Matthew J. Church

Ocean particles are a heterogeneous collection, including living and dead cells, feces, mucus‐rich aggregates, and mineral shells and frustules. In the well‐lit upper ocean, phototrophic processes fuel production of particulate matter; however, only a relatively small percentage (< 10% per day) of this material (mostly detrital) escapes the recycling‐intensive upper ocean, transiting downward by gravitational settling. In the North Pacific Subtropical Gyre, sinking particles are considered the major pathway supporting the vertical export of material to the mesopelagic zone. In the summer of 2021, an expedition explored a phytoplankton bloom, constrained within an anticyclonic eddy, that was detected from satellite chlorophyll products. Extensive near‐Lagrangian sampling of this bloom revealed a decaying population of diatoms containing diazotrophic symbionts imprinted over a relatively stable population of picocyanobacteria. Strong top‐down control appears to have led to the termination of this diazotrophy‐fueled growth, as evidenced by the prevalence of empty diatom frustules, incomplete drawdown of inorganic nutrients, and the presence and activity of protistan grazers/parasites coincident with the timing of bloom decline. Sinking rates of diatom frustules were ~ 50–100 m d ⁻¹ and drove elevated fluxes of carbon, nitrogen, and silicate into the mesopelagic zone, roughly 2–3× the regular summer fluxes measured at the nearby sampling station of the Hawaii Ocean Time‐series. While phytoplankton blooms are regular occurrences in this region, it is rare to sample their decay. The observations from the bloom demise described here highlight the significance of non‐steady‐state events in a region generally typified as a stable ecosystem.

Oceanic microorganisms can rapidly respond to environmental variability. Determining how physical and biological processes control microbial distributions, abundances, and metabolic dynamics is challenging. Here, we used autonomous underwater vehicles capable of Lagrangian feature tracking and in situ sampling, in combination with ship-based measurements, to examine diel to weekly scale changes in microbial transcription and biogeochemistry in the deep chlorophyll maximum (DCM) of a mesoscale cyclonic eddy. Nearly 20% of total transcript expression showed diel periodicity, highlighting the importance of the diurnal cycle on phytoplankton metabolism in the dim waters of the DCM. Eddy-induced isopycnal uplift increased nutrient concentrations and caused upward displacement of the DCM, driving increased picoeukaryotic cell abundances and transcriptional activity of nitrate-incorporating photoautotrophs. As the eddy weakened, the DCM deepened and transcriptional activity shifted towards chemolithoautotrophic ammonia-oxidizing archaea. The temporal dynamics observed demonstrate how plankton communities rapidly respond to both diel variation and stochastic mesoscale disturbances.

The metabolism of heterotrophic bacteria acts as a key control on the turnover of organic matter in the ocean. However, much remains unknown about how nutrient availability, particularly iron concentration, impacts bacterial growth. In the dimly lit waters of the lower photic and upper mesopelagic zones, the attenuation of sinking particulate flux is intense, due in part to remineralization by heterotrophic bacteria. In the North Pacific Subtropical Gyre, dissolved iron concentrations display a subsurface minimum near the base of the photic zone, and this is also a region where bacteria have elevated cellular iron demands. In a series of field experiments, we examined how the availability of iron, nitrogen, and organic carbon impacts bacterial metabolism in the lower photic zone. Results of these experiments suggest that low iron conditions limit the turnover of organic carbon by bacteria, potentially enhancing the efficiency of organic carbon export to the deep sea. Uptake of both dissolved iron and inorganic nitrogen by heterotrophic bacteria was greatest when bacteria metabolized carbon‐rich organic substrates, typical of the lower photic zone, compared to particulate material collected in the near‐surface ocean. Vertical changes in the composition of organic matter may be an important control on bacterial cellular iron requirements, potentially pushing this community toward iron limitation in the interior waters of the ocean.

Biological nitrogen fixation is a key driver of global primary production and climate. Decades of effort have repeatedly updated nitrogen fixation estimates for terrestrial and open ocean systems, yet other aquatic systems in between have largely been ignored. Here we present an evaluation of nitrogen fixation for inland and coastal waters. We demonstrate that water column and sediment nitrogen fixation is ubiquitous across these diverse aquatic habitats, with rates ranging six orders of magnitude. We conservatively estimate that, despite accounting for less than 10% of the global surface area, inland and coastal aquatic systems fix 40 (30 to 54) teragrams of nitrogen per year, equivalent to 15% of the nitrogen fixed on land and in the open ocean. Inland systems contribute more than half of this biological nitrogen fixation.

Uncertainties in the temporal and spatial patterns of marine primary production and respiration limit our understanding of the ocean carbon (C) cycle and our ability to predict its response to environmental changes. Here we present a comprehensive time‐series analysis of plankton metabolism at the Hawaii Ocean Time‐series program site, Station ALOHA, in the North Pacific Subtropical Gyre. Vertical profiles of gross oxygen production (GOP) and community respiration (CR) were quantified using the ¹⁸ O‐labeled water method together with net changes in O ₂ to Ar ratios during dawn to dusk in situ incubations. Rates of ¹⁴ C‐bicarbonate assimilation ( ¹⁴ C‐based primary production [ ¹⁴ C‐PP]) were also determined concurrently. During the observational period (April 2015 to July 2020), euphotic zone depth‐integrated (0–125 m) GOP and ¹⁴ C‐PP ranged from 35 to 134 mmol O ₂ m ⁻² d ⁻¹ and 18 to 75 mmol C m ⁻² d ⁻¹ , respectively, while CR ranged from 37 to 187 mmol O ₂ m ⁻² d ⁻¹ . All biological rates varied with depth and season, with seasonality most pronounced in the lower portion of the euphotic zone (75–125 m). The mean annual ratio of GOP to ¹⁴ C‐PP was 1.7 ± 0.1 mol O ₂ (mol C) ⁻¹ . While previous studies have reported convergence of GOP and ¹⁴ C‐PP with depth, we find a less pronounced vertical decline in the GOP to ¹⁴ C‐PP ratios, with GOP exceeding ¹⁴ C‐PP by 50% or more in the lower euphotic zone. Variability in CR was higher than for GOP, driving most of the variability in the balance between the two.

Biological nitrogen fixation is the conversion of dinitrogen (N₂) gas into bioavailable nitrogen by microorganisms with consequences for primary production, ecosystem function, and global climate. Here we present a compiled dataset of 4793 nitrogen fixation (N₂‐fixation) rates measured in the water column and benthos of inland and coastal systems via the acetylene reduction assay, ¹⁵N₂ labeling, or N₂/Ar technique. While the data are distributed across seven continents, most observations (88%) are from the northern hemisphere. ¹⁵N₂ labeling accounted for 67% of water column measurements, while the acetylene reduction assay accounted for 81% of benthic N₂‐fixation observations. Dataset median area‐, volume‐, and mass‐normalized N₂‐fixation rates are 7.1 μmol N₂‐N m⁻² h⁻¹, 2.3 × 10⁻⁴ μmol N₂‐N L⁻¹ h⁻¹, and 4.8 × 10⁻⁴ μmol N₂‐N g⁻¹ h⁻¹, respectively. This dataset will facilitate future efforts to study and scale N₂‐fixation contributions across inland and coastal aquatic environments.

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.

Most deep-ocean life relies on organic carbon from the surface ocean. While settling primary production rapidly attenuates in the water column, pulses of organic material can be quickly transported to depth in the form of food falls. One example of fresh material that can reach great depths across the tropical Atlantic Ocean and Caribbean Sea is the pelagic macroalgae Sargassum . However, little is known about the deep-ocean organisms able to use this food source. Here, we encountered the isopod Bathyopsurus nybelini at depths 5002–6288 m in the Puerto Rico Trench and Mid-Cayman Spreading Center using the Deep Submergence Vehicle Alvin . In most of the 32 observations, the isopods carried fronds of Sargassum . Through an integrative suite of morphological, DNA sequencing, and microbiological approaches, we show that this species is adapted to feed on Sargassum by using a specialized swimming stroke, having serrated and grinding mouthparts, and containing a gut microbiome that provides a dietary contribution through the degradation of macroalgal polysaccharides and fixing nitrogen. The isopod’s physiological, morphological, and ecological adaptations demonstrate that vertical deposition of Sargassum is a direct trophic link between the surface and deep ocean and that some deep-sea organisms are poised to use this material.