Metabolic trade-offs constrain the cell size ratio in a nitrogen-fixing symbiosis.

Biological dinitrogen (N2) fixation is a key metabolic process exclusively performed by prokaryotes, some of which are symbiotic with eukaryotes. Species of the marine haptophyte algae Braarudosphaera bigelowii harbor the N2-fixing endosymbiotic cyanobacteria UCYN-A, which might be evolving organelle-like characteristics. We found that the size ratio between UCYN-A and their hosts is strikingly conserved across sublineages/species, which is consistent with the size relationships of organelles in this symbiosis and other species. Metabolic modeling showed that this size relationship maximizes the coordinated growth rate based on trade-offs between resource acquisition and exchange. Our findings show that the size relationships of N2-fixing endosymbionts and organelles in unicellular eukaryotes are constrained by predictable metabolic underpinnings and that UCYN-A is, in many regards, functioning like a hypothetical N2-fixing organelle (or nitroplast).

Marine DNA Viral Macro- and Microdiversity from Pole to Pole.

Microbes drive most ecosystems and are modulated by viruses that impact their lifespan, gene flow, and metabolic outputs. However, ecosystem-level impacts of viral community diversity remain difficult to assess due to classification issues and few reference genomes. Here, we establish an ∼12-fold expanded global ocean DNA virome dataset of 195,728 viral populations, now including the Arctic Ocean, and validate that these populations form discrete genotypic clusters. Meta-community analyses revealed five ecological zones throughout the global ocean, including two distinct Arctic regions. Across the zones, local and global patterns and drivers in viral community diversity were established for both macrodiversity (inter-population diversity) and microdiversity (intra-population genetic variation). These patterns sometimes, but not always, paralleled those from macro-organisms and revealed temperate and tropical surface waters and the Arctic as biodiversity hotspots and mechanistic hypotheses to explain them. Such further understanding of ocean viruses is critical for broader inclusion in ecosystem models.

Clocks at sea: the genome-editing tide is rising.

The coastline is a particularly challenging environment for its inhabitants. Not only do they have to cope with the solar day and the passing of seasons, but they must also deal with tides. In addition, many marine species track the phase of the moon, especially to coordinate reproduction. Marine animals show remarkable behavioral and physiological adaptability, using biological clocks to anticipate specific environmental cycles. Presently, we lack a basic understanding of the molecular mechanisms underlying circatidal and circalunar clocks. Recent advances in genome engineering and the development of genetically tractable marine model organisms are transforming how we study these timekeeping mechanisms and opening a novel era in marine chronobiology.

Finding genes and pathways that underlie coral adaptation.

Mass coral bleaching is one of the clearest threats of climate change to the persistence of marine biodiversity. Despite the negative impacts of bleaching on coral health and survival, some corals may be able to rapidly adapt to warming ocean temperatures. Thus, a significant focus in coral research is identifying the genes and pathways underlying coral heat adaptation. Here, we review state-of-the-art methods that may enable the discovery of heat-adaptive loci in corals and identify four main knowledge gaps. To fill these gaps, we describe an experimental approach combining seascape genomics with CRISPR/Cas9 gene editing to discover and validate heat-adaptive loci. Finally, we discuss how information on adaptive genotypes could be used in coral reef conservation and management strategies.

Synchronous retreat of Thwaites and Pine Island glaciers in response to external forcings in the presatellite era.

Today, relatively warm Circumpolar Deep Water is melting Thwaites Glacier at the base of its ice shelf and at the grounding zone, contributing to significant ice retreat. Accelerating ice loss has been observed since the 1970s; however, it is unclear when this phase of significant melting initiated. We analyzed the marine sedimentary record to reconstruct Thwaites Glacier's history from the early Holocene to present. Marine geophysical surveys were carried out along the floating ice-shelf margin to identify core locations from various geomorphic settings. We use sedimentological data and physical properties to define sedimentary facies at seven core sites. Glaciomarine sediment deposits reveal that the grounded ice in the Amundsen Sea Embayment had already retreated to within ~45 km of the modern grounding zone prior to ca. 9,400 y ago. Sediments deposited within the past 100+ y record abrupt changes in environmental conditions. On seafloor highs, these shifts document ice-shelf thinning initiating at least as early as the 1940s. Sediments recovered from deep basins reflect a transition from ice proximal to slightly more distal conditions, suggesting ongoing grounding-zone retreat since the 1950s. The timing of ice-shelf unpinning from the seafloor for Thwaites Glacier coincides with similar records from neighboring Pine Island Glacier. Our work provides robust new evidence that glacier retreat in the Amundsen Sea was initiated in the mid-twentieth century, likely associated with climate variability.

Seafloor primary production in a changing Arctic Ocean.

Phytoplankton and sea ice algae are traditionally considered to be the main primary producers in the Arctic Ocean. In this Perspective, we explore the importance of benthic primary producers (BPPs) encompassing microalgae, macroalgae, and seagrasses, which represent a poorly quantified source of Arctic marine primary production. Despite scarce observations, models predict that BPPs are widespread, colonizing ~3 million km2 of the extensive Arctic coastal and shelf seas. Using a synthesis of published data and a novel model, we estimate that BPPs currently contribute ~77 Tg C y-1 of primary production to the Arctic, equivalent to ~20 to 35% of annual phytoplankton production. Macroalgae contribute ~43 Tg C y-1, seagrasses contribute ~23 Tg C y-1, and microalgae-dominated shelf habitats contribute ~11 to 16 Tg C y-1. Since 2003, the Arctic seafloor area exposed to sunlight has increased by ~47,000 km2 y-1, expanding the realm of BPPs in a warming Arctic. Increased macrophyte abundance and productivity is expected along Arctic coastlines with continued ocean warming and sea ice loss. However, microalgal benthic primary production has increased in only a few shelf regions despite substantial sea ice loss over the past 20 y, as higher solar irradiance in the ice-free ocean is counterbalanced by reduced water transparency. This suggests complex impacts of climate change on Arctic light availability and marine primary production. Despite significant knowledge gaps on Arctic BPPs, their widespread presence and obvious contribution to coastal and shelf ecosystem production call for further investigation and for their inclusion in Arctic ecosystem models and carbon budgets.

Global expansion of marine protected areas and the redistribution of fishing effort.

The expansion of marine protected areas (MPAs) is a core focus of global conservation efforts, with the "30x30" initiative to protect 30% of the ocean by 2030 serving as a prominent example of this trend. We consider a series of proposed MPA network expansions of various sizes, and we forecast the impact this increase in protection would have on global patterns of fishing effort. We do so by building a predictive machine learning model trained on a global dataset of satellite-based fishing vessel monitoring data, current MPA locations, and spatiotemporal environmental, geographic, political, and economic features. We then use this model to predict future fishing effort under various MPA expansion scenarios compared to a business-as-usual counterfactual scenario that includes no new MPAs. The difference between these scenarios represents the predicted change in fishing effort associated with MPA expansion. We find that regardless of the MPA network objectives or size, fishing effort would decrease inside the MPAs, though by much less than 100%. Moreover, we find that the reduction in fishing effort inside MPAs does not simply redistribute outside-rather, fishing effort outside MPAs would also decline. The overall magnitude of the predicted decrease in global fishing effort principally depends on where networks are placed in relation to existing fishing effort. MPA expansion will lead to a global redistribution of fishing effort that should be accounted for in network design, implementation, and impact evaluation.

A diverse portfolio of marine protected areas can better advance global conservation and equity.

Marine protected areas (MPAs) are widely used for ocean conservation, yet the relative impacts of various types of MPAs are poorly understood. We estimated impacts on fish biomass from no-take and multiple-use (fished) MPAs, employing a rigorous matched counterfactual design with a global dataset of >14,000 surveys in and around 216 MPAs. Both no-take and multiple-use MPAs generated positive conservation outcomes relative to no protection (58.2% and 12.6% fish biomass increases, respectively), with smaller estimated differences between the two MPA types when controlling for additional confounding factors (8.3% increase). Relative performance depended on context and management: no-take MPAs performed better in areas of high human pressure but similar to multiple-use in remote locations. Multiple-use MPA performance was low in high-pressure areas but improved significantly with better management, producing similar outcomes to no-take MPAs when adequately staffed and appropriate use regulations were applied. For priority conservation areas where no-take restrictions are not possible or ethical, our findings show that a portfolio of well-designed and well-managed multiple-use MPAs represents a viable and potentially equitable pathway to advance local and global conservation.

A submerged Stone Age hunting architecture from the Western Baltic Sea.

The Baltic Sea basins, some of which only submerged in the mid-Holocene, preserve Stone Age structures that did not survive on land. Yet, the discovery of these features is challenging and requires cross-disciplinary approaches between archeology and marine geosciences. Here, we combine shipborne and autonomousunderwater vehicle hydroacoustic data with up to a centimeter range resolution, sedimentological samples, and optical images to explore a Stone Age megastructure located in 21 m water depth in the Bay of Mecklenburg, Germany. The structure is made of 1,673 individual stones which are usually less than 1 m in height, placed side by side over a distance of 971 m in a way that argues against a natural origin by glacial transport or ice push ridges. Running adjacent to the sunken shoreline of a paleolake (or bog), whose youngest phase was dated to 9,143 ±36 ka B.P., the stonewall was likely used for hunting the Eurasian reindeer (Rangifer tarandus) during the Younger Dryas or early Pre-Boreal. It was built by hunter-gatherer groups that roamed the region after the retreat of the Weichselian Ice Sheet. Comparable Stone Age megastructures have become known worldwide in recent times but are almost unknown in Europe. The site represents one of the oldest documented man-made hunting structures on Earth, and ranges among the largest known Stone Age structure in Europe. It will become important for understanding subsistence strategies, mobility patterns, and inspire discussions concerning the territorial development in the Western Baltic Sea region.

Combining environmental DNA and visual surveys can inform conservation planning for coral reefs.

Environmental DNA (eDNA) metabarcoding has the potential to revolutionize conservation planning by providing spatially and taxonomically comprehensive data on biodiversity and ecosystem conditions, but its utility to inform the design of protected areas remains untested. Here, we quantify whether and how identifying conservation priority areas within coral reef ecosystems differs when biodiversity information is collected via eDNA analyses or traditional visual census records. We focus on 147 coral reefs in Indonesia's hyper-diverse Wallacea region and show large discrepancies in the allocation and spatial design of conservation priority areas when coral reef species were surveyed with underwater visual techniques (fishes, corals, and algae) or eDNA metabarcoding (eukaryotes and metazoans). Specifically, incidental protection occurred for 55% of eDNA species when targets were set for species detected by visual surveys and 71% vice versa. This finding is supported by generally low overlap in detection between visual census and eDNA methods at species level, with more overlap at higher taxonomic ranks. Incomplete taxonomic reference databases for the highly diverse Wallacea reefs, and the complementary detection of species by the two methods, underscore the current need to combine different biodiversity data sources to maximize species representation in conservation planning.

Evidence of nitrate-based nighttime atmospheric nucleation driven by marine microorganisms in the South Pacific.

Our understanding of ocean-cloud interactions and their effect on climate lacks insight into a key pathway: do biogenic marine emissions form new particles in the open ocean atmosphere? Using measurements collected in ship-borne air-sea interface tanks deployed in the Southwestern Pacific Ocean, we identified new particle formation (NPF) during nighttime that was related to plankton community composition. We show that nitrate ions are the only species for which abundance could support NPF rates in our semicontrolled experiments. Nitrate ions also prevailed in the natural pristine marine atmosphere and were elevated under higher sub-10 nm particle concentrations. We hypothesize that these nucleation events were fueled by complex, short-term biogeochemical cycling involving the microbial loop. These findings suggest a new perspective with a previously unidentified role of nitrate of marine biogeochemical origin in aerosol nucleation.

Chitin utilization by marine picocyanobacteria and the evolution of a planktonic lifestyle.

Marine picocyanobacteria Prochlorococcus and Synechococcus, the most abundant photosynthetic cells in the oceans, are generally thought to have a primarily single-celled and free-living lifestyle. However, while studying the ability of picocyanobacteria to supplement photosynthetic carbon fixation with the use of exogenous organic carbon, we found the widespread occurrence of genes for breaking down chitin, an abundant source of organic carbon that exists primarily as particles. We show that cells that encode a chitin degradation pathway display chitin degradation activity, attach to chitin particles, and show enhanced growth under low light conditions when exposed to chitosan, a partially deacetylated soluble form of chitin. Marine chitin is largely derived from arthropods, which underwent major diversifications 520 to 535 Mya, close to when marine picocyanobacteria are inferred to have appeared in the ocean. Phylogenetic analyses confirm that the chitin utilization trait was acquired at the root of marine picocyanobacteria. Together this leads us to postulate that attachment to chitin particles allowed benthic cyanobacteria to emulate their mat-based lifestyle in the water column, initiating their expansion into the open ocean, seeding the rise of modern marine ecosystems. Subsequently, transitioning to a constitutive planktonic life without chitin associations led to cellular and genomic streamlining along a major early branch within Prochlorococcus. Our work highlights how the emergence of associations between organisms from different trophic levels, and their coevolution, creates opportunities for colonizing new environments. In this view, the rise of ecological complexity and the expansion of the biosphere are deeply intertwined processes.

Terpene biosynthesis in marine sponge animals.

Sea sponges are the largest marine source of small-molecule natural products described to date. Sponge-derived molecules, such as the chemotherapeutic eribulin, the calcium-channel blocker manoalide, and antimalarial compound kalihinol A, are renowned for their impressive medicinal, chemical, and biological properties. Sponges contain microbiomes that control the production of many natural products isolated from these marine invertebrates. In fact, all genomic studies to date investigating the metabolic origins of sponge-derived small molecules concluded that microbes-not the sponge animal host-are the biosynthetic producers. However, early cell-sorting studies suggested the sponge animal host may play a role particularly in the production of terpenoid molecules. To investigate the genetic underpinnings of sponge terpenoid biosynthesis, we sequenced the metagenome and transcriptome of an isonitrile sesquiterpenoid-containing sponge of the order Bubarida. Using bioinformatic searches and biochemical validation, we identified a group of type I terpene synthases (TSs) from this sponge and multiple other species, the first of this enzyme class characterized from the sponge holobiome. The Bubarida TS-associated contigs consist of intron-containing genes homologous to sponge genes and feature GC percentage and coverage consistent with other eukaryotic sequences. We identified and characterized TS homologs from five different sponge species isolated from geographically distant locations, thereby suggesting a broad distribution amongst sponges. This work sheds light on the role of sponges in secondary metabolite production and speaks to the possibility that other sponge-specific molecules originate from the animal host.

An observation-based, reduced-form model for oxidation in the remote marine troposphere.

The hydroxyl radical (OH) fuels atmospheric chemical cycling as the main sink for methane and a driver of the formation and loss of many air pollutants, but direct OH observations are sparse. We develop and evaluate an observation-based proxy for short-term, spatial variations in OH (ProxyOH) in the remote marine troposphere using comprehensive measurements from the NASA Atmospheric Tomography (ATom) airborne campaign. ProxyOH is a reduced form of the OH steady-state equation representing the dominant OH production and loss pathways in the remote marine troposphere, according to box model simulations of OH constrained with ATom observations. ProxyOH comprises only eight variables that are generally observed by routine ground- or satellite-based instruments. ProxyOH scales linearly with in situ [OH] spatial variations along the ATom flight tracks (median r2 = 0.90, interquartile range = 0.80 to 0.94 across 2-km altitude by 20° latitudinal regions). We deconstruct spatial variations in ProxyOH as a first-order approximation of the sensitivity of OH variations to individual terms. Two terms modulate within-region ProxyOH variations-water vapor (H2O) and, to a lesser extent, nitric oxide (NO). This implies that a limited set of observations could offer an avenue for observation-based mapping of OH spatial variations over much of the remote marine troposphere. Both H2O and NO are expected to change with climate, while NO also varies strongly with human activities. We also illustrate the utility of ProxyOH as a process-based approach for evaluating intermodel differences in remote marine tropospheric OH.

Boundary exchange completes the marine Pb cycle jigsaw.

Material fluxes at the land-ocean interface impact seawater composition and global cycling of elements. However, most attention has been focused on the fluvial dissolved fluxes. For elements like lead (Pb), whose fluvial particulate flux into the ocean is two orders of magnitude higher than the dissolved counterpart, the role of particulates in elemental cycling is potentially important but currently less appreciated. Using both chemical analyses on samples collected from around equatorial Southeast Asia and model simulations, we show that particulate-dissolved exchange is an important mechanism controlling the concentration and isotopic composition of dissolved Pb in the ocean. Our model indicates that Pb contributed from particulate-dissolved exchange at ocean boundaries is larger than, or at least comparable to, other major Pb sources to the seawater before the Anthropocene, when the anthropogenic Pb was absent. Our work highlights the importance of boundary exchange in understanding marine element cycling and weathering-climate feedback.

Recovery of a marine keystone predator transforms terrestrial predator-prey dynamics.

Sea otters (Enhydra lutris) and wolves (Canis lupus) are two apex predators with strong and cascading effects on ecosystem structure and function. After decades of recovery from near extirpation, their ranges now overlap, allowing sea otters and wolves to interact for the first time in the scientific record. We intensively studied wolves during 2015 to 2021 in an island system colonized by sea otters in the 2000s and by wolves in 2013. After wolf colonization, we quantified shifts in foraging behavior with DNA metabarcoding of 689 wolf scats and stable isotope analyses, both revealing a dietary switch from Sitka black-tailed deer (Odocoileus hemionus), the terrestrial in situ primary prey, to sea otters. Here we show an unexpected result of the reintroduction and restoration of sea otters, which became an abundant marine subsidy for wolves following population recovery. The availability of sea otters allowed wolves to persist and continue to reproduce, subsequently nearly eliminating deer. Genotypes from 390 wolf scats and telemetry data from 13 wolves confirmed island fidelity constituting one of the highest known wolf population densities and upending standardly accepted wolf density predictions based on ungulate abundance. Whereas marine subsidies in other systems are generally derived from lower trophic levels, here an apex nearshore predator became a key prey species and linked nearshore and terrestrial food webs in a recently deglaciated and rapidly changing ecosystem. These results underscore that species restoration may serve as an unanticipated nutrient pathway for recipient ecosystems even resulting in cross-boundary subsidy cascades.

Marine reserves promote cycles in fish populations on ecological and evolutionary time scales.

Marine reserves are considered essential for sustainable fisheries, although their effectiveness compared to traditional fisheries management is debated. The effect of marine reserves is mostly studied on short ecological time scales, whereas fisheries-induced evolution is a well-established consequence of harvesting. Using a size-structured population model for an exploited fish population of which individuals spend their early life stages in a nursery habitat, we show that marine reserves will shift the mode of population regulation from low size-selective survival late in life to low, early-life survival due to strong resource competition. This shift promotes the occurrence of rapid ecological cycles driven by density-dependent recruitment as well as much slower evolutionary cycles driven by selection for the optimal body to leave the nursery grounds, especially with larger marine reserves. The evolutionary changes increase harvesting yields in terms of total biomass but cause disproportionately large decreases in yields of larger, adult fish. Our findings highlight the importance of carefully considering the size of marine reserves and the individual life history of fish when managing eco-evolutionary marine systems to ensure both population persistence as well as stable fisheries yields.

US climate policy yields water quality cobenefits in the Mississippi Basin and Gulf of Mexico.

We utilize a coupled economy-agroecology-hydrology modeling framework to capture the cascading impacts of climate change mitigation policy on agriculture and the resulting water quality cobenefits. We analyze a policy that assigns a range of United States government's social cost of carbon estimates ($51, $76, and $152/ton of CO2-equivalents) to fossil fuel-based CO2 emissions. This policy raises energy costs and, importantly for agriculture, boosts the price of nitrogen fertilizer production. At the highest carbon price, US carbon emissions are reduced by about 50%, and nitrogen fertilizer prices rise by about 90%, leading to an approximate 15% reduction in fertilizer applications for corn production across the Mississippi River Basin. Corn and soybean production declines by about 7%, increasing crop prices by 6%, while nitrate leaching declines by about 10%. Simulated nitrate export to the Gulf of Mexico decreases by 8%, ultimately shrinking the average midsummer area of the Gulf of Mexico hypoxic area by 3% and hypoxic volume by 4%. We also consider the additional benefits of restored wetlands to mitigate nitrogen loading to reduce hypoxia in the Gulf of Mexico and find a targeted wetland restoration scenario approximately doubles the effect of a low to moderate social cost of carbon. Wetland restoration alone exhibited spillover effects that increased nitrate leaching in other parts of the basin which were mitigated with the inclusion of the carbon policy. We conclude that a national climate policy aimed at reducing greenhouse gas emissions in the United States would have important water quality cobenefits.

Lipid biomarkers for algal resistance to viral infection in the ocean.

Marine viruses play a key role in regulating phytoplankton populations, greatly affecting the biogeochemical cycling of major nutrients in the ocean. Resistance to viral infection has been reported for various phytoplankton species under laboratory conditions. Nevertheless, the occurrence of resistant cells in natural populations is underexplored due to the lack of sensitive tools to detect these rare phenotypes. Consequently, our current understanding of the ecological importance of resistance and its underlying mechanisms is limited. Here, we sought to identify lipid biomarkers for the resistance of the bloom-forming alga Emiliania huxleyi to its specific virus, E. huxleyi virus (EhV). By applying an untargeted lipidomics approach, we identified a group of glycosphingolipid (GSL) biomarkers that characterize resistant E. huxleyi strains and were thus termed resistance-specific GSLs (resGSLs). Further, we detected these lipid biomarkers in E. huxleyi isolates collected from induced E. huxleyi blooms and in samples collected during an open-ocean E. huxleyi bloom, indicating that resistant cells predominantly occur during the demise phase of the bloom. Last, we show that the GSL composition of E. huxleyi cultures that recover following infection and gain resistance to the virus resembles that of resistant strains. These findings highlight the metabolic plasticity and coevolution of the GSL biosynthetic pathway and underscore its central part in this host-virus arms race.

Linking vertical movements of large pelagic predators with distribution patterns of biomass in the open ocean.

Many predator species make regular excursions from near-surface waters to the twilight (200 to 1,000 m) and midnight (1,000 to 3,000 m) zones of the deep pelagic ocean. While the occurrence of significant vertical movements into the deep ocean has evolved independently across taxonomic groups, the functional role(s) and ecological significance of these movements remain poorly understood. Here, we integrate results from satellite tagging efforts with model predictions of deep prey layers in the North Atlantic Ocean to determine whether prey distributions are correlated with vertical habitat use across 12 species of predators. Using 3D movement data for 344 individuals who traversed nearly 1.5 million km of pelagic ocean in [Formula: see text]42,000 d, we found that nearly every tagged predator frequented the twilight zone and many made regular trips to the midnight zone. Using a predictive model, we found clear alignment of predator depth use with the expected location of deep pelagic prey for at least half of the predator species. We compared high-resolution predator data with shipboard acoustics and selected representative matches that highlight the opportunities and challenges in the analysis and synthesis of these data. While not all observed behavior was consistent with estimated prey availability at depth, our results suggest that deep pelagic biomass likely has high ecological value for a suite of commercially important predators in the open ocean. Careful consideration of the disruption to ecosystem services provided by pelagic food webs is needed before the potential costs and benefits of proceeding with extractive activities in the deep ocean can be evaluated.