within globally distributed lineages of marine microbes (Kashtan et al, 2014).…”

“…Recently, the exploration of the plankton "interactome" (Lima-Mendez et al, 2015) allowed to describe how biotic interactions occur across trophic levels and relate to environmental conditions and ecosystem functioning, with many new symbiotic interactions identified (Guidi et al, 2016). When prior knowledge is too limited, food-web models could be inferred from simple size-based, or multi-traits assumptions (Albouy et al, 2014), or based on ecosystem models (e.g., Follows et al, 2007;Le Quéré et al, 2016) in combination with satellite estimates of (phyto)plankton community composition (e.g., Hirata et al, 2011).…”

“…For instance, an investigation of planktonic communities at the global scale using highthroughput metagenomic sampling techniques has recently linked carbon export patterns to specific plankton interaction networks (Guidi et al, 2016), suggesting that the who's who in the plankton world is of paramount importance for the carbon cycle. Integrated with revised estimates in species abundance and biomass (Buitenhuis et al, 2013), and combined with advances in statistical (Robinson et al, 2011) and mechanistic modeling techniques (Follows et al, 2007), novel high-throughput metagenomic data may allow us to relate biogeographic patterns of plankton distribution and diversity to further ecosystem processes.…”

Interactive network configuration maintains bacterioplankton community structure under elevated CO<sub>2</sub> in a eutrophic coastal mesocosm experiment

“…One promising method to elucidate these types of complex interactions is network analysis. Ecological network approaches have been successfully applied to investigate the complexity of interactions among zooplankton and phytoplankton from different trophic levels during the Tara Oceans Expedition project (Lima-Mendez et al, 2015;Guidi et al, 2016). Elucidating the complex interactions between bacterioplankton and other marine organisms under anthropogenic perturbations will increase our understanding of their impact in a holistic way.…”

Copepods Boost the Production but Reduce the Carbon Export Efficiency by Diatoms

“…On the smaller scale of such investigations are microcosm studies of sinking particles in rolling tanks (Shanks and Trent, 1980;Passow and De La Rocha, 2006) and flow through systems (Ploug et al, 2008;Long et al, 2015) that allow controlled examination of selected processes and interactions. At the other extreme are regional and global scale studies based on models, remote sensing, and observational data from time-series, cameras, autonomous platforms, and sediment traps (Klaas and Archer, 2002;Honjo et al, 2008;Klaas et al, 2008;Lee et al, 2009;Lam et al, 2011;Assmy et al, 2013;Quéguiner, 2013;Giering et al, 2014;Sanders et al, 2014;Guidi et al, 2016). However, whereas small scale laboratory investigations allow full control over environmental variables and mechanistic investigations, they often lack natural community composition.…”