Variable carbon isotope fractionation of photosynthetic communities over depth in an open-ocean euphotic zone.

Marine particulate organic carbon (POC) contributes to carbon export, food webs, and sediments, but uncertainties remain in its origins. Globally, variations in stable carbon isotope ratios (δ13C values) of POC between the upper and lower euphotic zones (LEZ) indicate either varying aspects of photosynthetic communities or degradative alteration of POC. During summertime in the subtropical north Atlantic Ocean, we find that δ13C values of the photosynthetic product phytol decreased by 6.3‰ and photosynthetic carbon isotope fractionation (εp) increased by 5.6‰ between the surface and the LEZ-variation as large as that found in the geologic record during major carbon cycle perturbations, but here reflecting vertical variation in δ13C values of photosynthetic communities. We find that simultaneous variations in light intensity and phytoplankton community composition over depth may be important factors not fully accounted for in common models of photosynthetic carbon isotope fractionation. Using additional isotopic and cell count data, we estimate that photosynthetic and non-photosynthetic material (heterotrophs or detritus) contribute relatively constant proportions of POC throughout the euphotic zone but are isotopically more distinct in the LEZ. As a result, the large vertical differences in εp result in significant, but smaller, differences in the δ13C values of total POC across the same depths (2.7‰). Vertical structuring of photosynthetic communities and export potential from the LEZ may vary across current and past ocean ecosystems; thus, LEZ photosynthesis may influence the exported and/or sedimentary δ13C values of both phytol and total organic carbon and affect interpretations of εp over geologic time.

Relating Molecular Properties to the Persistence of Marine Dissolved Organic Matter with Liquid Chromatography-Ultrahigh-Resolution Mass Spectrometry.

Marine dissolved organic matter (DOM) contains a complex mixture of small molecules that eludes rapid biological degradation. Spatial and temporal variations in the abundance of DOM reflect the existence of fractions that are removed from the ocean over different time scales, ranging from seconds to millennia. However, it remains unknown whether the intrinsic chemical properties of these organic components relate to their persistence. Here, we elucidate and compare the molecular compositions of distinct DOM fractions with different lability along a water column in the North Atlantic Gyre. Our analysis utilized ultrahigh-resolution Fourier transform ion cyclotron resonance mass spectrometry at 21 T coupled to liquid chromatography and a novel data pipeline developed in CoreMS that generates molecular formula assignments and metrics of isomeric complexity. Clustering analysis binned 14 857 distinct molecular components into groups that correspond to the depth distribution of semilabile, semirefractory, and refractory fractions of DOM. The more labile fractions were concentrated near the ocean surface and contained more aliphatic, hydrophobic, and reduced molecules than the refractory fraction, which occurred uniformly throughout the water column. These findings suggest that processes that selectively remove hydrophobic compounds, such as aggregation and particle sorption, contribute to variable removal rates of marine DOM.

Role of Syndiniales parasites in depth-specific networks and carbon flux in the oligotrophic ocean.

Microbial associations that result in phytoplankton mortality are important for carbon transport in the ocean. This includes parasitism, which in microbial food webs is dominated by the marine alveolate group, Syndiniales. Parasites are expected to contribute to carbon recycling via host lysis; however, knowledge on host dynamics and correlation to carbon export remain unclear and limit the inclusion of parasitism in biogeochemical models. We analyzed a 4-year 18S rRNA gene metabarcoding dataset (2016-19), performing network analysis for 12 discrete depths (1-1000 m) to determine Syndiniales-host associations in the seasonally oligotrophic Sargasso Sea. Analogous water column and sediment trap data were included to define environmental drivers of Syndiniales and their correlation with particulate carbon flux (150 m). Syndiniales accounted for 48-74% of network edges, most often associated with Dinophyceae and Arthropoda (mainly copepods) at the surface and Rhizaria (Polycystinea, Acantharea, and RAD-B) in the aphotic zone. Syndiniales were the only eukaryote group to be significantly (and negatively) correlated with particulate carbon flux, indicating their contribution to flux attenuation via remineralization. Examination of Syndiniales amplicons revealed a range of depth patterns, including specific ecological niches and vertical connection among a subset (19%) of the community, the latter implying sinking of parasites (infected hosts or spores) on particles. Our findings elevate the critical role of Syndiniales in marine microbial systems and reveal their potential use as biomarkers for carbon export.

Marine particle size-fractionation indicates organic matter is processed by differing microbial communities on depth-specific particles.

Passive sinking flux of particulate organic matter in the ocean plays a central role in the biological carbon pump and carbon export to the ocean's interior. Particle-associated microbes colonize particulate organic matter, producing "hotspots" of microbial activity. We evaluated variation in particle-associated microbial communities to 500 m depth across four different particle size fractions (0.2-1.2, 1.2-5, 5-20, >20 µm) collected using in situ pumps at the Bermuda Atlantic Time-series Study site. In situ pump collections capture both sinking and suspended particles, complementing previous studies using sediment or gel traps, which capture only sinking particles. Additionally, the 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.

Direct observations of microbial community succession on sinking marine particles.

Microbial community dynamics on sinking particles control the amount of carbon that reaches the deep ocean and the length of time that carbon is stored, with potentially profound impacts on Earth's climate. A mechanistic understanding of the controls on sinking particle distributions has been hindered by limited depth- and time-resolved sampling and methods that cannot distinguish individual particles. Here, we analyze microbial communities on nearly 400 individual sinking particles in conjunction with more conventional composite particle samples to determine how particle colonization and community assembly might control carbon sequestration in the deep ocean. We observed community succession with corresponding changes in microbial metabolic potential on the larger sinking particles transporting a significant fraction of carbon to the deep sea. Microbial community richness decreased as particles aged and sank; however, richness increased with particle size and the attenuation of carbon export. This suggests that the theory of island biogeography applies to sinking marine particles. Changes in POC flux attenuation with time and microbial community composition with depth were reproduced in a mechanistic ecosystem model that reflected a range of POC labilities and microbial growth rates. Our results highlight microbial community dynamics and processes on individual sinking particles, the isolation of which is necessary to improve mechanistic models of ocean carbon uptake.

Recurring seasonality exposes dominant species and niche partitioning strategies of open ocean picoeukaryotic algae.

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.

Coral thermal stress and bleaching enrich and restructure reef microbial communities via altered organic matter exudation.

Coral bleaching is a well-documented and increasingly widespread phenomenon in reefs across the globe, yet there has been relatively little research on the implications for reef water column microbiology and biogeochemistry. A mesocosm heating experiment and bottle incubation compared how unbleached and bleached corals alter dissolved organic matter (DOM) exudation in response to thermal stress and subsequent effects on microbial growth and community structure in the water column. Thermal stress of healthy corals tripled DOM flux relative to ambient corals. DOM exudates from stressed corals (heated and/or previously bleached) were compositionally distinct from healthy corals and significantly increased growth of bacterioplankton, enriching copiotrophs and putative pathogens. Together these results demonstrate how the impacts of both short-term thermal stress and long-term bleaching may extend into the water column, with altered coral DOM exudation driving microbial feedbacks that influence how coral reefs respond to and recover from mass bleaching events.

Suboxic DOM is bioavailable to surface prokaryotes in a simulated overturn of an oxygen minimum zone, Devil's Hole, Bermuda.

Oxygen minimum zones (OMZs) are expanding due to increased sea surface temperatures, subsequent increased oxygen demand through respiration, reduced oxygen solubility, and thermal stratification driven in part by anthropogenic climate change. Devil's Hole, Bermuda is a model ecosystem to study OMZ microbial biogeochemistry because the formation and subsequent overturn of the suboxic zone occur annually. During thermally driven stratification, suboxic conditions develop, with organic matter and nutrients accumulating at depth. In this study, the bioavailability of the accumulated dissolved organic carbon (DOC) and the microbial community response to reoxygenation of suboxic waters was assessed using a simulated overturn experiment. The surface inoculated prokaryotic community responded to the deep (formerly suboxic) 0.2 µm filtrate with cell densities increasing 2.5-fold over 6 days while removing 5 µmol L-1 of DOC. After 12 days, the surface community began to shift, and DOC quality became less diagenetically altered along with an increase in SAR202, a Chloroflexi that can degrade recalcitrant dissolved organic matter (DOM). Labile DOC production after 12 days coincided with an increase of Nitrosopumilales, a chemoautotrophic ammonia oxidizing archaea (AOA) that converts ammonia to nitrite based on the ammonia monooxygenase (amoA) gene copy number and nutrient data. In comparison, the inoculation of the deep anaerobic prokaryotic community into surface 0.2 µm filtrate demonstrated a die-off of 25.5% of the initial inoculum community followed by a 1.5-fold increase in cell densities over 6 days. Within 2 days, the prokaryotic community shifted from a Chlorobiales dominated assemblage to a surface-like heterotrophic community devoid of Chlorobiales. The DOM quality changed to less diagenetically altered material and coincided with an increase in the ribulose-1,5-bisphosphate carboxylase/oxygenase form I (cbbL) gene number followed by an influx of labile DOM. Upon reoxygenation, the deep DOM that accumulated under suboxic conditions is bioavailable to surface prokaryotes that utilize the accumulated DOC initially before switching to a community that can both produce labile DOM via chemoautotrophy and degrade the more recalcitrant DOM.