Disentangling top-down drivers of mortality underlying diel population dynamics of Prochlorococcus in the North Pacific Subtropical Gyre.

Photosynthesis fuels primary production at the base of marine food webs. Yet, in many surface ocean ecosystems, diel-driven primary production is tightly coupled to daily loss. This tight coupling raises the question: which top-down drivers predominate in maintaining persistently stable picocyanobacterial populations over longer time scales? Motivated by high-frequency surface water measurements taken in the North Pacific Subtropical Gyre (NPSG), we developed multitrophic models to investigate bottom-up and top-down mechanisms underlying the balanced control of Prochlorococcus populations. We find that incorporating photosynthetic growth with viral- and predator-induced mortality is sufficient to recapitulate daily oscillations of Prochlorococcus abundances with baseline community abundances. In doing so, we infer that grazers in this environment function as the predominant top-down factor despite high standing viral particle densities. The model-data fits also reveal the ecological relevance of light-dependent viral traits and non-canonical factors to cellular loss. Finally, we leverage sensitivity analyses to demonstrate how variation in life history traits across distinct oceanic contexts, including variation in viral adsorption and grazer clearance rates, can transform the quantitative and even qualitative importance of top-down controls in shaping Prochlorococcus population dynamics.

Understanding opposing predictions of Prochlorococcus in a changing climate.

Statistically derived species distribution models (SDMs) are increasingly used to predict ecological changes on a warming planet. For Prochlorococcus, the most abundant phytoplankton, an established statistical prediction conflicts with dynamical models as they predict large, opposite, changes in abundance. We probe the SDM at various spatial-temporal scales, showing that light and temperature fail to explain both temporal fluctuations and sharp spatial transitions. Strong correlations between changes in temperature and population emerge only at very large spatial scales, as transects pass through transitions between regions of high and low abundance. Furthermore, a two-state model based on a temperature threshold matches the original SDM in the surface ocean. We conclude that the original SDM has little power to predict changes when Prochlorococcus is already abundant, which resolves the conflict with dynamical models. Our conclusion suggests that SDMs should prove efficacy across multiple spatial-temporal scales before being trusted in a changing ocean.

Ocean mover's distance: using optimal transport for analysing oceanographic data.

Remote sensing observations from satellites and global biogeochemical models have combined to revolutionize the study of ocean biogeochemical cycling, but comparing the two data streams to each other and across time remains challenging due to the strong spatial-temporal structuring of the ocean. Here, we show that the Wasserstein distance provides a powerful metric for harnessing these structured datasets for better marine ecosystem and climate predictions. The Wasserstein distance complements commonly used point-wise difference methods such as the root-mean-squared error, by quantifying differences in terms of spatial displacement in addition to magnitude. As a test case, we consider chlorophyll (a key indicator of phytoplankton biomass) in the northeast Pacific Ocean, obtained from model simulations, in situ measurements, and satellite observations. We focus on two main applications: (i) comparing model predictions with satellite observations, and (ii) temporal evolution of chlorophyll both seasonally and over longer time frames. The Wasserstein distance successfully isolates temporal and depth variability and quantifies shifts in biogeochemical province boundaries. It also exposes relevant temporal trends in satellite chlorophyll consistent with climate change predictions. Our study shows that optimal transport vectors underlying the Wasserstein distance provide a novel visualization tool for testing models and better understanding temporal dynamics in the ocean.

Trophic interactions with heterotrophic bacteria limit the range of Prochlorococcus.

Prochlorococcus is both the smallest and numerically most abundant photosynthesizing organism on the planet. While thriving in the warm oligotrophic gyres, Prochlorococcus concentrations drop rapidly in higher-latitude regions. Transect data from the North Pacific show the collapse occurring at a wide range of temperatures and latitudes (temperature is often hypothesized to cause this shift), suggesting an ecological mechanism may be at play. An often used size-based theory of phytoplankton community structure that has been incorporated into computational models correctly predicts the dominance of Prochlorococcus in the gyres, and the relative dominance of larger cells at high latitudes. However, both theory and computational models fail to explain the poleward collapse. When heterotrophic bacteria and predators that prey nonspecifically on both Prochlorococcus and bacteria are included in the theoretical framework, the collapse of Prochlorococcus occurs with increasing nutrient supplies. The poleward collapse of Prochlorococcus populations then naturally emerges when this mechanism of "shared predation" is implemented in a complex global ecosystem model. Additionally, the theory correctly predicts trends in both the abundance and mean size of the heterotrophic bacteria. These results suggest that ecological controls need to be considered to understand the biogeography of Prochlorococcus and predict its changes under future ocean conditions. Indirect interactions within a microbial network can be essential in setting community structure.

Moving ecological and biogeochemical transitions across the North Pacific.

In the North Pacific Ocean, nutrient rich surface waters flow south from the subpolar gyre through a transitional region and into the subtropics. Along the way, nutrients are used, recycled, and exported, leading to lower biomass and a commensurate change in ecosystem structure moving southward. We focus on the region between the two gyres (the Transition Zone) using a coupled biophysical ocean model, remote sensing, floats, and cruise data to explore the nature of the physical, biogeochemical, and ecological fields in this region. Nonlinear interactions between biological processes and the meridional gradient in nutrient supply lead to sharp shifts across this zone. These transitions between a southern region with more uniform biological and biogeochemical properties and steep meridional gradients to the north are diagnosed from extrema in the first derivative of the properties with latitude. Some transitions like that for chlorophyll a (the transition zone chlorophyll front [TZCF]) experience large seasonal excursions while the location of the transitions in other properties moves very little. The seasonal shifts are not caused by changes in the horizontal flow field, but rather by the interaction of seasonal, depth related, forcing with the mean latitudinal gradients. Focusing on the TZCF as a case study, we express its phase velocity in terms of vertical nutrient flux and internal ecosystem processes, demonstrating their nearly equal influence on its motion. This framework of propagating biogeochemical transitions can be systematically expanded to better understand the processes that structure ecosystems and biogeochemistry in the North Pacific and beyond.

Carbon Transfer from the Host Diatom Enables Fast Growth and High Rate of N2 Fixation by Symbiotic Heterocystous Cyanobacteria.

Diatom-diazotroph associations (DDAs) are symbioses where trichome-forming cyanobacteria support the host diatom with fixed nitrogen through dinitrogen (N2) fixation. It is inferred that the growth of the trichomes is also supported by the host, but the support mechanism has not been fully quantified. Here, we develop a coarse-grained, cellular model of the symbiosis between Hemiaulus and Richelia (one of the major DDAs), which shows that carbon (C) transfer from the diatom enables a faster growth and N2 fixation rate by the trichomes. The model predicts that the rate of N2 fixation is 5.5 times that of the hypothetical case without nitrogen (N) transfer to the host diatom. The model estimates that 25% of fixed C from the host diatom is transferred to the symbiotic trichomes to support the high rate of N2 fixation. In turn, 82% of N fixed by the trichomes ends up in the host. Modeled C fixation from the vegetative cells in the trichomes supports only one-third of their total C needs. Even if we ignore the C cost for N2 fixation and for N transfer to the host, the total C cost of the trichomes is higher than the C supply by their own photosynthesis. Having more trichomes in a single host diatom decreases the demand for N2 fixation per trichome and thus decreases their cost of C. However, even with five trichomes, which is about the highest observed for Hemiaulus and Richelia symbiosis, the model still predicts a significant C transfer from the diatom host. These results help quantitatively explain the observed high rates of growth and N2 fixation in symbiotic trichomes relative to other aquatic diazotrophs.

Can Rates of Ocean Primary Production and Biological Carbon Export Be Related Through Their Probability Distributions?

We describe the basis of a theory for interpreting measurements of two key biogeochemical fluxes-primary production by phytoplankton (p, µg C · L-1 · day-1) and biological carbon export from the surface ocean by sinking particles (f, mg C · m-2 · day-1)-in terms of their probability distributions. Given that p and f are mechanistically linked but variable and effectively measured on different scales, we hypothesize that a quantitative relationship emerges between collections of the two measurements. Motivated by the many subprocesses driving production and export, we take as a null model that large-scale distributions of p and f are lognormal. We then show that compilations of p and f measurements are consistent with this hypothesis. The compilation of p measurements is extensive enough to subregion by biome, basin, depth, or season; these subsets are also well described by lognormals, whose log-moments sort predictably. Informed by the lognormality of both p and f we infer a statistical scaling relationship between the two quantities and derive a linear relationship between the log-moments of their distributions. We find agreement between two independent estimates of the slope and intercept of this line and show that the distribution of f measurements is consistent with predictions made from the moments of the p distribution. These results illustrate the utility of a distributional approach to biogeochemical fluxes. We close by describing potential uses and challenges for the further development of such an approach.

Seasonal resource conditions favor a summertime increase in North Pacific diatom-diazotroph associations.

In the North Pacific Subtropical Gyre (NPSG), an annual pulse of sinking organic carbon is observed at 4000 m between July and August, driven by large diatoms found in association with nitrogen fixing, heterocystous, cyanobacteria: Diatom-Diazotroph Associations (DDAs). Here we ask what drives the bloom of DDAs and present a simplified trait-based model of subtropical phototroph populations driven by observed, monthly averaged, environmental characteristics. The ratio of resource supply rates favors nitrogen fixation year round. The relative fitness of DDA traits is most competitive in early summer when the mixed layer is shallow, solar irradiance is high, and phosphorus and iron are relatively abundant. Later in the season, as light intensity drops and phosphorus is depleted, the traits of small unicellular diazotrophs become more competitive. The competitive transition happens in August, at the time when the DDA export event occurs. This seasonal dynamic is maintained when embedded in a more complex, global-scale, ecological model, and provides predictions for the extent of the North Pacific DDA bloom. The model provides a parsimonious and testable hypothesis for the stimulation of DDA blooms.

Hidden cycle of dissolved organic carbon in the deep ocean.

Marine dissolved organic carbon (DOC) is a large (660 Pg C) reactive carbon reservoir that mediates the oceanic microbial food web and interacts with climate on both short and long timescales. Carbon isotopic content provides information on the DOC source via δ(13)C and age via Δ(14)C. Bulk isotope measurements suggest a microbially sourced DOC reservoir with two distinct components of differing radiocarbon age. However, such measurements cannot determine internal dynamics and fluxes. Here we analyze serial oxidation experiments to quantify the isotopic diversity of DOC at an oligotrophic site in the central Pacific Ocean. Our results show diversity in both stable and radio isotopes at all depths, confirming DOC cycling hidden within bulk analyses. We confirm the presence of isotopically enriched, modern DOC cocycling with an isotopically depleted older fraction in the upper ocean. However, our results show that up to 30% of the deep DOC reservoir is modern and supported by a 1 Pg/y carbon flux, which is 10 times higher than inferred from bulk isotope measurements. Isotopically depleted material turns over at an apparent time scale of 30,000 y, which is far slower than indicated by bulk isotope measurements. These results are consistent with global DOC measurements and explain both the fluctuations in deep DOC concentration and the anomalous radiocarbon values of DOC in the Southern Ocean. Collectively these results provide an unprecedented view of the ways in which DOC moves through the marine carbon cycle.

Closely related phytoplankton species produce similar suites of dissolved organic matter.

Production of dissolved organic matter (DOM) by marine phytoplankton supplies the majority of organic substrate consumed by heterotrophic bacterioplankton in the sea. This production and subsequent consumption converts a vast quantity of carbon, nitrogen, and phosphorus between organic and inorganic forms, directly impacting global cycles of these biologically important elements. Details regarding the chemical composition of DOM produced by marine phytoplankton are sparse, and while often assumed, it is not currently known if phylogenetically distinct groups of marine phytoplankton release characteristic suites of DOM. To investigate the relationship between specific phytoplankton groups and the DOM they release, hydrophobic phytoplankton-derived dissolved organic matter (DOMP) from eight axenic strains was analyzed using high-performance liquid chromatography coupled to mass spectrometry (HPLC-MS). Identification of DOM features derived from Prochlorococcus, Synechococcus, Thalassiosira, and Phaeodactylum revealed DOMP to be complex and highly strain dependent. Connections between DOMP features and the phylogenetic relatedness of these strains were identified on multiple levels of phylogenetic distance, suggesting that marine phytoplankton produce DOM that in part reflects its phylogenetic origin. Chemical information regarding the size and polarity ranges of features from defined biological sources was also obtained. Our findings reveal DOMP composition to be partially conserved among related phytoplankton species, and implicate marine DOM as a potential factor influencing microbial diversity in the sea by acting as a link between autotrophic and heterotrophic microbial community structures.