Metagenomic analysis reveals global-scale patterns of ocean nutrient limitation

Ustick, Lucas J.; Larkin, Alyse A.; Garcia, Catherine A.; Garcia, Nathan S.; Brock, M. Louise; Lee, Jenna; Wiseman, Nicola A.; Moore, J. Keith; Martiny, Adam C.

doi:10.1126/science.abe6301

Cited by 113 publications

(148 citation statements)

References 64 publications

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“…The continuing expansion of global-scale meta'omic surveys, such as BioGeoTraces Biller et al (2018) and Bio-GO-SHIP (Ustick et al, 2021), highlights the importance of developing scalable and automated methods to enable more complete analysis of these data. Metagenomic pipelines that specifically integrate steps for handling eukaryotic biology, such as the EukHeist pipeline, are vital as eukaryotes are important members of microbial communities, ranging from the ocean, to soil (Bailly et al, 2007) and human- (Lukeš et al, 2015) and animal-associated (Campo et al, 2019) environments.…”

Section: Discussionmentioning

confidence: 99%

Eukaryotic genomes from a global metagenomic dataset illuminate trophic modes and biogeography of ocean plankton

Alexander

Krinos

et al. 2021

Preprint

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Molecular and genomic approaches that target mixed microbial communities (e.g., metagenomics or metatranscriptomics) provide insight into the ecological roles, evolutionary histories, and physiological capabilities of the microorganisms and the processes in the environment. Computational tools that harness large-scale sequence surveys have become a valuable resource for characterizing the genetic make-up of the bacterial and archaeal component of the marine microbiome. Yet, fewer studies have focused on the unicellular eukaryotic fraction of the community. Here, we developed the EukHeist automated computational pipeline, to retrieve eukaryotic and prokaryotic metagenome assembled genomes (MAGs). We applied EukHeist to the eukaryote-dominated large-size fraction data (0.8-2000 μm) from the Tara Oceans survey to recover both eukaryotic and prokaryotic MAGs, which we refer to as TOPAZ (Tara Oceans Particle-Associated MAGs). The TOPAZ MAGs consisted of more than 900 eukaryotic MAGs representing environmentally-relevant microbial and multicellular eukaryotes in addition to over 4,000 bacterial and archaeal MAGs. The bacterial and archaeal TOPAZ MAGs retrieved with EukHeist complement previous efforts by expanding the existing phylogenetic diversity through the increase in coverage of many likely particle- and host-associated taxa. We also demonstrate how the novel eukaryotic genomic content recovered from this study might be used to infer functional traits, such as trophic mode. By coupling MAGs and metatranscriptomic data, we explored ecologically-significant protistan groups, such as the Stramenopiles. A global survey of both eukaryotic and prokaryotic MAGs enabled the identification of ecological cohorts, driven by specific environmental factors, and putative host-microbe associations. Accessible and scalable computational tools, such as EukHeist, are likely to accelerate the identification of meaningful genetic signatures from large datasets, ultimately expanding the eukaryotic tree of life.

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Section: Discussionmentioning

confidence: 99%

Eukaryotic genomes from a global metagenomic dataset illuminate trophic modes and biogeography of ocean plankton

Alexander

Krinos

et al. 2021

Preprint

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“…A set of mechanistic experiments within a single model demonstrated that minor parameter adjustments that altered the strength of iron limitation and its replacement by nitrogen limitation in the tropical Pacific led to large changes in both the magnitude and sign of changes to regional NPP (Tagliabue et al, 2020). It is highly likely that there is divergence in the representation of nutrient limitation regimes across CMIP5 and CMIP6 models, in part due to the paucity of observational constraints (Moore et al, 2013;Ustick et al, 2021). Indeed, it was notable that the emergent constraint that assessed NPP projections from CMIP5 using the co-variation of sea surface temperature and NPP anomalies (Kwiatkowski et al, 2017), was not able to strongly discriminate among different iron-nitrogen limitation scenarios (Tagliabue et al, 2020).…”

Section: Uncertainties In the Representation Of Biogeochemical Processesmentioning

confidence: 99%

“…Associated with the challenge of constraining the magnitude of present-day NPP is uncertain knowledge of the drivers of change and how inter-model differences in atmospheric and ocean physics cascade through ocean biogeochemical cycles to drive resource limitation of NPP. Knowledge is growing regarding the role of multiple concurrent factors regulating microbial activity (Saito et al, 2014;Browning et al, 2017;Caputi et al, 2019;Ustick et al, 2021). But how the emergence of these multiple drivers are affected by the climate responses of key physical components, like winds, in the Indo-Pacific region in particular, is a major knowledge gap.…”

Section: Future Efforts To Reduce Uncertainty In Npp Projectionsmentioning

confidence: 99%

Persistent Uncertainties in Ocean Net Primary Production Climate Change Projections at Regional Scales Raise Challenges for Assessing Impacts on Ecosystem Services

et al. 2021

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Ocean net primary production (NPP) results from CO2 fixation by marine phytoplankton, catalysing the transfer of organic matter and energy to marine ecosystems, supporting most marine food webs, and fisheries production as well as stimulating ocean carbon sequestration. Thus, alterations to ocean NPP in response to climate change, as quantified by Earth system model experiments conducted as part of the 5th and 6th Coupled Model Intercomparison Project (CMIP5 and CMIP6) efforts, are expected to alter key ecosystem services. Despite reductions in inter-model variability since CMIP5, the ocean components of CMIP6 models disagree roughly 2-fold in the magnitude and spatial distribution of NPP in the contemporary era, due to incomplete understanding and insufficient observational constraints. Projections of NPP change in absolute terms show large uncertainty in CMIP6, most notably in the North Atlantic and the Indo-Pacific regions, with the latter explaining over two-thirds of the total inter-model uncertainty. While the Indo-Pacific has previously been identified as a hotspot for climate impacts on biodiversity and fisheries, the increased inter-model variability of NPP projections further exacerbates the uncertainties of climate risks on ocean-dependent human communities. Drivers of uncertainty in NPP changes at regional scales integrate different physical and biogeochemical factors that require more targeted mechanistic assessment in future studies. Globally, inter-model uncertainty in the projected changes in NPP has increased since CMIP5, which amplifies the challenges associated with the management of associated ecosystem services. Notably, this increased regional uncertainty in the projected NPP change in CMIP6 has occurred despite reduced uncertainty in the regional rates of NPP for historical period. Improved constraints on the magnitude of ocean NPP and the mechanistic drivers of its spatial variability would improve confidence in future changes. It is unlikely that the CMIP6 model ensemble samples the complete uncertainty in NPP, with the inclusion of additional mechanistic realism likely to widen projections further in the future, especially at regional scales. This has important consequences for assessing ecosystem impacts. Ultimately, we need an integrated mechanistic framework that considers how NPP and marine ecosystems respond to impacts of not only climate change, but also the additional non-climate drivers.

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“…Co has been shown to be the metallic cofactor for alkaline phosphatase in the hyperthermophile Thermotoga maritima (Wojciechowski et al, 2002), although Co substitution for Zn in marine cyanobacterial alkaline phosphatase is currently unconfirmed. The Pacific Ocean, in contrast, broadly shows less evidence for P limitation and more evidence for N and Fe stress in the oligotrophic gyres (Bonnet et al, 2008;Saito et al, 2014) and Fe and other trace metal stress in the upwelling regions of the subpolar gyre and equatorial Pacific (Boyd et al, 2004;Coale et al, 1996;Moore et al, 2013;Tsuda et al, 2005;Ustick et al, 2021). This difference in extent of P stress in the Pacific basin compared to the Atlantic was likely the reason for the more linear relationship between dCo and dPO4 throughout the upper Pacific Ocean.…”

Section: The Dco and Dpo4 Relationship Depicts Co Uptake Remineralization And Scavengingmentioning

confidence: 99%

Major processes of the dissolved cobalt cycle in the North and equatorial Pacific Ocean

Chmiel

Lanning

Laubach

et al. 2021

Preprint

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Abstract. Over the past decade, the GEOTRACES and wider trace metal geochemical community have made substantial contributions towards constraining the marine cobalt (Co) cycle and its major biogeochemical processes. However, few Co speciation studies have been conducted in the North and equatorial Pacific Ocean, a vast portion of the world’s oceans by volume and an important endmember of deep thermohaline circulation. Dissolved Co (dCo) samples, including total dissolved and labile Co, were measured at-sea during the GEOTRACES Pacific meridional transect (GP15) along the 152° W longitudinal from 56° N to 20° S. Along this transect, upper ocean dCo was linearly correlated to dissolved phosphate (slope = 82 ± 2 µM:M) due to phytoplankton uptake and remineralization. As depth increased, dCo concentrations became increasingly decoupled from phosphate concentrations due to co-scavenging with manganese oxide particles in the mesopelagic. The transect revealed an organically-bound coastal source of dCo to the Alaskan Stream associated with low salinity waters. An intermediate-depth hydrothermal flux of dCo was observed off the Hawaiian coast at the Loihi Seamount, and the elevated dCo was correlated to estimated xs3He at and above the vent site; however, the Loihi Seamount likely did not represent a major source of Co to the Pacific basin. Elevated concentrations of dCo within oxygen minimum zones (OMZs) in the equatorial North and South Pacific were consistent with the suppression of oxidative scavenging, and we estimate that future deoxygenation could increase the OMZ dCo inventory by 13–28 % over the next century. In North Pacific Deep Water (NPDW), a fraction of elevated ligand-bound dCo appeared protected from scavenging by the high biogenic particle flux in the North Pacific basin. This finding is counter to previous expectations of low dCo concentrations in the deep Pacific due to scavenging over thermohaline circulation. Compared to a Co global biogeochemical model, the observed transect displayed more extreme inventories and fluxes of dCo than predicted by the model, suggesting a highly dynamic Pacific Co cycle.

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Metagenomic analysis reveals global-scale patterns of ocean nutrient limitation

Cited by 113 publications

References 64 publications

Eukaryotic genomes from a global metagenomic dataset illuminate trophic modes and biogeography of ocean plankton

Eukaryotic genomes from a global metagenomic dataset illuminate trophic modes and biogeography of ocean plankton

Persistent Uncertainties in Ocean Net Primary Production Climate Change Projections at Regional Scales Raise Challenges for Assessing Impacts on Ecosystem Services

Major processes of the dissolved cobalt cycle in the North and equatorial Pacific Ocean

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