Marine Microbial Food Web Research Articles

Temporal temperature shifts govern the population succession of picoeukaryotes and picocyanobacteria in a coastal ecosystem

Picophytoplankton are vital components of the marine microbial food web. Being the smallest in the phytoplankton group, their short life cycles make them excellent bioindicators of environmental conditions. Given this, an investigation was conducted at the Kandla Port ecosystem (Latitude 23º 01' N; Longitude 70º 13' E) in the state of Gujarat, India to assess the response of picophytoplankton community structure to temporal and spatial environmental conditions. The sampling was conducted in July 2015, October-November 2015, and February 2016 at twenty-six stations. The results revealed a wide annual temperature range due to the study site's proximity to the Tropic of Cancer. The salinity ranged up to 40 while the turbulence caused by the macrotides resulted in highly turbid waters, especially during July due to precipitation. The picophytoplankton community was represented by picocyanobacteria (three sub-groups of Synechococcus) and picoeukaryotes (three sub-groups including Cryptophytes). The picocyanobacteria were abundant during the less turbid, warmer October-November period and lower during the cooler February period. The dominant Synechoccocus groups are associated positively with NH4+ and negatively with PO43-. The Cryptophytes were present during the warm and cool periods indicating tolerance to a wide range of temperature, salinity, and light. Their positive correlation with PO43- and NH4+ concentrations during February and October-November, respectively suggests a causal relationship. The picoeukaryotic group dominated the picophytoplankton community during the cooler period (February). The relative importance of the two picophytoplankton groups changed throughout the year exhibiting temporal niche segregation and hence establishing their role as bioindicators of temperature.

Analysis of the Influence of Seasonal Water Column Dynamics on the Relationship between Marine Viruses and Microbial Food Web Components Using an Artificial Neural Network

Artificial neural network analysis (ANN) is used to study the seasonal distribution of viruses and microbial food web (MFW) components in the open Adriatic Sea. The effect of viruses within the MFW is often overlooked, although viruses play an important role in microbial community dynamics. The results showed that the strongest influence is found in the nonlinear relationship between viruses and temperature. In addition, the algorithm showed that the number of viral populations in the P-limited open sea varies by season and according to the abundance of their main hosts, HB. A strong positive relationship between viruses and HB was found in more than 50% of the observed data. Moreover, this algorithm confirmed the association of the virus with the autotrophic part of the picoplankton and with heterotrophic nanoflagellates. The dynamics of the four resulting clusters, characterized by biological and environmental parameters, is described as a cyclic pattern in the water layer above the thermocline. Neural gas network analysis has been shown to be an excellent tool for describing changes in MFW components in the open Adriatic.

Particulate and dissolved metabolite distributions along a latitudinal transect of the western Atlantic Ocean

AbstractMetabolites, or the small organic molecules that are synthesized by cells during metabolism, comprise a complex and dynamic pool of carbon in the ocean. They are an essential currency in interactions at the population and community levels of biological organization. Characterizing metabolite distributions inside microbial cells and dissolved in seawater is essential to understanding the controls on their production and fate, as well as their roles in shaping marine microbial food webs. Here, we apply a targeted metabolomics method to quantify particulate and dissolved distributions of a suite of biologically relevant metabolites including vitamins, amino acids, nucleic acids, osmolytes, and intermediates in biosynthetic pathways along a latitudinal transect in the western Atlantic Ocean. We find that, in the upper 200 m of the water column, most particulate or intracellular metabolites positively covary with the most abundant microbial taxa. In contrast, dissolved metabolites exhibited greater variability with differences in distribution between ocean regions. Although fewer particulate metabolites were detected below 200 m, the particulate metabolites identified in the deep ocean may be linked to adaptive physiological strategies of deep‐sea microbes. Based on the identified metabolite distributions, we propose relationships between certain metabolites and microbial populations, and find that dissolved metabolite distributions are not directly related to their particulate abundances.

Microplankton life histories revealed by holographic microscopy and deep learning.

The marine microbial food web plays a central role in the global carbon cycle. However, our mechanistic understanding of the ocean is biased toward its larger constituents, while rates and biomass fluxes in the microbial food web are mainly inferred from indirect measurements and ensemble averages. Yet, resolution at the level of the individual microplankton is required to advance our understanding of the microbial food web. Here, we demonstrate that, by combining holographic microscopy with deep learning, we can follow microplanktons throughout their lifespan, continuously measuring their three-dimensional position and dry mass. The deep-learning algorithms circumvent the computationally intensive processing of holographic data and allow rapid measurements over extended time periods. This permits us to reliably estimate growth rates, both in terms of dry mass increase and cell divisions, as well as to measure trophic interactions between species such as predation events. The individual resolution provides information about selectivity, individual feeding rates, and handling times for individual microplanktons. The method is particularly useful to detail the rates and routes of organic matter transfer in micro-zooplankton, the most important and least known group of primary consumers in the oceans. Studying individual interactions in idealized small systems provides insights that help us understand microbial food webs and ultimately larger-scale processes. We exemplify this by detailed descriptions of micro-zooplankton feeding events, cell divisions, and long-term monitoring of single cells from division to division.

Trade-offs of lipid remodeling in a marine predator–prey interaction in response to phosphorus limitation

Phosphorus (P) is a key nutrient limiting bacterial growth and primary production in the oceans. Unsurprisingly, marine microbes have evolved sophisticated strategies to adapt to P limitation, one of which involves the remodeling of membrane lipids by replacing phospholipids with non-P-containing surrogate lipids. This strategy is adopted by both cosmopolitan marine phytoplankton and heterotrophic bacteria and serves to reduce the cellular P quota. However, little, if anything, is known of the biological consequences of lipid remodeling. Here, using the marine bacterium Phaeobacter sp. MED193 and the ciliate Uronema marinum as a model, we sought to assess the effect of remodeling on bacteria-protist interactions. We discovered an important trade-off between either escape from ingestion or resistance to digestion. Thus, Phaeobacter grown under P-replete conditions was readily ingested by Uronema, but not easily digested, supporting only limited predator growth. In contrast, following membrane lipid remodeling in response to P depletion, Phaeobacter was less likely to be captured by Uronema, thanks to the reduced expression of mannosylated glycoconjugates. However, once ingested, membrane-remodeled cells were unable to prevent phagosome acidification, became more susceptible to digestion, and, as such, allowed rapid growth of the ciliate predator. This trade-off between adapting to a P-limited environment and susceptibility to protist grazing suggests the more efficient removal of low-P prey that potentially has important implications for the functioning of the marine microbial food web in terms of trophic energy transfer and nutrient export efficiency.

Phytoplankton Sources and Sinks of Dimethylsulphoniopropionate (DMSP) in Temperate Coastal Waters of Australia.

The ecologically important organic sulfur compound, dimethylsulfoniopropionate (DMSP), is ubiquitous in marine environments. Produced by some species of phytoplankton and bacteria, it plays a key role in cellular responses to environmental change. Recently, uptake of DMSP by non-DMSP-producing phytoplankton species has been demonstrated, highlighting knowledge gaps concerning DMSP distribution through the marine microbial food web. In this study, we traced the uptake and distribution of DMSP through a natural marine microbial community collected from off the eastern coastline Australia. We found a diverse phytoplankton community representing six major taxonomic groups and conducted DMSP-enrichment experiments both on the whole community, and the community separated into large (≥8.0 µm), medium (3.0–8.0 µm), and small (0.2–3.0 µm) size fractions. Our results revealed active uptake of DMSP in all three size fractions of the community, with the largest fraction (>8 µm) forming the major DMSP sink, where enrichment resulted in an increase of DMSPp by 144%. We observed evidence for DMSP catabolism in all size fractions with DMSP enrichment, highlighting loss from the system via MeSH or DMS production. Based on taxonomic diversity, we postulate the sources of DMSP were the dinoflagellates, Phaeocystis sp., and Trichodesmium sp., which were present in a relatively high abundance, and the sinks for DMSP were the diatoms and picoeucaryotes in this temperate community. These findings corroborate the role of hitherto disregarded phytoplankton taxa as potentially important players in the cycling of DMSP in coastal waters of Australia and emphasize the need to better understand the fate of accumulated DMSP and its significance in cellular metabolism of non-DMSP producers.

Seasonal Dynamics in Carbon Cycling of Marine Bacterioplankton Are Lifestyle Dependent.

Although free-living (FL) and particle-attached (PA) bacteria are recognized as ecologically distinct compartments of marine microbial food-webs, few, if any, studies have determined their dynamics in abundance, function (production, respiration and substrate utilization) and taxonomy over a yearly cycle. In the Baltic Sea, abundance and production of PA bacteria (defined as the size-fraction >3.0 μm) peaked over 3 months in summer (6 months for FL bacteria), largely coinciding with blooms of Chitinophagales (Bacteroidetes). Pronounced changes in the growth efficiency (range 0.05–0.27) of FL bacteria (defined as the size-fraction <3.0 μm) indicated the magnitude of seasonal variability of ecological settings bacteria experience. Accordingly, 16S rRNA gene analyses of bacterial community composition uncovered distinct correlations between taxa, environmental variables and metabolisms, including Firmicutes associated with elevated hydrolytic enzyme activity in winter and Verrucomicrobia with utilization of algal-derived substrates during summer. Further, our results suggested a substrate-controlled succession in the PA fraction, from Bacteroidetes using polymers to Actinobacteria and Betaproteobacteria using monomers across the spring to autumn phytoplankton bloom transition. Collectively, our findings emphasize pronounced seasonal changes in both the composition of the bacterial community in the PA and FL size-fractions and their contribution to organic matter utilization and carbon cycling. This is important for interpreting microbial ecosystem function-responses to natural and human-induced environmental changes.

The Microbiological Drivers of Temporally Dynamic Dimethylsulfoniopropionate Cycling Processes in Australian Coastal Shelf Waters.

The organic sulfur compounds dimethylsulfoniopropionate (DMSP) and dimethyl sulfoxide (DMSO) play major roles in the marine microbial food web and have substantial climatic importance as sources and sinks of dimethyl sulfide (DMS). Seasonal shifts in the abundance and diversity of the phytoplankton and bacteria that cycle DMSP are likely to impact marine DMS (O) (P) concentrations, but the dynamic nature of these microbial interactions is still poorly resolved. Here, we examined the relationships between microbial community dynamics with DMS (O) (P) concentrations during a 2-year oceanographic time series conducted on the east Australian coast. Heterogenous temporal patterns were apparent in chlorophyll a (chl a) and DMSP concentrations, but the relationship between these parameters varied over time, suggesting the phytoplankton and bacterial community composition were affecting the net DMSP concentrations through differential DMSP production and degradation. Significant increases in DMSP were regularly measured in spring blooms dominated by predicted high DMSP-producing lineages of phytoplankton (Heterocapsa, Prorocentrum, Alexandrium, and Micromonas), while spring blooms that were dominated by predicted low DMSP-producing phytoplankton (Thalassiosira) demonstrated negligible increases in DMSP concentrations. During elevated DMSP concentrations, a significant increase in the relative abundance of the key copiotrophic bacterial lineage Rhodobacterales was accompanied by a three-fold increase in the gene, encoding the first step of DMSP demethylation (dmdA). Significant temporal shifts in DMS concentrations were measured and were significantly correlated with both fractions (0.2–2 μm and >2 μm) of microbial DMSP lyase activity. Seasonal increases of the bacterial DMSP biosynthesis gene (dsyB) and the bacterial DMS oxidation gene (tmm) occurred during the spring-summer and coincided with peaks in DMSP and DMSO concentration, respectively. These findings, along with significant positive relationships between dsyB gene abundance and DMSP, and tmm gene abundance with DMSO, reinforce the significant role planktonic bacteria play in producing DMSP and DMSO in ocean surface waters. Our results highlight the highly dynamic nature and myriad of microbial interactions that govern sulfur cycling in coastal shelf waters and further underpin the importance of microbial ecology in mediating important marine biogeochemical processes.

Niche Partitioning of Labyrinthulomycete Protists Across Sharp Coastal Gradients and Their Putative Relationships With Bacteria and Fungi.

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.

Mechanisms Generating Dichotomies in the Life Strategies of Heterotrophic Marine Prokaryotes

Understanding the mechanisms that generate and maintain diversity in marine prokaryotic communities is one of the main challenges for contemporary marine microbiology. We here review how observational, experimental, and theoretical evidence converge on the conclusion that the marine pelagic community of heterotrophic prokaryotes consists of organisms with two main types of life strategies. We illustrate this dichotomy by SAR11 and Vibrio spp. as typical representatives of the two strategies. A theory for life strategy dichotomy exists in classical r/K-selection. We here discuss an additional dichotomy introduced by what we term S/L-selection (for Small and Large, respectively). While r/K-selection focuses on the role of environmental disturbances, steady-state models suggest that high abundance at species level should be closely related to a low trade-off between competition and defense. We summarize literature indicating that the high availability of organic C is an essential environmental factor favoring Vibrio spp. and suggest that the essence of the generalized L-strategy is to reduce the competition-predator defense trade-off by using non-limiting organic C to increase size. The “streamlining” theory that has been suggested for the S-strategist SAR11 proposes the opposite: that low trade-off is achieved by a reduction in size. We show how this apparent contradiction disappears when the basic assumptions of diffusion-limited uptake are considered. We propose a classification scheme that combines S/L and r/K-selection using the two dimensions of organic C availability and environmental disturbance. As organic C in terrestrial runoff and size of the oligotrophic oceanic gyres are both changing, habitat size for both S- and L-strategists are affected by global change. A theory capturing the main aspects of prokaryote life strategies is therefore crucial for predicting responses of the marine microbial food web to climate change and other anthropogenic influences.

Food web structure and intraguild predation affect ecosystem functioning in an established plankton model

AbstractUnderstanding how marine microbial food webs and their ecosystem functions are changing is crucial for projections of the future ocean. Often, simplified food web models are employed and their solutions are only evaluated against available observations of plankton biomass. With such an approach, it remains unclear how different underlying trophic interactions affect interpretations of plankton dynamics and functioning. Here, we quantitatively compare four hypothetical food webs to data from an existing mesocosm experiment using a refined version of the Minimum Microbial Food Web model. Food web representations range from separated food chains to complex food webs featuring additional trophic links including intraguild predation (IGP). Optimization against observations and taking into account model complexity ensures a fair comparison of the different food webs. Although the different optimized model food webs capture the observations similarly well, projected ecosystem functions differ depending on the underlying food web structure and the presence or absence of IGP. Mesh‐like food webs dominated by the microbial loop yield higher recycling and net primary production (NPP) than models dominated by the classical diatom‐copepod food chain. A high degree of microzooplankton IGP increases NPP and organic matter recycling, but decreases trophic transfer efficiency (TTE) to copepods. Copepod production, the trophic role of copepods, and TTE are more sensitive to initial biomass changes in chain‐like than in complex food webs. Measurements resolving trophic interactions, in particular those quantifying IGP, remain essential to reduce model uncertainty and allow sound conclusions for ecosystem functioning in plankton ecosystems.

High Dynamics of Ciliate Community Revealed via Short-Term, High-Frequency Sampling in a Subtropical Estuarine Ecosystem.

Ciliates are pivotal components of the marine microbial food web, exerting profound impacts on oceanic biogeochemical cycling. However, the temporal dynamics of ciliate assemblages on a short time scale in the highly fluctuating estuarine ecosystem remain largely unexplored. We studied changes in the ciliate community during a short time frame in the high salinity waters (>26) of a subtropical estuary. Ciliate abundance, biomass, size and oral diameter structure, and community composition fluctuated considerably and irregularly over a few days or even a few hours. Spearman correlations and the generalized linear model revealed that heterotrophic prokaryotes (HPs) and viral abundances drove the dynamics of ciliate abundance and biomass. The structural equation model further identified a major path from the high-fluorescence content virus (HFV) to HPs and then ciliates. Given the substantial correlation between salinity and HPs/HFV, we proposed that the response of HPs and HFV to salinity drives the dynamics of ciliate biomass. Additionally, the Mantel test showed that phytoplankton pigments such as Lutein and Neoxanthin, phosphate, and pigmented picoeukaryotes were key covariates of the ciliate community composition. This study demonstrated the highly changing patterns of ciliate assemblages and identified potential processes regulating ciliate biomass and community composition on short timescales in a subtropical, hydrographically complex estuary.

Evidence for mixotrophy in pico-chlorophytes from a new Picochlorum (Trebouxiophyceae) strain.

Mixotrophs are increasingly recognized for their wide distribution in aquatic ecosystems and significant contributions to biogeochemical cycling. Many taxa within the phyla Chrysophyta, Cryptophyta, and Haptophyta are capable of phago-mixotrophy, however, phagotrophy in the Chlorophyta remains controversial due to insufficient research and solid evidence. In this study, we identified a new strain, Picochlorum sp. GLMF1 (Trebouxiophyceae), using 18S rRNA gene analysis and morphological observations. It displayed multi-cell division through autosporulation (two- or four-cell daughters) and has two unequal flagella that have never been reported in the genus Picochlorum. By using multiple methods, including 3D bioimaging analysis, acidic food vacuole-like compartment staining, and prey reduction calculation, we discovered and confirmed bacterivory in Picochlorum, which provided strong evidence for phago-mixotrophy in this green alga. In addition, we found that Picochlorum sp. GLMF1 cannot grow under complete darkness or prey-depleted conditions, suggesting that both light and bacteria are indispensable for this strain, and its mixotrophic nutrition mode is obligate. Like other phago-phototrophs, Picochlorum sp. GLMF1 is capable of regulating their growth and ingestion rates according to light intensity and inorganic nutrient concentration. The confirmation of mixotrophy in this Picochlorum strain advances our understanding of the trophic roles of green algae, as well as the photosynthetic picoeukaryotes, in marine microbial food webs.

How Microbial Food Web Interactions Shape the Arctic Ocean Bacterial Community Revealed by Size Fractionation Experiments.

In the Arctic, seasonal changes are substantial, and as a result, the marine bacterial community composition and functions differ greatly between the dark winter and light-intensive summer. While light availability is, overall, the external driver of the seasonal changes, several internal biological interactions structure the bacterial community during shorter timescales. These include specific phytoplankton–bacteria associations, viral infections and other top-down controls. Here, we uncover these microbial interactions and their effects on the bacterial community composition during a full annual cycle by manipulating the microbial food web using size fractionation. The most profound community changes were detected during the spring, with ‘mutualistic phytoplankton’—Gammaproteobacteria interactions dominating in the pre-bloom phase and ‘substrate-dependent phytoplankton’—Flavobacteria interactions during blooming conditions. Bacterivores had an overall limited effect on the bacterial community composition most of the year. However, in the late summer, grazing was the main factor shaping the community composition and transferring carbon to higher trophic levels. Identifying these small-scale interactions improves our understanding of the Arctic marine microbial food web and its dynamics.

Diversity and distribution of heterotrophic flagellates in seawater of the Powell Basin, Antarctic Peninsula

Heterotrophic flagellates are essential components of the marine microbial food web. However, how the changes in flagellate populations reflect environmental changes in marine ecosystems is still unclear, especially in polar regions. In this study, we used pyrosequencing to examine the community structure of heterotrophic flagellates (HFs) in the Powell Basin’s surface waters of the northern Antarctic Peninsula. OTUs (operational taxonomic units) of different taxa and the correlations between community structure and environmental factors were analysed. Eight taxa of HFs were selected for the principal analysis: Telonemia, Picozoa, Rhizaria, Amoebozoa, Apusomonas, Centrohelida, Choanomonada and marine stramenopiles (MASTs). The HFs were defined as heterotrophic picoflagellates (HPFs; &lt;3 μm) and heterotrophic nanoflagellates (HNFs; &gt;3 μm, &lt;20 μm), which had similar dominant phyla (MASTs and Telonemia). However, their taxonomic composition differed. Environmental factors exerted similar effects on the community structure of both HPFs and HNPs. Compared with the correlation between HPF and environmental factors, the correlation between HNF and environmental factors was stronger. Salinity, bacterial biomass and the biological interactions amongst dominant taxa were the main variables to influence the diversity and community structure of HFs.

Removal of large viruses and their dispersal through fecal pellets of the appendicularianOikopleura dioicaduringEmiliania huxleyibloom conditions

AbstractDespite their importance in shaping the structure and function of marine microbial food webs, little is known about factors regulating marine virus abundance. Previous work demonstrated clearance of laboratory‐culturedEmiliania huxleyivirus by the appendicularianOikopleura dioica; however, the applicability of this interaction to natural virus assemblages was not investigated. Here, we conducted controlled laboratory experiments usingO. dioicaand mesocosm water containing natural virus assemblages with high densities of virus, and measured removal of virus byO. dioicausing both flow cytometry and molecular methods. Bayesian models based on flow cytometry quantification of virus particles demonstrated efficient removal of viruses (mean 90.3 mL ind−1d−1), with a clearance efficiency of 42.6% relative to food algae. Molecular detection of virus removal by quantification of viralmcpgene copies revealed a mean clearance rate of 68.1 mL ind−1d−1. Fecal pellets from these experiments demonstrated that viruses in fecal pellets retain infectivity despite passage through theO. dioicagut. Shotgun metavirome analysis demonstratedO. dioicaremoval of large virus groups, notably the Phycodnaviridae. The results demonstrate the removal ofE. huxleyivirus from natural virus assemblages byO. dioicaand the maintenance of viral infectivity when incorporated into fecal pellets, prompting further investigation on the fate of fecal‐packaged viruses and their impact on host dynamics. Furthermore, our results indicate the generality of this interaction for other large algal viruses, raising questions about the implications of this mechanism of marine virus redistribution on the broader marine virus community.

Heterotrophic Dinoflagellate Growth and Grazing Rates Reduced by Microplastic Ingestion

Microplastics are ubiquitous contaminants in marine ecosystems worldwide, threatening fisheries production, food safety, and human health. Ingestion of microplastics by fish and large zooplankton has been documented, but there are few studies focusing on single-celled marine predators, including heterotrophic dinoflagellates. In laboratory experiments, the heterotrophic dinoflagellate species Oxyrrhis marina and Gyrodinium sp. readily ingested both algal prey and polystyrene microplastic spheres (2.5–4.5 μm), while Protoperidinium sp. did not ingest microplastics. Compared to algae-only fed dinoflagellates, those that ingested microplastics had growth rates reduced by 25–35% over the course of 5 days. Reduced growth resulted in a 30–50% reduction of secondary production as measured as predator biomass. Ingestion rates of algal prey were also reduced in the microplastic treatments. When given a mixture of microplastics and algal prey, O. marina displayed a higher selectivity for algal prey than Gyrodinium sp. Observations in the coastal ocean showed that phylogenetically diverse taxa ingested microplastic beads, and thus heterotrophic dinoflagellates could contribute to trophic transfer of microplastics to higher trophic levels. The results of this study may suggest that continued increase in microplastic pollution in the ocean could lead to reduced secondary production of heterotrophic protists due to microplastic ingestion, altering the flow of energy and matter in marine microbial food webs.

Spring Distribution of Ciliate Plankton in the Southeastern Yellow Sea in 2019

As planktonic ciliates have been recognized as important players in marine microbial food webs, relevant studies have been conducted in the western coastal waters of the Yellow Sea. However, little is known about ciliate distributions from the eastern coast of the Yellow Sea near the Korean Peninsula. A spring cruise in April 2019 was carried out to investigate vertical and horizontal distributions of ciliate plankton at 18 stations that form three zonal sections in the eastern area. Biological (picoplankton, nanophytoplankton, and mesozooplankton) and hydrological (water temperature and salinity) environments were also analyzed to understand relationships between the ciliate distributions and the environments. High abundance (ca. 2400 cells L−1) of a large ciliate species, Laboea strobila, was observed at the surface water of Stn. 37–5. Abundance peak of large (> 50 μm) ciliates coincided with the peak of mesozooplankton abundance. Spatial distribution of the large ciliates was associated with nanophytoplankton distribution while a smaller (20–50 μm) ciliate group was associated with picoplankton distribution. Therefore, the spring distribution of ciliate plankton in the southeastern coast of the Yellow Sea indicates that food size for the ciliates is one of the important factors controlling ciliate compositions as well as their abundances. Further investigations need to be carried out to understand seasonal differences of ciliate distributions in the eastern Yellow Sea.

Annual Partitioning Patterns of Labyrinthulomycetes Protists Reveal Their Multifaceted Role in Marine Microbial Food Webs.

Heterotrophic microbes play a key role in remineralizing organic material in the coastal ocean. While there is a significant body of literature examining heterotrophic bacterioplankton and phytoplankton communities, much less is known about the diversity, dynamics, and ecology of eukaryotic heterotrophs. Here, we focus on the Labyrinthulomycetes, a fungus-like protistan group whose biomass can exceed that of the bacterioplankton in coastal waters. We examined their diversity and community structure in a weekly temperate coastal ocean time series. Their seasonal community patterns were related to temperature, insolation, dissolved inorganic carbon, fungal abundance, ammonia, chlorophyll a, pH, and other environmental variables. Similar to the bacterioplankton, annual community patterns of the Labyrinthulomycetes were dominated by a few persistent taxa with summer or winter preferences. However, like the patterns of fungi at this site, the majority of the Labyrinthulomycetes phylotypes occurred mostly as short, reoccurring, season-specific blooms. Furthermore, some specific phylotypes of Labyrinthulomycetes displayed time-lagged correlations or cooccurrences with bacterial, algal, or fungal phylotypes, suggesting their potentially multifaceted involvement in the marine food webs. Overall, this study reports niche partitioning between closely related Labyrinthulomycetes and identifies distinct ecotypes and temporal patterns compared to bacterioplankton and fungi.IMPORTANCE Increasing evidence has shown that heterotrophic microeukaryotes are an important component in global marine ecosystems, while their diversity and ecological functions remain largely unknown. Without appropriately incorporating these organisms into the food web models, our current understanding of marine microbial community ecology is incomplete, which may further hamper broader studies of biogeochemistry and climate change. This study focuses on a major group of unicellular fungus-like protists (Labyrinthulomycetes) and reveals their distinct annual community patterns relative to fungi and bacteria. Results of our observations provide new information on the community structure and ecology of this protistan group and shed light on the intricate ecological roles of unicellular heterotrophic eukaryotes in the coastal oceans.

Molecular approach for analysis of in situ feeding by the dinoflagellate Noctiluca scintillans

The red tide forming heterotrophic dinoflagellate Noctiluca scintillans is common in temperate to tropical waters around the world. Understanding the in situ prey of N. scintillans is essential for elucidating its role in marine microbial food webs. In this study, we applied two polymerase chain reaction (PCR)-based cloning techniques, a predator-specific restriction enzyme, and a blocking primer. The PCR of nuclear 18S rDNA was performed on single N. scintillans cells that were collected from Ishinomaki Bay, Japan, in May 2018. The maximum detection rates of non-Noctiluca sequences were 56% using the restriction enzyme method and 87% with the blocking primer method, representing a broad taxonomic range of organisms, including diatom, dinoflagellate, bolidophyte, haptophyte, euglenophyte, green algae, golden algae, ciliate, heliozoa, copepod, brown seaweed, sponge, bivalve, and polychaete. The diverse DNA was probably ingested by N. scintillans directly or indirectly through secondary predation or ingestion of marine snow or detritus containing many organisms. The application of molecular approaches to various species may reveal undiscovered interactions within the phytoplankton community, including prey-predator, or symbiotic relationships.