Edward F. DeLong’s research while affiliated with Honolulu University and other places

Mesoscale eddies, horizontally rotating currents sometimes referred to as “ocean weather,” influence open ocean macronutrient distributions, primary production, and microbial community structure. Such eddies impact ecosystems like the North Pacific Subtropical Gyre, where year-round thermal stratification limits the mixing of subsurface macronutrients with surface waters. Populations of the dominant primary producer Prochlorococcusin the North Pacific Subtropical Gyre consist of genetic variants with differential adaptive traits to light intensity, temperature, and macronutrient availability. How Prochlorococcuspopulation variants respond to transient, localized environmental changes, however, remains an open question. Leveraging microbial community phylogenetic, metagenomic, and metatranscriptomic data, we report here a consistent, specific enrichment of Prochlorococcushigh-light I ecotypes around the deep chlorophyll maximum in cyclonic eddies, but not adjacent anticyclonic eddies. The shallower deep chlorophyll maximum depths of cyclones had lower temperatures, higher light intensities, and elevated nutrient concentrations compared to adjacent anticyclones, which favored Prochlorococcushigh-light I ecotype proliferation. Prochlorococcushigh-light I ecotypes in the cyclone deep chlorophyll maximum exhibited unique genetic traits related to nitrogen metabolism and were enriched in gene transcripts associated with energy production, cell replication, and proliferation. Prochlorococcusgene transcripts involved in amino acid transport, metabolism, and biosynthesis were also elevated in the cyclone. These results suggest the potential importance of nitrogen metabolism in Prochlorococcushigh-light I ecotype proliferation in cyclonic eddies. Our findings demonstrate how mesoscale eddies shape microbial community structure in the oligotrophic ocean and how Prochlorococcuscommunities respond to short-term localized environmental variability.

Horizontal gene transfer (HGT) is enabled in part through the movement of DNA within two broad groups of small (<0.2 µm), diffusible nanoparticles: extracellular vesicles (EVs) and virus-like particles (VLPs; including viruses, gene transfer agents, and phage satellites). The information enclosed within these structures represents a substantial portion of the HGT potential available in planktonic ecosystems, but whether some genes might be preferentially transported through one type of nanoparticle versus another is unknown. Here we use long-read sequencing to compare the genetic content of EVs and VLPs from the oligotrophic North Pacific. Fractionated EV-enriched and VLP-enriched subpopulations contain diverse DNA from the surrounding microbial community, but differ in their capacity and encoded functions. The sequences carried by both particle types are enriched in mobile genetic elements (MGEs) as compared with other cellular chromosomal regions, and we highlight how this property enables novel MGE discovery. Examining the Pelagibacter mobilome reveals >7200 distinct chromosomal fragments and MGEs, many differentially partitioned between EVs and VLPs. Together these results suggest that distinctions in nanoparticle contents contribute to the mode and trajectory of microbial HGT networks and evolutionary dynamics in natural habitats.

Ocean eddies are mesoscale features that can extend > 100 km and maintain cohesiveness for months, impacting planktonic community structure and water column biogeochemical cycles. Standing stocks of protists in the water column and on sinking particles were investigated using microscopy, in situ imagery, and metabarcoding across an anticyclonic to cyclonic eddy dipole in the North Pacific Subtropical Gyre during July 2017. The water column was sampled from the surface to 500 m and particle interceptor traps were deployed at 150 m. Protistan assemblage composition varied substantially between sample type and analytical approach across the eddy dipole. Alveolates represented 63% of sequences from water samples. In contrast to water samples, rhizarian protists represented 79% of trap sequences obtained by metabarcoding of sediment trap material. Microscopy of trap material supported the important contribution of Rhizaria to sinking particles and revealed increased relative abundances of ciliates in the anticyclonic eddy and diatoms in the cyclonic eddy. In situ imagery confirmed the presence of relatively large Rhizaria that were not adequately assessed from water samples but contributed significantly to particle flux. Together, these data demonstrate differing perspectives of planktonic protistan community composition and contributions to sinking particles gained from the application of different sampling and analytic approaches. Our observations and analyses indicate a specific subset of the protistan community contributed disproportionately to organic matter downward export.

The North Pacific subtropical gyre is a globally important contributor to carbon uptake despite being a persistently oligotrophic ecosystem. Supply of the micronutrient iron to the upper ocean varies seasonally to episodically, and when coupled with rapid biological consumption, results in low iron concentrations. In this study, we examined changes in iron uptake rates, along with siderophore concentrations and biosynthesis potential at Station ALOHA across time (2013–2016) and depth (surface to 500 m) to observe changes in iron acquisition and internal cycling by the microbial community. The genetic potential for siderophore biosynthesis was widespread throughout the upper water column, and biosynthetic gene clusters peaked in spring and summer along with siderophore concentrations, suggesting changes in nutrient delivery, primary production, and carbon export seasonally impact iron acquisition. Dissolved iron turnover times, calculated from iron‐amended experiments in surface (15 m) and mesopelagic (300 m) waters, ranged from 9 to 252 d. The shortest average turnover times at both depths were associated with inorganic iron additions (14 ± 9 d) and the longest with iron bound to strong siderophores (148 ± 225 d). Uptake rates of siderophore‐bound iron were faster in mesopelagic waters than in the surface, leading to high Fe : C uptake ratios of heterotrophic bacteria in the upper mesopelagic. The rapid cycling and high demand for iron at 300 m suggest differences in microbial metabolism and iron acquisition in the mesopelagic compared to surface waters. Together, changes in siderophore production and consumption over the seasonal cycle suggest organic carbon availability impacts iron cycling at Station ALOHA.

Horizontal gene transfer (HGT) is enabled in part through the movement of DNA within two broad groups of small (<0.2 µm), diffusible nanoparticles: extracellular vesicles (EVs) and virus-like particles (VLPs; including viruses, gene transfer agents, and phage satellites). These structures enclose a substantial portion of the HGT potential in planktonic ecosystems, but whether genes move preferentially through one type of nanoparticle versus another is unknown. Here we show that EVs and VLPs from the oligotrophic ocean differ in their DNA capacity and encoded functions. Both particle types are enriched in mobile genetic elements (MGEs), and we highlight how this property enables novel MGE discovery. Examining the Pelagibacter mobilome reveals >7200 diverse chromosomal fragments and MGEs, many differentially partitioned between EVs and VLPs. Together these results suggest that distinctions in nanoparticle contents contribute to the mode and trajectory of microbial HGT networks and evolutionary dynamics in natural habitats.

A considerable amount of particulate carbon produced by oceanic photosynthesis is exported to the deep-sea by the “gravitational pump” (~6.8 to 7.7 Pg C/year), sequestering it from the atmosphere for centuries. How particulate organic carbon (POC) is transformed during export to the deep sea however is not well understood. Here, we report that dominant suspended prokaryotes also found in sinking particles serve as informative tracers of particle export processes. In a three-year time series from oceanographic campaigns in the Pacific Ocean, upper water column relative abundances of suspended prokaryotes entrained in sinking particles decreased exponentially from depths of 75 to 250 m, conforming to known depth-attenuation patterns of carbon, energy, and mass fluxes in the epipelagic zone. Below ~250 m however, the relative abundance of suspended prokaryotes entrained in sinking particles increased with depth. These results indicate that microbial entrainment, colonization, and sinking particle formation are elevated at mesopelagic and bathypelagic depths. Comparison of suspended and sinking particle-associated microbes provides information about the depth-variability of POC export and biotic processes, that is not evident from biogeochemical data alone.

Oxygen-deficient marine waters referred to as oxygen minimum zones (OMZs) or anoxic marine zones (AMZs) are common oceanographic features. They host both cosmopolitan and endemic microorganisms adapted to low oxygen conditions. Microbial metabolic interactions within OMZs and AMZs drive coupled biogeochemical cycles resulting in nitrogen loss and climate active trace gas production and consumption. Global warming is causing oxygen-deficient waters to expand and intensify. Therefore, studies focused on microbial communities inhabiting oxygen-deficient regions are necessary to both monitor and model the impacts of climate change on marine ecosystem functions and services. Here we present a compendium of 5,129 single-cell amplified genomes (SAGs) from marine environments encompassing representative OMZ and AMZ geochemical profiles. Of these, 3,570 SAGs have been sequenced to different levels of completion, providing a strain-resolved perspective on the genomic content and potential metabolic interactions within OMZ and AMZ microbiomes. Hierarchical clustering confirmed that samples from similar oxygen concentrations and geographic regions also had analogous taxonomic compositions, providing a coherent framework for comparative community analysis.

Mesoscale eddies have been shown to support elevated dinitrogen (N2) fixation rates (NFRs) and abundances of N2‐fixing microorganisms (diazotrophs), but the mechanisms underlying these observations are not well understood. We sampled two pairs of mesoscale cyclones and anticyclones in the North Pacific Subtropical Gyre in 2017 and 2018 and compared our observations with seasonal patterns from the Hawaii Ocean Time‐series (HOT) program. Consistent with previous reports, we found that NFRs were anomalously high for this region (up to 3.7‐fold above previous monthly HOT observations) in the centers of both sampled anticyclones. In 2017, these elevated rates coincided with high concentrations of the diazotroph Crocosphaera. We then coupled our field‐based observations, together with transcriptomic analyses of nutrient stress marker genes and ecological models, to evaluate the role of biological (via estimates of growth and grazing rates) and physical controls on populations of Crocosphaera, Trichodesmium, and diatom symbionts at the mesoscale. Our results suggest that increased Crocosphaera abundances in the 2017 anticyclone resulted from the alleviation of phosphate limitation, allowing cells to grow at rates exceeding grazing losses. In contrast, distributions of larger, buoyant taxa (Trichodesmium and diatom symbionts) appeared less affected by eddy‐driven biological controls. Instead, they appeared driven by physical dynamics along frontal boundaries that separate cyclonic and anticyclonic eddies. No examined controls were able to explain our 2018 findings of higher NFRs in the anticyclone. A generalized explanation of elevated NFRs in mesoscale eddies remains challenging due to the interplay of eddy‐driven bottom‐up, top‐down, and physical control mechanisms.