Photosynthesis and net primary productivity in three Antarctic diatoms: Possible significance for their distribution in the Antarctic marine ecosystem

Photosynthesis and net primary productivity were measured in 3 Antarctic diatoms, Fragilariopsis cylindrus, Pseudo-nitzschia subcurvata and Chaetoceros sp., exposed to rapid changes in temperature and salinity representing a range of conditions found during a seasonal cycle. Measured differences in fluorescence-derived photosynthetic activity and oxygen evolution suggested that some alternative electron cycling activity was present under high irradiances. F. cylindrus displayed the highest rates of relative electron transport and net primary productivity under all salinity and temperature combinations and showed adaptive traits towards the sea-icelike environment. P. subcurvata displayed a preference for low saline conditions where production rates were greatest. However, there was evidence of photosynthetic sensitivity to the lowest temperatures and highest salinities, suggesting a lack of adaptation for dealing with sea-ice-like conditions. Chaetoceros sp. showed high plasticity, acclimating well to all conditions but performing best under pelagic conditions. The study shows species-specific sensitivities to environmental change, highlighting photosynthetic capacity as a potentially important mechanism in ecological niche adaptation. When these data were modelled over different seasons, integrated daily net primary production was greatest under summer pelagic conditions. The findings from this study support the general observations of light control and seasonal development of net primary productivity and species succession in the Antarctic marine ecosystem. © Inter-Research 2011

Coral bleaching from a single cell perspective

© 2018 The Author(s). 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 (F V/F M, 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

Single-cell biomolecular analysis of coral algal symbionts reveals opposing metabolic responses to heat stress and expulsion

© 2018 Petrou, Nielsen and Heraud. The success of corals in nutrient poor environments is largely attributed to the symbiosis between the cnidarian host and its intracellular alga. Warm water anomalies have been shown to destabilize this symbiosis, yet detailed analysis of the effect of temperature and expulsion on cell-specific carbon and nutrient allocation in the symbiont is limited. Here, we exposed colonies of the hard coral Acropora millepora to heat stress and using synchrotron-based infrared microspectroscopy measured the biomolecular profiles of individual in hospite and expelled symbiont cells at an acute state of bleaching. Our results showed symbiont metabolic profiles to be remarkably distinct with heat stress and expulsion, where the two effectors elicited opposing metabolic adjustments independent of treatment or cell type. Elevated temperature resulted in biomolecular changes reflecting cellular stress, with relative increases in free amino acids and phosphorylation of molecules and a concomitant decline in protein content, suggesting protein modification and degradation. This contrasted with the metabolic profiles of expelled symbionts, which showed relative decreases in free amino acids and phosphorylated molecules, but increases in proteins and lipids, suggesting expulsion lessens the overall effect of heat stress on the metabolic signature of the algal symbionts. Interestingly, the combined effects of expulsion and thermal stress were additive, reducing the overall shifts in all biomolecules, with the notable exception of the significant accumulation of lipids and saturated fatty acids. This first use of a single-cell metabolomics approach on the coral symbiosis provides novel insight into coral bleaching and emphasizes the importance of a single-cell approach to demark the cell-to-cell variability in the physiology of coral cellular populations

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

Desiccation stress in two intertidal beachrock biofilms

© Springer-Verlag Berlin Heidelberg 2014. Chlorophyll a fluorescence was used to look at the effect of desiccation on the photophysiology in two beachrock microbial biofilms from the intertidal rock platform of Heron Island, Australia. The photophysiological response to desiccation differed between the beachrock microbial communities. The black biofilm from the upper shoreline, dominated by Calothrix sp., showed a response typical of desiccation-tolerant cyanobacteria, where photosynthesis closed down during air exposure with a rapid and complete recovery upon rehydration. In contrast, the pink biofilm from the mid-intertidal zone, dominated by Blennothrix sp., showed no distinct response to desiccation stress and instead maintained reduced photosynthesis throughout drying and re-wetting cycles. Spatial differences in photosynthetic activity within the black biofilm were evident with a faster recovery rate of photosynthesis in the surface cyanobacteria than in the deeper layers of the biofilm. There was no variation with depth in the pink biofilm. The photophysiological differences in desiccation responses between the beachrock biofilms exemplify the ecological niche specialisation of these complex microbial communities, where the functional differences help to explain their vertical distribution on the intertidal shoreline

From the ice to the open ocean : threats to phytoplankton productivity in the Antarctic marine ecosystem from a changing climate

University of Technology, Sydney. Faculty of Science.The Antarctic marine ecosystem is unique and dynamic, changing seasonally and forming specialised niche habitats including open ocean, sea ice and meltwater environments. Phytoplankton are key species in the structure and function of the Antarctic ecosystem, instrumental in the regions biogeochemistry, fundamental to the food web and strong contributors to global primary production and carbon sequestration. Understanding the photosynthetic plasticity of Antarctic phytoplankton is essential to understanding the effects global change is likely to have on primary production in the region. Through a series of experiments, this thesis explores the processes of light acclimation, photoprotection and photoinhibition in Antarctic microalgae under different environmental stressors, comparing photophysiological responses of species known to inhabit the sea-ice, meltwater and pelagic regions of Antarctic waters. The photosynthetic properties of three Antarctic diatoms (Fragilariopsis cylindrus, Pseudo-nitzschia subcurvata and Chaetoceros sp.) to changes in salinity, temperature and light were compared. Large heterogeneities in the photoprotective capacity of the three species and several distinct physiological strategies in response to the rapid changes in the ambient environment were observed (Publication I). Similarly, photosynthesis and net primary productivity was species-specific with large differences between environmental conditions (Publication II). Fast induction kinetics and pulse amplitude modulated fluorometry were used to demonstrate high levels of flexibility in light acclimation capabilities of sea ice algae from the east Antarctic. Inhibitors and pigment analyses identified xanthophyll cycling as the critical mechanism for photoprotection and preferred means by which sea ice diatoms regulated energy flow to PS1 (Publication III). While immunoblot analyses of natural communities measured minimal D1 protein breakdown in algae exposed to irradiances up to 200 µmol photons m⁻² s⁻¹. These data showed that sea ice diatoms had low intrinsic susceptibility to PSII photoinactivation and strong irradiance-dependent induction of non-photochemical quenching that was independent of protein resynthesis (Publication IV). The remaining chapters investigated photoprotective strategies and photosynthetic plasticity of phytoplankton under nutrient limitation. Nitrogen depletion in F. cylindrus had a strong influence on non-photochemical quenching capacity and resulted in the impairment of photosynthetic electron transport resulting in the formation of Qʙ non-reducing PSII centres within the photosystem (Publication V). The influence of iron-limitation and high light stress on the growth and physiology of Southern Ocean phytoplankton revealed a community-based response of measurable changes in pigment ratios, photosynthetic capacity and community composition (Publication VI). Iron-limited phytoplankton altered the allocation of photosynthetically derived energy, increasing photoprotective pigment pools and down-regulating photochemistry, at the expense of photosynthetic plasticity

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

© 2017. Published by The Company of Biologists Ltd. 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

Characterisation of coral explants: a model organism for cnidarian–dinoflagellate studies

© 2014, Springer-Verlag Berlin Heidelberg. Coral cell cultures made from reef-building scleractinian corals have the potential to aid in the pursuit of understanding of the cnidarian–dinoflagellate symbiosis. Various methods have previously been described for the production of cell cultures in vitro with a range of success and longevity. In this study, viable tissue spheroids containing host tissue and symbionts (coral explants) were grown from the tissues of Fungia granulosa. The cultured explants remained viable for over 2 months and showed morphological similarities in tissue structure and internal microenvironment to reef-building scleractinian corals. The photophysiology of the explants (1 week old) closely matched that of the parent coral F. granulosa. This study provides the first empirical basis for supporting the use of coral explants as laboratory models for studying coral symbioses. In particular, it highlights how these small, self-sustaining, skeleton-free models can be useful for a number of molecular, genetic and physiological analyses necessary for investigating host–symbiont interactions at the microscale

The impact of iron limitation on the physiology of the Antarctic diatom Chaetoceros simplex

Iron availability strongly governs the growth of Southern Ocean phytoplankton. To investigate how iron limitation affects photosynthesis as well as the uptake of carbon and iron in the Antarctic diatom Chaetoceros simplex, a combination of chlorophyll a fluorescence measurements and radiotracer incubations in the presence and absence of chemical inhibitors was conducted. Iron limitation in C. simplex led to a decline in growth rates, photochemical efficiency and structural changes in photosystem II (PSII), including a reorganisation of photosynthetic units in PSII and an increase in size of the functional absorption cross section of PSII. Iron-limited cells further exhibited a reduced plastoquinone pool and decreased photosynthetic electron transport rate, while non-photochemical quenching and relative xanthophyll pigment content were strongly increased, suggesting a photoprotective response. Additionally, iron limitation resulted in a strong decline in carbon fixation and thus the particulate organic carbon quotas. Inhibitor studies demonstrated that, independent of the iron supply, carbon fixation was dependent on internal, but not on extracellular carbonic anhydrase activity. Orthovanadate more strongly inhibited iron uptake in iron-limited cells, indicating that P-type ATPase transporters are involved in iron uptake. The stronger reduction in iron uptake by ascorbate in iron-limited cells suggests that the re-oxidation of iron is required before it can be taken up and further supports the presence of a high-affinity iron transport pathway. The measured changes to photosystem architecture and shifts in carbon and iron uptake strategies in C. simplex as a result of iron limitation provide evidence for a complex interaction of these processes to balance the iron requirements for photosynthesis and carbon demand for sustained growth in iron-limited waters. © 2014 The Author(s)

A game of russian roulette for a generalist dinoflagellate parasitoid: Host susceptibility is the key to success

© 2016 Alacid, Park, Turon, Petrou and Garcés. 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