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While planktonic microbes play key roles in the coastal oceans, our understanding of heterotrophic microeukaryotes’ ecology, particularly their spatiotemporal patterns, drivers, and functions, remains incomplete. In this study, we focus on a ubiquitous marine fungus-like protistan group, the Labyrinthulomycetes, whose biomass can exceed that of bacterioplankton in coastal oceans but whose ecology is largely unknown. Using quantitative PCR and amplicon sequencing of their 18S rRNA genes, we examine their community variation in repeated five-station transects across the nearshore-to-offshore surface waters of North Carolina, United States. Their total 18S rRNA gene abundance and phylotype richness decrease significantly from the resource-rich nearshore to the oligotrophic offshore waters, but their Pielou’s community evenness appears to increase offshore. Similar to the bacteria and fungi, the Labyrinthulomycete communities are significantly structured by distance from shore, water temperature, and other environmental factors, suggesting potential niche partitioning. Nevertheless, only several Labyrinthulomycete phylotypes, which belong to aplanochytrids, thraustochytrids, or unclassified Labyrinthulomycetes, are prevalent and correlated with cohesive bacterial communities, while more phylotypes are patchy and often co-occur with fungi. Overall, these results complement previous time-series observations that resolve the Labyrinthulomycetes as persistent and short-blooming ecotypes with distinct seasonal preferences, further revealing their partitioning spatial patterns and multifaceted roles in coastal marine microbial food webs. 

ABSTRACT Labyrinthulomycetes protists are an important heterotrophic component of microeukaryotes in the world’s oceans, but their distribution patterns and ecological roles are poorly understood in pelagic waters. This study employed flow cytometry and high-throughput sequencing to characterize the abundance, diversity, and community structure of Labyrinthulomycetes in the pelagic Eastern Indian Ocean. The total Labyrinthulomycetes abundance varied much more among stations than did the abundance of prokaryotic plankton, reaching over 1,000 cells mL −1 at a few “bloom” stations. The total Labyrinthulomycetes abundance did not decline with depth throughout the whole water column (5 to 2,000 m) like the abundance of prokaryotic plankton did, and the Labyrinthulomycetes average projected biomass over all samples was higher than that of the prokaryotic plankton. However, Labyrinthulomycetes diversity showed obvious vertical variations, with richness, Shannon diversity, and evenness greatest in the upper epipelagic, lower epipelagic, and deep waters, respectively. Many abundant phylotypes were detected across multiple water layers, which aligned with the constant vertical Labyrinthulomycetes biomass, suggesting potential sinking and contribution to the biological pump. Hierarchical clustering revealed distinct ecotypes partitioning by vertical distribution patterns, suggesting their differential roles in the carbon cycle and storage processes. Particularly, most phylotypes showed patchy distributions (occurring in only few samples) as previously found in the coastal waters, but they were less associated with the Labyrinthulomycetes blooms than the prevalent phylotypes. Overall, this study revealed distinct patterns of Labyrinthulomycetes ecotypes and shed light on their importance in the pelagic ocean carbon cycling and sequestration relative to that of the prokaryotic plankton. IMPORTANCE While prokaryotic heterotrophic plankton are well accepted as major players in oceanic carbon cycling, the ecological distributions and functions of their microeukaryotic counterparts in the pelagic ocean remain largely unknown. This study focused on an important group of heterotrophic (mainly osmotrophic) protistan microbes, the Labyrinthulomycetes, whose biomass can surpass that of the prokaryotic plankton in many marine ecosystems, including the bathypelagic ocean. We found patchy horizontal but persistent vertical abundance profiles of the Labyrinthulomycetes protists in the pelagic waters of the Eastern Indian Ocean, which were distinct from the spatial patterns of the prokaryotic plankton. Moreover, multiple Labyrinthulomycetes ecotypes with distinct vertical patterns were detected and, based on the physiologic, metabolic, and genomic understanding of their cultivated relatives, were inferred to play multifaceted key roles in the carbon cycle and sequestration, particularly as contributors to the vertical carbon export from the surface to the dark ocean, i.e., the biological pump. 

Understanding the interplay of ocean physics and biology at the submesoscale and below (<30 km) is an ongoing challenge in oceanography. While poorly constrained, these scales may be of critical importance for understanding how changing ocean dynamics will impact marine ecosystems. Fronts in the ocean, regions where two disparate water masses meet and isopycnals become tilted toward vertical, are considered hotspots for biophysical interaction, but there is limited observational evidence at the appropriate scales to assess their importance. Fronts around western boundary currents like the Gulf Stream are of particular interest as these dynamic physical regions are thought to influence both productivity and composition of primary producers; however, how exactly this plays out is not well known. Using satellite data and 2 years of in situ observations across the Gulf Stream front near Cape Hatteras, North Carolina, we investigate how submesoscale frontal dynamics could affect biological communities and generate hotspots of productivity and export. We assess the seasonality and phenology of the region, generalize the kilometer‐scale structure of the front, and analyze 69 transects to assess two physical processes of potential biogeochemical importance: cold shelf filament subduction and high salinity Sargasso Sea obduction. We link these processes observationally to meanders in the Gulf Stream and discuss how cold filament subduction could be exporting carbon and how obduction of high salinity water from depth is connected with high chlorophyll‐a. Finally, we report on phytoplankton community composition in each of these features and integrate these observations into our understanding of frontal submesoscale dynamics.

 

The biological pump plays a vital role in exporting organic particles into the deep ocean for long-term carbon sequestration. However, much remains unknown about some of its key microbial players. In this study, Labyrinthulomycetes protists (LP) were used to understand the significance of heterotrophic microeukaryotes in the transport of particulate organic matter from the surface to the dark ocean. Unlike the sharp vertical decrease of prokaryotic biomass, the LP biomass only slightly decreased with depth and eventually exceeded prokaryotic biomass in the bathypelagic layer. Sequencing identified high diversity of the LP communities with a dominance of Aplanochytrium at all depths. Notably, ASVs that were observed in the surface layer comprised ~20% of ASVs and ~60% of sequences in each of the deeper (including bathypelagic) layers, suggesting potential vertical export of the LP populations to the deep ocean. Further analyses of the vertical patterns of the 50 most abundant ASVs revealed niche partitioning of LP phylotypes in the pelagic ocean, including those that could decompose organic detritus and/or facilitate the formation of fast-sinking particles. Overall, this study presents several lines of evidence that the LP can be an important component of the biological pump through their multiple ecotypes in the pelagic ocean. 

Disturbances, here defined as events that directly alter microbial community composition, are commonly studied in host‐associated and engineered systems. In spite of global change both altering environmental averages and increasing extreme events, there has been relatively little research into the causes, persistence and population‐level impacts of disturbance in the dynamic coastal ocean. Here, we utilize 3 years of observations from a coastal time series to identify disturbances based on the largest week‐over‐week changes in the microbiome (i.e. identifying disturbance as events that alter the community composition). In general, these microbiome disturbances were not clearly linked to specific environmental factors and responsive taxa largely differed, aside from SAR11, which generally declined. However, several disturbance metagenomes identified increased phage‐associated genes, suggesting that unexplained community shifts might be caused by increased mortality. Furthermore, a category 1 hurricane, the only event that would likely be classifieda priorias an environmental disturbance, was not an outlier in microbiome composition, but did enhance a bloom in seasonally abundant phytoplankton. Thus, as extreme environmental changes intensify, assumptions of what constitutes a disturbance should be re‐examined in the context of ecological history and microbiome responses.

 

Ambient conditions shape microbiome responses to both short- and long-duration environment changes through processes including physiological acclimation, compositional shifts, and evolution. Thus, we predict that microbial communities inhabiting locations with larger diel, episodic, and annual variability in temperature and pH should be less sensitive to shifts in these climate-change factors. To test this hypothesis, we compared responses of surface ocean microbes from more variable (nearshore) and more constant (offshore) sites to short-term factorial warming (+3 °C) and/or acidification (pH −0.3). In all cases, warming alone significantly altered microbial community composition, while acidification had a minor influence. Compared with nearshore microbes, warmed offshore microbiomes exhibited larger changes in community composition, phylotype abundances, respiration rates, and metatranscriptomes, suggesting increased sensitivity of microbes from the less-variable environment. Moreover, while warming increased respiration rates, offshore metatranscriptomes yielded evidence of thermal stress responses in protein synthesis, heat shock proteins, and regulation. Future oceans with warmer waters may enhance overall metabolic and biogeochemical rates, but they will host altered microbial communities, especially in relatively thermally stable regions of the oceans.

 

Abstract A substantial body of research now exists demonstrating sensitivities of marine organisms to ocean acidification (OA) in laboratory settings. However, corresponding in situ observations of marine species or ecosystem changes that can be unequivocally attributed to anthropogenic OA are limited. Challenges remain in detecting and attributing OA effects in nature, in part because multiple environmental changes are co-occurring with OA, all of which have the potential to influence marine ecosystem responses. Furthermore, the change in ocean pH since the industrial revolution is small relative to the natural variability within many systems, making it difficult to detect, and in some cases, has yet to cross physiological thresholds. The small number of studies that clearly document OA impacts in nature cannot be interpreted as a lack of larger-scale attributable impacts at the present time or in the future but highlights the need for innovative research approaches and analyses. We summarize the general findings in four relatively well-studied marine groups (seagrasses, pteropods, oysters, and coral reefs) and integrate overarching themes to highlight the challenges involved in detecting and attributing the effects of OA in natural environments. We then discuss four potential strategies to better evaluate and attribute OA impacts on species and ecosystems. First, we highlight the need for work quantifying the anthropogenic input of CO2 in coastal and open-ocean waters to understand how this increase in CO2 interacts with other physical and chemical factors to drive organismal conditions. Second, understanding OA-induced changes in population-level demography, potentially increased sensitivities in certain life stages, and how these effects scale to ecosystem-level processes (e.g. community metabolism) will improve our ability to attribute impacts to OA among co-varying parameters. Third, there is a great need to understand the potential modulation of OA impacts through the interplay of ecology and evolution (eco–evo dynamics). Lastly, further research efforts designed to detect, quantify, and project the effects of OA on marine organisms and ecosystems utilizing a comparative approach with long-term data sets will also provide critical information for informing the management of marine ecosystems. 

Subsurface chlorophyll maximum layers (SCMLs) are nearly ubiquitous in stratified water columns and exist at horizontal scales ranging from the submesoscale to the extent of oligotrophic gyres. These layers of heightened chlorophyll and/or phytoplankton concentrations are generally thought to be a consequence of a balance between light energy from above and a limiting nutrient flux from below, typically nitrate (NO₃). Here we present multiple lines of evidence demonstrating that iron (Fe) limits or with light colimits phytoplankton communities in SCMLs along a primary productivity gradient from coastal to oligotrophic offshore waters in the southern California Current ecosystem. SCML phytoplankton responded markedly to added Fe or Fe/light in experimental incubations and transcripts of diatom and picoeukaryote Fe stress genes were strikingly abundant in SCML metatranscriptomes. Using a biogeochemical proxy with data from a 40-y time series, we find that diatoms growing in California Current SCMLs are persistently Fe deficient during the spring and summer growing season. We also find that the spatial extent of Fe deficiency within California Current SCMLs has significantly increased over the last 25 y in line with a regional climate index. Finally, we show that diatom Fe deficiency may be common in the subsurface of major upwelling zones worldwide. Our results have important implications for our understanding of the biogeochemical consequences of marine SCML formation and maintenance.

 

Recent studies have focused on linking marine microbial communities with environmental factors, yet, relatively little is known about the drivers of microbial community patterns across the complex gradients from the nearshore to open ocean. Here, we examine microbial dynamics in 15 five‐station transects beginning at the estuarine Piver's Island Coastal Observatory (PICO) time‐series site and continuing 87 km across the continental shelf to the oligotrophic waters of the Sargasso Sea. 16S rRNA gene libraries reveal strong clustering by sampling site with distinct nearshore, continental shelf and offshore oceanic communities. Water temperature and distance from shore (which serves as a proxy for gradients in factors such as productivity, terrestrial input and nutrients) both most influence community composition. However, at the phylotype level, modelling shows the distribution of some taxa is linked to temperature, others to distance from shore and some by both factors, highlighting that taxa with distinct environmental preferences underlie apparent clustering by station. Thus, continental margins contain microbial communities that are distinct from those of either the nearshore or the offshore environments and contain mixtures of phylotypes with nearshore or offshore preferences rather than those unique to the shelf environment.