Search

Phytoplankton are important primary producers. Here the authors investigate phytoplankton physiological changes associated with bloom phases and mixing regimes in the North Atlantic, finding that stratification and deep mixing shape accumulation rates by altering physiology and viral production.

Microbial interactions have profound impacts on biodiversity, biogeochemistry, and ecosystem functioning, and yet, they remain poorly understood in the ocean and with respect to changing environmental conditions. We applied hierarchical clustering of an annual 16S and 18S amplicon dataset in the Skidaway River Estuary, which revealed two similar clusters for prokaryotes (Bacteria and Archaea) and protists: Cluster 1 (March-May and November-February) and Cluster 2 (June-October). We constructed co-occurrence networks from each cluster to explore how microbial networks and relationships vary between environmentally distinct periods in the estuary. Cluster 1 communities were exposed to significantly lower temperature, sunlight, NO3, and SiO4; only NH4 was higher at this time. Several network properties (e.g., edge number, degree, and centrality) were elevated for networks constructed with Cluster 1 vs. 2 samples. There was also evidence that microbial nodes in Cluster 1 were more connected (e.g., higher edge density and lower path length) compared to Cluster 2, though opposite trends were observed when networks considered Prokaryote-Protist edges only. The number of Prokaryote-Prokaryote and Prokaryote-Protist edges increased by >100% in the Cluster 1 network, mainly involving Flavobacteriales, Rhodobacterales, Peridiniales, and Cryptomonadales associated with each other and other microbial groups (e.g., SAR11, Bacillariophyta, and Strombidiida). Several Protist-Protist associations, including Bacillariophyta correlated with Syndiniales (Dino-Groups I and II) and an Unassigned Dinophyceae group, were more prevalent in Cluster 2. Based on the type and sign of associations that increased in Cluster 1, our findings indicate that mutualistic, competitive, or predatory relationships may have been more representative among microbes when conditions were less favorable in the estuary; however, such relationships require further exploration and validation in the field and lab. Coastal networks may also be driven by shifts in the abundance of certain taxonomic or functional groups. Sustained monitoring of microbial communities over environmental gradients, both spatial and temporal, is critical to predict microbial dynamics and biogeochemistry in future marine ecosystems.

Bacteria and phytoplankton form close associations in the ocean that are driven by the exchange of chemical compounds. The bacterial signal 2-heptyl-4-quinolone (HHQ) slows phytoplankton growth; however, the mechanism responsible remains unknown.

Abstract Background Marine bacteria form complex relationships with eukaryotic hosts, from obligate symbioses to pathogenic interactions. These interactions can be tightly regulated by bioactive molecules, creating a complex system of chemical interactions through which these species chemically communicate thereby directly altering the host’s physiology and community composition. Quorum sensing (QS) signals were first described in a marine bacterium four decades ago, and since then, we have come to discover that QS mediates processes within the marine carbon cycle, affects the health of coral reef ecosystems, and shapes microbial diversity and bacteria-eukaryotic host relationships. Yet, only recently have alkylquinolone signals been recognized for their role in cell-to-cell communication and the orchestration of virulence in biomedically relevant pathogens. The alkylquinolone, 2-heptyl-4-quinolone (HHQ), was recently found to arrest cell growth without inducing cell mortality in selected phytoplankton species at nanomolar concentrations, suggesting QS molecules like HHQ can influence algal physiology, playing pivotal roles in structuring larger ecological frameworks. Results To understand how natural communities of phytoplankton and bacteria respond to HHQ, field-based incubation experiments with ecologically relevant concentrations of HHQ were conducted over the course of a stimulated phytoplankton bloom. Bulk flow cytometry measurements indicated that, in general, exposure to HHQ caused nanoplankton and prokaryotic cell abundances to decrease. Amplicon sequencing revealed HHQ exposure altered the composition of particle-associated and free-living microbiota, favoring the relative expansion of both gamma- and alpha-proteobacteria, and a concurrent decrease in Bacteroidetes. Specifically, Pseudoalteromonas spp., known to produce HHQ, increased in relative abundance following HHQ exposure. A search of representative bacterial genomes from genera that increased in relative abundance when exposed to HHQ revealed that they all have the genetic potential to bind HHQ. Conclusions This work demonstrates HHQ has the capacity to influence microbial community organization, suggesting alkylquinolones have functions beyond bacterial communication and are pivotal in driving microbial community structure and phytoplankton growth. Knowledge of how bacterial signals alter marine communities will serve to deepen our understanding of the impact these chemical interactions have on a global scale.

Phytoplankton play a central role in the regulation of global carbon and nutrient cycles, forming the basis of the marine food webs. A group of biogeochemically important phytoplankton, the coccolithophores, produce calcium carbonate scales that have been hypothesized to deter or reduce grazing by microzooplankton. Here, a meta-analysis of mesocosm-based experiments demonstrates that calcification of the cosmopolitan coccolithophore, Emiliania huxleyi, fails to deter microzooplankton grazing. The median grazing to growth ratio for E. huxleyi (0.56 ± 0.40) was not significantly different among non-calcified nano- or picoeukaryotes (0.71 ± 0.31 and 0.55 ± 0.34, respectively). Additionally, the environmental concentration of E. huxleyi did not drive preferential grazing of non-calcified groups. These results strongly suggest that the possession of coccoliths does not provide E. huxleyi effective protection from microzooplankton grazing. Such indiscriminate consumption has implications for the dissolution and fate of CaCO3 in the ocean, and the evolution of coccoliths.

ABSTRACT Syndiniales are a ubiquitous group of protist parasites that infect and kill a wide range of hosts, including harmful bloom-forming dinoflagellates. Despite the importance of parasitism as an agent of plankton mortality, parasite-host dynamics remain poorly understood, especially over time, hindering the inclusion of parasitism in food web and ecosystem models. For a full year in the Skidaway River Estuary (Georgia), we employed weekly 18S rRNA sampling and co-occurrence network analysis to characterize temporal parasite-host infection dynamics of Syndiniales. Over the year, Syndiniales exhibited strong temporal variability, with higher relative abundance from June to October (7 to 28%) than other months in the year (0.01% to 6%). Nonmetric dimensional scaling of Syndiniales composition revealed tight clustering in June to October that coincided with elevated temperatures (23 to 31°C), though in general, abiotic factors poorly explained composition (canonical correspondence analysis [CCA] and partial least-squares [PLS]) and were less important in the network than biotic relationships. Syndiniales amplicon sequence variants (ASVs) were well represented in the co-occurrence network (20% of edges) and had significant positive associations (Spearman r > 0.7), inferred to be putative parasite-host relationships, with known dinoflagellate hosts (e.g., Akashiwo and Gymnodinium) and other protist groups (e.g., ciliates, radiolarians, and diatoms). Positive associations rarely involved a single Syndiniales and dinoflagellate species, implying flexible parasite-host infection dynamics. These findings provide insight into the temporal dynamics of Syndiniales over a full year and reinforce the importance of single-celled parasites in driving plankton population dynamics. Further empirical work is needed to confirm network interactions and to incorporate parasitism within the context of ecosystem models. IMPORTANCE Protist parasites in the marine alveolate group, Syndiniales, have been observed within infected plankton host cells for decades, and recently, global-scale efforts (Tara Ocean exploration) have confirmed their importance within microbial communities. Yet, protist parasites remain enigmatic, particularly with respect to their temporal dynamics and parasite-host interactions. We employed weekly 18S amplicon surveys over a full year in a coastal estuary, revealing strong temporal shifts in Syndiniales parasites, with highest relative abundance during warmer summer to fall months. Though influenced by temperature, Syndiniales population dynamics were also driven by a high frequency of biological interactions with other protist groups, as determined through co-occurrence network analysis. Parasitic interactions implied by the network highlighted a range of confirmed (dinoflagellates) and putative (diatoms) interactions and suggests parasites may be less selective in their preferred hosts. Understanding parasite-host dynamics over space and time will improve our ability to include parasitism as a loss term in microbial food web models.

In marine waters, ubiquitous reactive oxygen species (ROS) drive biogeochemical cycling of metals and carbon. Marine phytoplankton produce the ROS superoxide (O2−) extracellularly and can be a dominant source of O2− in natural aquatic systems. However, the cellular regulation, biological functioning, and broader ecological impacts of extracellular O2− production by marine phytoplankton remain mysterious. Here, we explored the regulation and potential roles of extracellular O2− production by a noncalcifying strain of the cosmopolitan coccolithophorid Emiliania huxleyi, a key species of marine phytoplankton that has not been examined for extracellular O2− production previously. Cell-normalized extracellular O2− production was the highest under presumably low-stress conditions during active proliferation and inversely related to cell density during exponential growth phase. Removal of extracellular O2− through addition of the O2− scavenger superoxide dismutase (SOD), however, increased growth rates, growth yields, cell biovolume, and photosynthetic efficiency (Fv/Fm) indicating an overall physiological improvement. Thus, the presence of extracellular O2− does not directly stimulate E. huxleyi proliferation, as previously suggested for other phytoplankton, bacteria, fungi, and protists. Extracellular O2− production decreased in the dark, suggesting a connection with photosynthetic processes. Taken together, the tight regulation of this stress independent production of extracellular O2− by E. huxleyi suggests that it could be involved in fundamental photophysiological processes.

Rates of microzooplankton grazing and phytoplankton growth are seldom measured with respect to time, yet such estimates may better reflect temporal variability in coastal phytoplankton communities and offer insight into mechanisms that control populations. To assess seasonal patterns in rates, we performed 41, weekly dilution experiments over a full year in the Skidaway River Estuary (GA), measuring rates of phytoplankton growth, microzooplankton grazing, and viral lysis based on total chlorophyll and group-specific abundances (Synechococcus spp., picoeukaryotes, and nanoeukaryotes). Seasonal variability in microzooplankton grazing (0–2.11 day-1) and phytoplankton growth rates (-0.3–2.43 day-1) was observed, with highest values typically recorded in summer and lowest in winter. Grazing pressure was strongest in winter-spring, as phytoplankton accumulation rates were often negative (-0.16–0.28 day-1). Rates varied similarly over seasons for chlorophyll, pico-, and nanoeukaryotes, while rates on Synechococcus spp. were rarely significant in dilutions and did not follow seasonal trends. Few experiments (7%) yielded significant rates of viral lysis. While temperature was an important predictor of phytoplankton rates via PLS analysis, temperature exhibited stronger linearity with growth rates (R2 = 0.46–0.56) compared to grazing rates (R2 = 0.11–0.27), which were more likely driven by observed seasonal shifts in plankton community composition (e.g., fall diatom blooms). Establishing temporal rate measurements is critical to identify factors that drive phytoplankton growth and mortality and accurately predict shifts in phytoplankton population dynamics and food web processes within marine systems.

The North Atlantic Aerosols and Marine Ecosystems Study (NAAMES) is an interdisciplinary investigation to improve understanding of Earth's ocean ecosystem-aerosol-cloud system. Specific overarching science objectives for NAAMES are to (1) characterize plankton ecosystem properties during primary phases of the annual cycle and their dependence on environmental forcings, (2) determine how these phases interact to recreate each year the conditions for an annual plankton bloom, and (3) resolve how remote marine aerosols and boundary layer clouds are influenced by plankton ecosystems. Four NAAMES field campaigns were conducted in the western subarctic Atlantic between November 2015 and April 2018, with each campaign targeting specific seasonal events in the annual plankton cycle. A broad diversity of measurements were collected during each campaign, including ship, aircraft, autonomous float and drifter, and satellite observations. Here, we present an overview of NAAMES science motives, experimental design, and measurements. We then briefly describe conditions and accomplishments during each of the four field campaigns and provide information on how to access NAAMES data. The intent of this manuscript is to familiarize the broad scientific community with NAAMES and to provide a common reference overview of the project for upcoming publications.

Interactions between phytoplankton and bacteria play a central role in mediating biogeochemical cycling and food web structure in the ocean. However, deciphering the chemical drivers of these interspecies interactions remains challenging. Here we report the isolation of 2-heptyl-4-quinolone (HHQ), released by Pseudoalteromonas piscicida, a marine gamma-proteobacteria previously reported to induce phytoplankton mortality through a hitherto unknown algicidal mechanism. HHQ functions as both an antibiotic and a bacterial signaling molecule in cell-cell communication in clinical infection models. Co-culture of the bloom-forming coccolithophore, Emiliania huxleyi with both live P. piscicida and cell-free filtrates caused a significant decrease in algal growth. Investigations of the P. piscicida exometabolome revealed HHQ, at nanomolar concentrations, induced mortality in three strains of E. huxleyi. Mortality of E. huxleyi in response to HHQ occurred slowly, implying static growth rather than a singular loss event (e.g. rapid cell lysis). In contrast, the marine chlorophyte, Dunaliella tertiolecta and diatom, Phaeodactylum tricornutum were unaffected by HHQ exposures. These results suggest that HHQ mediates the type of interkingdom interactions that cause shifts in phytoplankton population dynamics. These chemically mediated interactions, and other like it, ultimately influence large-scale oceanographic processes.

In the plankton, heterotrophic microbes encounter and ingest phytoplankton prey, which effectively removes >50% of daily phytoplankton production in the ocean and influences global primary production and biochemical cycling rates. Factors such as size, shape, nutritional value, and presence of chemical deterrents are known to affect predation pressure. Effects of movement behaviors of either predator or prey on predation pressure, and particularly fleeing behaviors in phytoplankton are thus far unknown. Here, we quantified individual 3D movements, population distributions, and survival rates of the toxic phytoplankton species, Heterosigma akashiwo in response to a ciliate predator and predator-derived cues. We observed predator-induced defense behaviors previously unknown for phytoplankton. Modulation of individual phytoplankton movements during and after predator exposure resulted in an effective separation of predator and prey species. The strongest avoidance behaviors were observed when H. akashiwo co-occurred with an actively grazing predator. Predator-induced changes in phytoplankton movements resulted in a reduction in encounter rate and a 3-fold increase in net algal population growth rate. A spatially explicit population model predicted rapid phytoplankton bloom formation only when fleeing behaviors were incorporated. These model predictions reflected field observations of rapid H. akashiwo harmful algal bloom (HAB) formation in the coastal ocean. Our results document a novel behavior in phytoplankton that can significantly reduce predation pressure and suggests a new mechanism for HAB formation. Phytoplankton behaviors that minimize predatory losses, maximize resource acquisition, and alter community composition and distribution patterns could have major implications for our understanding and predictive capacity of marine primary production and biochemical cycling rates.