Seasonal environmental transitions and metabolic plasticity in a sea-ice alga from an individual cell perspective.

Sea-ice microalgae are a key source of energy and nutrient supply to polar marine food webs, particularly during spring, prior to open-water phytoplankton blooms. The nutritional quality of microalgae as a food source depends on their biomolecular (lipid:protein:carbohydrate) composition. In this study, we used synchrotron-based Fourier transform infra-red microspectroscopy (s-FTIR) to measure the biomolecular content of a dominant sea-ice taxa, Nitzschia frigida, from natural land-fast ice communities throughout the Arctic spring season. Repeated sampling over six weeks from an inner (relatively stable) and an outer (relatively dynamic) fjord site revealed high intra-specific variability in biomolecular content, elucidating the plasticity of N. frigida to adjust to the dynamic sea ice and water conditions. Environmental triggers indicating the end of productivity in the ice and onset of ice melt, including nitrogen limitation and increased water temperature, drove an increase in lipid and fatty acids stores, and a decline in protein and carbohydrate content. In the context of climate change and the predicted Atlantification of the Arctic, dynamic mixing and abrupt warmer water advection could truncate these important end-of-season environmental shifts, causing the algae to be released from the ice prior to adequate lipid storage, influencing carbon transfer through the polar marine system.

Beyond a single temperature threshold: Applying a cumulative thermal stress framework to plant heat tolerance.

Most plant thermal tolerance studies focus on single critical thresholds, which limit the capacity to generalise across studies and predict heat stress under natural conditions. In animals and microbes, thermal tolerance landscapes describe the more realistic, cumulative effects of temperature. We tested this in plants by measuring the decline in leaf photosynthetic efficiency (FV/FM) following a combination of temperatures and exposure times and then modelled these physiological indices alongside recorded environmental temperatures. We demonstrate that a general relationship between stressful temperatures and exposure durations can be effectively employed to quantify and compare heat tolerance within and across plant species and over time. Importantly, we show how FV/FM curves translate to plants under natural conditions, suggesting that environmental temperatures often impair photosynthetic function. Our findings provide more robust descriptors of heat tolerance in plants and suggest that heat tolerance in disparate groups of organisms can be studied with a single predictive framework.

Biomolecular profiles of Arctic sea-ice diatoms highlight the role of under-ice light in cellular energy allocation.

Arctic sea-ice diatoms fuel polar marine food webs as they emerge from winter darkness into spring. Through their photosynthetic activity they manufacture the nutrients and energy that underpin secondary production. Sea-ice diatom abundance and biomolecular composition vary in space and time. With climate change causing short-term extremes and long-term shifts in environmental conditions, understanding how and in what way diatoms adjust biomolecular stores with environmental perturbation is important to gain insight into future ecosystem energy production and nutrient transfer. Using synchrotron-based Fourier transform infrared microspectroscopy, we examined the biomolecular composition of five dominant sea-ice diatom taxa from landfast ice communities covering a range of under-ice light conditions during spring, in Svalbard, Norway. In all five taxa, we saw a doubling of lipid and fatty acid content when light transmitted to the ice-water interface was >5% but <15% (85%-95% attenuation through snow and ice). We determined a threshold around 15% light transmittance after which biomolecular synthesis plateaued, likely because of photoinhibitory effects, except for Navicula spp., which continued to accumulate lipids. Increasing under-ice light availability led to increased energy allocation towards carbohydrates, but this was secondary to lipid synthesis, whereas protein content remained stable. It is predicted that under-ice light availability will change in the Arctic, increasing because of sea-ice thinning and potentially decreasing with higher snowfall. Our findings show that the nutritional content of sea-ice diatoms is taxon-specific and linked to these changes, highlighting potential implications for future energy and nutrient supply for the polar marine food web.

Phytoplankton-Bacteria Interactions 1.0.

Phytoplankton and bacteria regulate many essential functions in aquatic ecosystems [...].

Phytoplankton-Bacteria Interactions 2.0.

There are multiple ways in which phytoplankton and bacteria interact, starting from the fundamental symbiotic associations of direct attachment, through intimate interactions within the phytoplankton phycosphere, to random associations within the water column via the exudation and cycling of dissolved organic carbon (DOC) and other chemical compounds [...].

Lipid stores reveal the state of the coral-algae symbiosis at the single-cell level.

Coral reefs worldwide are threatened by environmental stress. The observable decline in coral cover, is principally due to the intensifying breakdown of the coral symbiosis, a process known as 'bleaching'. Overproduction of reactive oxygen species (ROS) is considered a key driver of coral bleaching, where environmental stress leads to increased ROS expression. To explore the link between ROS damage and symbiont status, we measured lipid peroxidation (LPO), a ubiquitous form of ROS damage, in the lipid stores of individual endo- and ex-symbiotic algal cells of three coral species, using confocal microscopy and a lipid hydroperoxide sensitive fluorescent dye. We found LPO was higher in endosymbionts, while lipid volume was greater in ex-symbiotic cells. Cluster analysis revealed three metabolic profiles differentiating endosymbiotic (#1: high LPO, low lipid) and ex-symbiotic cells (#3: low LPO, high lipid), with the intermediate group (#2) containing both cell types. Heat stress caused endosymbionts of Pocillopora acuta to shift away from cluster #1, suggesting this cluster represents cells in healthy/stable symbiosis. Our study delivers a new means to assess the coral symbiosis, demonstrating that symbiont LPO ratio combined with lipid store volume is a robust metabolic marker for the state of the symbiosis at the cellular level.

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.

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.

Ocean acidification alters the nutritional value of Antarctic diatoms.

Primary production in the Southern Ocean is dominated by diatom-rich phytoplankton assemblages, whose individual physiological characteristics and community composition are strongly shaped by the environment, yet knowledge on how diatoms allocate cellular energy in response to ocean acidification (OA) is limited. Understanding such changes in allocation is integral to determining the nutritional quality of diatoms and the subsequent impacts on the trophic transfer of energy and nutrients. Using synchrotron-based Fourier transform infrared microspectroscopy, we analysed the macromolecular content of selected individual diatom taxa from a natural Antarctic phytoplankton community exposed to a gradient of fCO2 levels (288-1263 µatm). Strong species-specific differences in macromolecular partitioning were observed under OA. Large taxa showed preferential energy allocation towards proteins, while smaller taxa increased both lipid and protein stores at high fCO2 . If these changes are representative of future Antarctic diatom physiology, we may expect a shift away from lipid-rich large diatoms towards a community dominated by smaller taxa, but with higher lipid and protein stores than their present-day contemporaries, a response that could have cascading effects on food web dynamics in the Antarctic marine ecosystem.

Biogeographical and seasonal dynamics of the marine Roseobacter community and ecological links to DMSP-producing phytoplankton.

Ecological interactions between marine bacteria and phytoplankton play a pivotal role in governing the ocean's major biogeochemical cycles. Among these, members of the marine Roseobacter Group (MRG) can establish mutualistic relationships with phytoplankton that are, in part, maintained by exchanges of the organosulfur compound, dimethylsulfoniopropionate (DMSP). Yet most of what is known about these interactions has been derived from culture-based laboratory studies. To investigate temporal and spatial co-occurrence patterns between members of the MRG and DMSP-producing phytoplankton we analysed 16S and 18S rRNA gene amplicon sequence variants (ASVs) derived from 5 years of monthly samples from seven environmentally distinct Australian oceanographic time-series. The MRG and DMSP-producer communities often displayed contemporaneous seasonality, which was greater in subtropical and temperate environments compared to tropical environments. The relative abundance of both groups varied latitudinally, displaying a poleward increase, peaking (MRG at 33% of total bacteria, DMSP producers at 42% of eukaryotic phototrophs) during recurrent spring-summer phytoplankton blooms in the most temperate site (Maria Island, Tasmania). Network analysis identified 20,140 significant positive correlations between MRG ASVs and DMSP producers and revealed that MRGs exhibit significantly stronger correlations to high DMSP producers relative to other DMSP-degrading bacteria (Pelagibacter, SAR86 and Actinobacteria). By utilising the power of a continental network of oceanographic time-series, this study provides in situ confirmation of interactions found in laboratory studies and demonstrates that the ecological dynamics of an important group of marine bacteria are shaped by the production of an abundant and biogeochemically significant organosulfur compound.

Uptake of Dimethylsulfoniopropionate (DMSP) by Natural Microbial Communities of the Great Barrier Reef (GBR), Australia.

Dimethylsulfoniopropionate (DMSP) is a key organic sulfur compound that is produced by many phytoplankton and macrophytes and is ubiquitous in marine environments. Following its release into the water column, DMSP is primarily metabolised by heterotrophic bacterioplankton, but recent evidence indicates that non-DMSP producing phytoplankton can also assimilate DMSP from the surrounding environment. In this study, we examined the uptake of DMSP by communities of bacteria and phytoplankton within the waters of the Great Barrier Reef (GBR), Australia. We incubated natural GBR seawater with DMSP and quantified the uptake of DMSP by different fractions of the microbial community (>8 µm, 3-8 µm, <3 µm). We also evaluated how microbial community composition and the abundances of DMSP degrading genes are influenced by elevated dissolved DMSP levels. Our results showed uptake and accumulation of DMSP in all size fractions of the microbial community, with the largest fraction (>8 µm) forming the dominant sink, increasing in particulate DMSP by 44-115% upon DMSP enrichment. Longer-term incubations showed however, that DMSP retention was short lived (<24 h) and microbial responses to DMSP enrichment differed depending on the community carbon and sulfur demand. The response of the microbial communities from inside the reef indicated a preference towards cleaving DMSP into the climatically active aerosol dimethyl sulfide (DMS), whereas communities from the outer reef were sulfur and carbon limited, resulting in more DMSP being utilised by the cells. Our results show that DMSP uptake is shared across members of the microbial community, highlighting larger phytoplankton taxa as potentially relevant DMSP reservoirs and provide new information on sulfur cycling as a function of community metabolism in deeper, oligotrophic GBR waters.

Corrigendum: Regional and Microenvironmental Scale Characterization of the Zostera muelleri Seagrass Microbiome.

[This corrects the article DOI: 10.3389/fmicb.2019.01011.].

Phenotypic trait variability as an indication of adaptive capacity in a cosmopolitan marine diatom.

Determining the adaptive capacity of marine phytoplankton is important in predicting changes in phytoplankton responses to ocean warming. Phytoplankton may consist of high levels of standing phenotypic and genetic variability, the basis of rapid evolution; however, few studies have quantified trait variability within and amongst closely related diatom species. Using 35 clonal cultures of the ubiquitous marine diatom Leptocylindrus isolated from six locations, spanning 2000 km of the south-eastern Australian coastline, we found evidence of significant intraspecific morphological and metabolic trait variability, which for 8 of 9 traits (growth rate, biovolume, C:N, silica deposition, silica incorporation rate, chl-a, and photosynthetic efficiency under dark adapted, growth irradiance, and high-light adaptation) were greater within a species than between species. Moreover, only two traits revealed a latitudinal trend with strains isolated from lower latitudes showing significantly higher silicification rates and protein:lipid content compared to their higher latitude counterparts. These data mirror recent studies on diatom intraspecific genetic diversity, which has found comparable levels of genetic diversity at a single site to those thousands of kilometres apart, and provide evidence of a functional role of diatom diversity that will allow for rapid adaptation via ecological selection on standing variation in response to changing conditions.

Microbial tropicalization driven by a strengthening western ocean boundary current.

Western boundary currents (WBCs) redistribute heat and oligotrophic seawater from the tropics to temperate latitudes, with several displaying substantial climate change-driven intensification over the last century. Strengthening WBCs have been implicated in the poleward range expansion of marine macroflora and fauna, however, the impacts on the structure and function of temperate microbial communities are largely unknown. Here we show that the major subtropical WBC of the South Pacific Ocean, the East Australian Current (EAC), transports microbial assemblages that maintain tropical and oligotrophic (k-strategist) signatures, to seasonally displace more copiotrophic (r-strategist) temperate microbial populations within temperate latitudes of the Tasman Sea. We identified specific characteristics of EAC microbial assemblages compared with non-EAC assemblages, including strain transitions within the SAR11 clade, enrichment of Prochlorococcus, predicted smaller genome sizes and shifts in the importance of several functional genes, including those associated with cyanobacterial photosynthesis, secondary metabolism and fatty acid and lipid transport. At a temperate time-series site in the Tasman Sea, we observed significant reductions in standing stocks of total carbon and chlorophyll a, and a shift towards smaller phytoplankton and carnivorous copepods, associated with the seasonal impact of the EAC microbial assemblage. In light of the substantial shifts in microbial assemblage structure and function associated with the EAC, we conclude that climate-driven expansions of WBCs will expand the range of tropical oligotrophic microbes, and potentially profoundly impact the trophic status of temperate waters.

Regional and Microenvironmental Scale Characterization of the Zostera muelleri Seagrass Microbiome.

Seagrasses are globally distributed marine plants that represent an extremely valuable component of coastal ecosystems. Like terrestrial plants, seagrass productivity and health are likely to be strongly governed by the structure and function of the seagrass microbiome, which will be distributed across a number of discrete microenvironments within the plant, including the phyllosphere, the endosphere and the rhizosphere, all different in physical and chemical conditions. Here we examined patterns in the composition of the microbiome of the seagrass Zostera muelleri, within six plant-associated microenvironments sampled across four different coastal locations in New South Wales, Australia. Amplicon sequencing approaches were used to characterize the diversity and composition of bacterial, microalgal, and fungal microbiomes and ultimately identify "core microbiome" members that were conserved across sampling microenvironments. Discrete populations of bacteria, microalgae and fungi were observed within specific seagrass microenvironments, including the leaves and roots and rhizomes, with "core" taxa found to persist within these microenvironments across geographically disparate sampling sites. Bacterial, microalgal and fungal community profiles were most strongly governed by intrinsic features of the different seagrass microenvironments, whereby microscale differences in community composition were greater than the differences observed between sampling regions. However, our results showed differing strengths of microbial preferences at the plant scale, since this microenvironmental variability was more pronounced for bacteria than it was for microalgae and fungi, suggesting more specific interactions between the bacterial consortia and the seagrass host, and potentially implying a highly specialized coupling between seagrass and bacterial metabolism and ecology. Due to their persistence within a given seagrass microenvironment, across geographically discrete sampling locations, we propose that the identified "core" microbiome members likely play key roles in seagrass physiology as well as the ecology and biogeochemistry of seagrass habitats.

Coral bleaching from a single cell perspective.

Ocean warming is resulting in increased occurrence of mass coral bleaching; a response in which the intracellular algal endosymbionts (Symbiodinium sp.) are expelled from the coral host due to physiological stress. This detrimental process is often attributed to overproduction of reactive oxygen species (ROS) that leak out of the endosymbionts and causes damage to the host cell, though direct evidence validating this link is limited. Here, for the first time, we used confocal microscopy and fluorescent dyes to investigate if endosymbiont ROS production significantly and predictably affects physiological parameters in its host cell. Heat treatment resulted in a 60% reduction in coral symbiont density, a ~70% increase in median endosymbiont ROS and a small reduction in photosystem efficiency (FV/FM, 11%), indicating absence of severe light stress. Notably, no other physiological parameters were affected in either endosymbionts or host cells, including reduced glutathione and ROS-induced lipid peroxidation. Taken together, the increase in endosymbiont ROS could not be linked to physiological damage in either partner, suggesting that oxidative stress is unlikely to have been the driver for symbiont expulsion in this study.

A multi-trait systems approach reveals a response cascade to bleaching in corals.

BACKGROUND: Climate change causes the breakdown of the symbiotic relationships between reef-building corals and their photosynthetic symbionts (genus Symbiodinium), with thermal anomalies in 2015-2016 triggering the most widespread mass coral bleaching on record and unprecedented mortality on the Great Barrier Reef. Targeted studies using specific coral stress indicators have highlighted the complexity of the physiological processes occurring during thermal stress, but have been unable to provide a clear mechanistic understanding of coral bleaching. RESULTS: Here, we present an extensive multi-trait-based study in which we compare the thermal stress responses of two phylogenetically distinct and widely distributed coral species, Acropora millepora and Stylophora pistillata, integrating 14 individual stress indicators over time across a simulated thermal anomaly. We found that key stress responses were conserved across both taxa, with the loss of symbionts and the activation of antioxidant mechanisms occurring well before collapse of the physiological parameters, including gross oxygen production and chlorophyll a. Our study also revealed species-specific traits, including differences in the timing of antioxidant regulation, as well as drastic differences in the production of the sulfur compound dimethylsulfoniopropionate during bleaching. Indeed, the concentration of this antioxidant increased two-fold in A. millepora after the corals started to bleach, while it decreased 70% in S. pistillata. CONCLUSIONS: We identify a well-defined cascading response to thermal stress, demarking clear pathophysiological reactions conserved across the two species, which might be central to fully understanding the mechanisms triggering thermally induced coral bleaching. These results highlight that bleaching is a conserved mechanism, but specific adaptations linked to the coral's antioxidant capacity drive differences in the sensitivity and thus tolerance of each coral species to thermal stress.

Reactive oxygen species (ROS) and dimethylated sulphur compounds in coral explants under acute thermal stress.

Coral bleaching is intensifying with global climate change. Although the causes for these catastrophic events are well understood, the cellular mechanism that triggers bleaching is not well established. Our understanding of coral bleaching processes is hindered by the lack of robust methods for studying interactions between host and symbiont at the single-cell level. Here, we exposed coral explants to acute thermal stress and measured oxidative stress, more specifically, reactive oxygen species (ROS), in individual symbiont cells. Furthermore, we measured concentrations of dimethylsulphoniopropionate (DMSP) and dimethylsulphoxide (DMSO) to elucidate the role of these compounds in coral antioxidant function. This work demonstrates the application of coral explants for investigating coral physiology and biochemistry under thermal stress and delivers a new approach to study host-symbiont interactions at the microscale, allowing us to directly link intracellular ROS with DMSP and DMSO dynamics.

A novel mechanism for host-mediated photoprotection in endosymbiotic foraminifera.

Light underpins the health and function of coral reef ecosystems, where symbiotic partnerships with photosynthetic algae constitute the life support system of the reef. Decades of research have given us detailed knowledge of the photoprotective capacity of phototrophic organisms, yet little is known about the role of the host in providing photoprotection in symbiotic systems. Here we show that the intracellular symbionts within the large photosymbiotic foraminifera Marginopora vertebralis exhibit phototactic behaviour, and that the phototactic movement of the symbionts is accomplished by the host, through rapid actin-mediated relocation of the symbionts deeper into the cavities within the calcium carbonate test. Using a photosynthetic inhibitor, we identified that the infochemical signalling for host regulation is photosynthetically derived, highlighting the presence of an intimate communication between the symbiont and the host. Our results emphasise the central importance of the host in photosymbiotic photoprotection via a new mechanism in foraminifera that can serve as a platform for exploring host-symbiont communication in other photosymbiotic organisms.

A Game of Russian Roulette for a Generalist Dinoflagellate Parasitoid: Host Susceptibility Is the Key to Success.

Marine microbial interactions involving eukaryotes and their parasites play an important role in shaping the structure of phytoplankton communities. These interactions may alter population densities of the main host, which in turn may have consequences for the other concurrent species. The effect generalist parasitoids exert on a community is strongly dependent on the degree of host specificity. Parvilucifera sinerae is a generalist parasitoid able to infect a wide range of dinoflagellates, including toxic-bloom-forming species. A density-dependent chemical cue has been identified as the trigger for the activation of the infective stage. Together these traits make Parvilucifera-dinoflagellate hosts a good model to investigate the degree of specificity of a generalist parasitoid, and the potential effects that it could have at the community level. Here, we present for the first time, the strategy by which a generalist dinoflagellate parasitoid seeks out its host and determine whether it exhibits host preferences, highlighting key factors in determining infection. Our results demonstrate that in its infective stage, P. sinerae is able to sense potential hosts, but does not actively select among them. Instead, the parasitoids contact the host at random, governed by the encounter probability rate and once encountered, the chance to penetrate inside the host cell and develop the infection strongly depends on the degree of host susceptibility. As such, their strategy for persistence is more of a game of Russian roulette, where the chance of survival is dependent on the susceptibility of the host. Our study identifies P. sinerae as a potential key player in community ecology, where in mixed dinoflagellate communities consisting of hosts that are highly susceptible to infection, parasitoid preferences may mediate coexistence between host species, reducing the dominance of the superior competitor. Alternatively, it may increase competition, leading to species exclusion. If, however, highly susceptible hosts are absent from the community, the parasitoid population could suffer a dilution effect maintaining a lower parasitoid density. Therefore, both host community structure and host susceptibility will determine infectivity in the field.