Alexandra Z. Worden’s research while affiliated with University of Illinois Chicago and other places

Marine eastern boundary current ecosystems, such as the California Current System (CCS), involve productive, mesotrophic transition zones. The CCS exhibits highly variable primary production (PP), yet factors driving the variability and underlying phytoplankton communities remain poorly understood. We integrated physicochemical and biological data from surface waters sampled during 10 CCS expeditions, spanning 13 yr, and resolved regimes with distinct phytoplankton communities. Additional to an oligotrophic regime (OR), mesotrophic waters beyond the coastal area partitioned into Meso‐High and Meso‐Low regimes, differing in nitrate concentrations and PP. The OR was dominated by Prochlorococcus High‐Light I (HLI), and eukaryotic phytoplankton were largely predatory mixotrophs. Eukaryotes dominated Meso‐Low and Meso‐High phytoplankton biomass. Within the Meso‐Low, Pelagomonas calceolata was important, and Prochlorococcus Low‐Light I (LLI) rose in prominence. In the Meso‐High, the picoprasinophyte Ostreococcus lucimarinus was abundant, and Synechococcus Clade IV was notable. The Meso‐High exhibited the highest PP (38 ± 16 mg C m⁻³ d⁻¹; p < 0.01) and higher growth rates for photosynthetic eukaryotes (0.84 ± 0.02 d⁻¹) than for Prochlorococcus (0.61 ± 0.01 d⁻¹) and Synechococcus (0.31 ± 0.05 d⁻¹). An experiment simulating seasonal oligotrophic seawater intrusion into the Meso‐High resulted in growth rates reaching 1.18 ± 0.10 d⁻¹ (O. lucimarinus), 0.75 ± 0.21 d⁻¹ (Prochlorococcus LLI), and 0.50 ± 0.04 d⁻¹ (Synechococcus EPC2). Thus, variable PP is underpinned by distinct phytoplankton communities across CCS mesotrophic regimes, and their dynamic nature is influenced by the rapidity with which specific taxa respond to changing environmental conditions or possibly transient nutrient release from viral encounters. Future work should assess whether these dynamics are consistent across eastern boundary current ecosystems and over temporal variations.

Predictions of how the biogeochemical reservoir of marine dissolved organic matter (DOM) will respond to future ocean changes require an improved understanding of the thousands of individual microbe-molecule interactions which regulate the transformation and fate of DOM. Bulk characterizations of organic matter can mask this complex network of interactions comprised of rich chemical and taxonomic diversity. Here, we present a three-year, depth-resolved time-series of the seasonal dynamics of the exometabolome and the bacterioplankton community at the Bermuda Atlantic Time-series Study (BATS) site. We find both time-series to be highly structured and compositionally distinct across sampling depths. Putative exometabolite identifications (gonyol, glucose 6-sulfate, succinate, and trehalose) indicate that at least a portion of the exometabolome contains rapidly remineralized, labile molecules. We hypothesize that apparent seasonal accumulation of these labile molecules could result from environmental conditions that alter community composition on a seasonal timescale and thus shift the relative proportions of microbial functions that produce and consume the substrates. Critically, we found the composition of seasonal DOM features was more stable interannually than the microbial community structure. By estimating redundancy of metabolic functions responsible for cycling these molecules in BATS metagenomes, we propose a paradigm whereby core microbial metabolisms, either those utilized by all or by a subset of marine microbes, are better predictors of DOM composition than microbial taxonomies. The molecular-level characterization of DOM achieved herein highlights the metabolic imprint of microbial activity in DOM composition and greatly enhances our understanding of the dynamics regulating the largest reservoir of organic carbon on Earth.

Viral lysis accounts for much of microbial mortality in the ocean, and iron (Fe) is a critical micronutrient that can limit phytoplankton growth, yet interactions between Fe-nutrition and viral lysis are not well known. Here, we present viral infection dynamics under Fe-limited and Fe-replete conditions for three distinct marine microbes, the photosynthetic picoeukaryote Ostreococcus lucimarinus , the cyanobacterium Synechococcus , and two strains of the heterotrophic bacterium Vibrio . Iron limitation of Ostreococcus resulted in slowed growth, and a corresponding decrease in viral burst sizes was observed; this is similar to results from studies of larger eukaryotic phytoplankton (Slagter et al. 2016; Kranzler et al. 2021), where reduced viral replication under Fe-limitation is attributed to the viral reliance on host metabolism and replication machinery. For one strain of Vibrio , Fe-limitation similarly impacted viral dynamics, increasing the latent period before infected cells burst to release new virus, and reducing the number of infective viral particles released upon viral lysis. Unexpectedly, for another strain of Vibrio , Fe-limitation had no discernible effect on viral replication. Furthermore, dynamics of three Synechococcus cyanophages was not affected by Fe-limitation of the host, either in terms of latent period or burst size. The results illuminate the extraordinary ability of some marine viruses, particularly cyanophages, to highjack host metabolism to produce new viral particles, even when host growth is compromised. This has implications for marine ecology and carbon cycling in Fe-limited regions of the global ocean.

Passive sinking flux of particulate organic matter (POM) in the ocean plays a central role in the biological carbon pump and carbon export to the ocean’s interior. Particle-associated (PA) microbes colonize POM, producing “hotspots” of microbial activity. We evaluated variation in PA microbial communities to 500 m depth across four different particle size fractions (0.2 – 1.2 μm, 1.2 – 5 μm, 5 - 20 μm, >20 μm) collected using in situ pumps at the Bermuda Atlantic Time-series Study (BATS) site. In situ pump collections capture both sinking and suspended particles, complimenting previous studies using sediment or gel traps, which capture only sinking particles. Additionally, diagenetic state of size-fractionated particles was examined using isotopic signatures alongside microbial analysis. Our findings emphasize that different particle sizes contain distinctive microbial communities, and each size category experiences a similar degree of change in communities over depth, contradicting previous findings. The robust patterns observed in this study suggest that particle residence times may be long relative to microbial succession rates, indicating that many of the particles collected in this study may be slow sinking or neutrally buoyant. Alternatively, rapid community succession on sinking particles could explain the change between depths. Complementary isotopic analysis of particles revealed significant differences in composition between particles of different sizes and depths, indicative of organic particle transformation by microbial hydrolysis and metazoan grazing. Our results couple observed patterns in microbial communities with the diagenetic state of associated organic matter, and highlight unique successional patterns in varying particle sizes across depth.

Ocean spring phytoplankton blooms are dynamic periods important to global primary production. We document vertical patterns of a diverse suite of eukaryotic algae, the prasinophytes, in the North Atlantic Subtropical Gyre with monthly sampling over four years at the Bermuda Atlantic Time-series Study site. Water column structure was used to delineate seasonal stability periods more ecologically relevant than seasons defined by calendar dates. During winter mixing, tiny prasinophytes dominated by Class II comprise 46 ± 24% of eukaryotic algal (plastid-derived) 16S rRNA V1-V2 amplicons, specifically Ostreococcus Clade OII, Micromonas commoda, and Bathycoccus calidus. In contrast, Class VII are rare and Classes I and VI peak during warm stratified periods when surface eukaryotic phytoplankton abundances are low. Seasonality underpins a reservoir of genetic diversity from multiple prasinophyte classes during warm periods that harbor ephemeral taxa. Persistent Class II sub-species dominating the winter/spring bloom period retreat to the deep chlorophyll maximum in summer, poised to seed the mixed layer upon winter convection, exposing a mechanism for initiating high abundances at bloom onset. Comparisons to tropical oceans reveal broad distributions of the dominant sub-species herein. This unparalleled window into temporal and spatial niche partitioning of picoeukaryotic primary producers demonstrates how key prasinophytes prevail in warm oceans.

Subtropical oceans contribute significantly to global primary production, but the fate of the picophytoplankton that dominate in these low-nutrient regions is poorly understood. Working in the subtropical Mediterranean, we demonstrate that subduction of water at ocean fronts generates 3D intrusions with uncharacteristically high carbon, chlorophyll, and oxygen that extend below the sunlit photic zone into the dark ocean. These contain fresh picophytoplankton assemblages that resemble the photic-zone regions where the water originated. Intrusions propagate depth-dependent seasonal variations in microbial assemblages into the ocean interior. Strikingly, the intrusions included dominant biomass contributions from nonphotosynthetic bacteria and enrichment of enigmatic heterotrophic bacterial lineages. Thus, the intrusions not only deliver material that differs in composition and nutritional character from sinking detrital particles, but also drive shifts in bacterial community composition, organic matter processing, and interactions between surface and deep communities. Modeling efforts paired with global observations demonstrate that subduction can flux similar magnitudes of particulate organic carbon as sinking export, but is not accounted for in current export estimates and carbon cycle models. Intrusions formed by subduction are a particularly important mechanism for enhancing connectivity between surface and upper mesopelagic ecosystems in stratified subtropical ocean environments that are expanding due to the warming climate.

Bacterial communities directly influence ecological processes in the ocean, and depth has a major influence due to the changeover in primary energy sources between the sunlit photic zone and dark ocean. Here, we examine the abundance and diversity of bacteria in Monterey Bay depth profiles collected from the surface to just above the sediments (e.g., 2000 m). Bacterial abundance in these Pacific Ocean samples decreased by >1 order of magnitude, from 1.22 ±0.69 ×10⁶ cells ml⁻¹ in the variable photic zone to 1.44 ± 0.25 ×10⁵ and 6.71 ± 1.23 ×10⁴ cells ml⁻¹ in the mesopelagic and bathypelagic, respectively. V1-V2 16S rRNA gene profiling showed diversity increased sharply between the photic and mesopelagic zones. Weighted Gene Correlation Network Analysis clustered co-occurring bacterial amplicon sequence variants (ASVs) into seven subnetwork modules, of which five strongly correlated with depth-related factors. Within surface-associated modules there was a clear distinction between a ‘copiotrophic’ module, correlating with chlorophyll and dominated by e.g., Flavobacteriales and Rhodobacteraceae, and an ‘oligotrophic’ module dominated by diverse Oceanospirillales (such as uncultured JL-ETNP-Y6, SAR86) and Pelagibacterales. Phylogenetic reconstructions of Pelagibacterales and SAR324 using full-length 16S rRNA gene data revealed several additional subclades, expanding known microdiversity within these abundant lineages, including new Pelagibacterales subclades Ia.B, Id, and IIc, which comprised 4–10% of amplicons depending on the subclade and depth zone. SAR324 and Oceanospirillales dominated in the mesopelagic, with SAR324 clade II exhibiting its highest relative abundances (17±4%) in the lower mesopelagic (300–750 m). The two newly-identified SAR324 clades showed highest relative abundances in the photic zone (clade III), while clade IV was extremely low in relative abundance, but present across dark ocean depths. Hierarchical clustering placed microbial communities from 900 m samples with those from the bathypelagic, where Marinimicrobia was distinctively relatively abundant. The patterns resolved herein, through high resolution and statistical replication, establish baselines for marine bacterial abundance and taxonomic distributions across the Monterey Bay water column, against which future change can be assessed.