Coral bleaching patterns are the outcome of complex biological and environmental networking

© 2019 John Wiley & Sons Ltd Continued declines in coral reef health over the past three decades have been punctuated by severe mass coral bleaching-induced mortality events that have grown in intensity and frequency under climate change. Intensive global research efforts have therefore persistently focused on bleaching phenomena to understand where corals bleach, when and why—resulting in a large—yet still somewhat patchy—knowledge base. Particularly catastrophic bleaching-induced coral mortality events in the past 5 years have catalyzed calls for a more diverse set of reef management tools, extending far beyond climate mitigation and reef protection, to also include more aggressive interventions. However, the effectiveness of these various tools now rests on rapidly assimilating our knowledge base of coral bleaching into more integrated frameworks. Here, we consider how the past three decades of intensive coral bleaching research has established the basis for complex biological and environmental networks, which together regulate outcomes of bleaching severity. We discuss how we now have enough scaffold for conceptual biological and environmental frameworks underpinning bleaching susceptibility, but that new tools are urgently required to translate this to an operational system informing—and testing—bleaching outcomes. Specifically, adopting network models that can fully describe and predict metabolic functioning of coral holobionts, and how this functioning is regulated by complex doses and interactions among environmental factors. Identifying knowledge gaps limiting operation of such models is the logical step to immediately guide and prioritize future experiments and observations. We are at a time-critical point where we can implement new capacity to resolve how coral bleaching patterns emerge from complex biological–environmental networks, and so more effectively inform rapidly evolving ecological management and social adaptation frameworks aimed at securing the future of coral reefs

Working with Nature to Identify Coral Reefs with Increased Environmental Tolerance

Understanding what drives tolerance among coral species is key to deriving focused and effective management plans for the future. Corals have survived for millions of years and have witnessed great changes in the earth?s climate. This study compares coral species across growth environments looking at architectural differences within the skeletal structure and discusses how this may impact upon their tolerance to stress events. Results identify that variation occurs in the density of coral skeleton, density of aragonite and porosity of the skeleton. Symbiont population densities were found to be variable among coral species, but no significant differences were found across light environments. This study suggests that the micro-density of aragonite, laid down to form the coral skeleton, can vary from the previously assumed density of pure aragonite (2.94g cm-3). Massive corals were found to have greater variability within these values and to be significantly lower that aragonite deposited in the skeletons of branching corals. These differences in skeletal architecture may hold the key in discovering the fundamental variables driving coral tolerance differences. Coral skeleton density may alter the relationship at the skeletal-tissue interface, therefore influence bleaching severity. The ability to identify susceptibility of corals to stress via proxies such as skeletal architecture will enable direction of management to areas most at need and those most likely to become refugia in the future

Irradiance and nutrient-dependent effects on photosynthetic electron transport in Arctic phytoplankton: A comparison of two chlorophyll fluorescence-based approaches to derive primary photochemistry.

We employed Fast Repetition Rate fluorometry for high-resolution mapping of marine phytoplankton photophysiology and primary photochemistry in the Lancaster Sound and Barrow Strait regions of the Canadian Arctic Archipelago in the summer of 2019. Continuous ship-board analysis of chlorophyll a variable fluorescence demonstrated relatively low photochemical efficiency over most of the cruise-track, with the exception of localized regions within Barrow Strait, where there was increased vertical mixing and proximity to land-based nutrient sources. Along the full transect, we observed strong non-photochemical quenching of chlorophyll fluorescence, with relaxation times longer than the 5-minute period used for dark acclimation. Such long-term quenching effects complicate continuous underway acquisition of fluorescence amplitude-based estimates of photosynthetic electron transport rates, which rely on dark acclimation of samples. As an alternative, we employed a new algorithm to derive electron transport rates based on analysis of fluorescence relaxation kinetics, which does not require dark acclimation. Direct comparison of kinetics- and amplitude-based electron transport rate measurements demonstrated that kinetic-based estimates were, on average, 2-fold higher than amplitude-based values. The magnitude of decoupling between the two electron transport rate estimates increased in association with photophysiological diagnostics of nutrient stress. Discrepancies between electron transport rate estimates likely resulted from the use of different photophysiological parameters to derive the kinetics- and amplitude-based algorithms, and choice of numerical model used to fit variable fluorescence curves and analyze fluorescence kinetics under actinic light. Our results highlight environmental and methodological influences on fluorescence-based photochemistry estimates, and prompt discussion of best-practices for future underway fluorescence-based efforts to monitor phytoplankton photosynthesis

Defining the core microbiome of the symbiotic dinoflagellate, Symbiodinium

© 2017 Society for Applied Microbiology and John Wiley & Sons Ltd Dinoflagellates of the genus Symbiodinium underpin the survival and ecological success of corals. The use of cultured strains has been particularly important to disentangle the complex life history of Symbiodinium and their contribution to coral host physiology. However, these cultures typically harbour abundant bacterial communities which likely play important, but currently unknown, roles in Symbiodinium biology. We characterized the bacterial communities living in association with a wide phylogenetic diversity of Symbiodinium cultures (18 types spanning 5 clades) to define the core Symbiodinium microbiome. Similar to other systems, bacteria were nearly two orders of magnitude more numerically abundant than Symbiodinium cells and we identified three operational taxonomic units (OTUs) which were present in all cultures. These represented the α-proteobacterium Labrenzia and the γ-proteobacteria Marinobacter and Chromatiaceae. Based on the abundance and functional potential of bacteria harboured in these cultures, their contribution to Symbiodinium physiology can no longer be ignored

Large centric diatoms allocate more cellular nitrogen to photosynthesis to counter slower RUBISCO turnover rates

© 2014 Wu, Jeans, Suggett, Finkel and Campbell. Diatoms contribute ~40% of primary production in the modern ocean and encompass the largest cell size range of any phytoplankton group. Diatom cell size influences their nutrient uptake, photosynthetic light capture, carbon export efficiency, and growth responses to increasing pCO2. We therefore examined nitrogen resource allocations to the key protein complexes mediating photosynthesis across six marine centric diatoms, spanning 5 orders of magnitude in cell volume, under past, current and predicted future pCO2 levels, in balanced growth under nitrogen repletion. Membrane bound photosynthetic protein concentrations declined with cell volume in parallel with cellular concentrations of total protein, total nitrogen and chlorophyll. Larger diatom species, however, allocated a greater fraction (by 3.5-fold) of their total cellular nitrogen to the soluble Ribulose-1,5-bisphosphate Carboxylase Oxygenase (RUBISCO) carbon fixation complex than did smaller species. Carbon assimilation per unit of RUBISCO large subunit (C RbcL-1 s-1) decreased with cell volume, from ~8 to ~2 C RbcL-1 s-1 from the smallest to the largest cells. Whilst a higher allocation of cellular nitrogen to RUBISCO in larger cells increases the burden upon their nitrogen metabolism, the higher RUBISCO allocation buffers their lower achieved RUBISCO turnover rate to enable larger diatoms to maintain carbon assimilation rates per total protein comparable to small diatoms. Individual species responded to increased pCO2, but cell size effects outweigh pCO2 responses across the diatom species size range examined. In large diatoms a higher nitrogen cost for RUBISCO exacerbates the higher nitrogen requirements associated with light absorption, so the metabolic cost to maintain photosynthesis is a cell size-dependent trait

Dynamic variability of the phytoplankton electron requirement for carbon fixation in eastern Australian waters

© 2019 Elsevier B.V. Fast Repetition Rate fluorometry (FRRf) generates high-resolution measures of phytoplankton primary productivity as electron transport rates (ETRs). How ETRs scale to corresponding inorganic carbon (C) uptake rates (the so-called electron requirement for carbon fixation, Φe,C), inherently describes the extent and effectiveness with which absorbed light energy drives C-fixation. However, it remains unclear whether and how Φe,C follows predictable patterns for oceanographic datasets spanning physically dynamic, and complex, environmental gradients. We utilise a unique high-throughput approach, coupling ETRs and 14C-incubations to produce a semi-continuous dataset of Φe,C (n = 80), predominantly from surface waters, along the Australian coast (Brisbane to the Tasman Sea), including the East Australian Current (EAC). Environmental conditions along this transect could be generally grouped into cooler, more nutrient-rich waters dominated by larger size-fractionated Chl-a (>10 μm) versus warmer nutrient-poorer waters dominated by smaller size-fractionated Chl-a (<2 μm). Whilst Φe,C was higher for warmer water samples, environmental conditions alone explained <20% variance of Φe,C, and changes in predominant size-fraction(s) distributions of Chl-a (biomass) failed to explain variance of Φe,C. Instead, normalised Stern-Volmer non-photochemical quenching (NPQNSV = F0′/Fv′) was a better predictor of Φe,C, explaining ~55% of observed variability. NPQNSV is a physiological descriptor that accounts for changes in both long-term driven acclimation in non-radiative decay, and quasi-instantaneous PSII downregulation, and thus may prove a useful predictor of Φe,C across physically-dynamic regimes, provided the slope describing their relationship is predictable. We also consider recent advances in fluorescence-based corrections to evaluate the potential role of baseline fluorescence (Fb) in contributing to overestimation of Φe,C and the correlation between Φe,C and NPQNSV – in doing so, we highlight the need for Fb corrections for future field-based assessments of Φe,C

Divergence of photosynthetic strategies amongst marine diatoms.

Marine phytoplankton, and in particular diatoms, are responsible for almost half of all primary production on Earth. Diatom species thrive from polar to tropical waters and across light environments that are highly complex to relatively benign, and so have evolved highly divergent strategies for regulating light capture and utilization. It is increasingly well established that diatoms have achieved such successful ecosystem dominance by regulating excitation energy available for generating photosynthetic energy via highly flexible light harvesting strategies. However, how different light harvesting strategies and downstream pathways for oxygen production and consumption interact to balance excitation pressure remains unknown. We therefore examined the responses of three diatom taxa adapted to inherently different light climates (estuarine Thalassioisira weissflogii, coastal Thalassiosira pseudonana and oceanic Thalassiosira oceanica) during transient shifts from a moderate to high growth irradiance (85 to 1200 μmol photons m-2 s-1). Transient high light exposure caused T. weissflogii to rapidly downregulate PSII with substantial nonphotochemical quenching, protecting PSII from inactivation or damage, and obviating the need for induction of O2 consuming (light-dependent respiration, LDR) pathways. In contrast, T. oceanica retained high excitation pressure on PSII, but with little change in RCII photochemical turnover, thereby requiring moderate repair activity and greater reliance on LDR. T. pseudonana exhibited an intermediate response compared to the other two diatom species, exhibiting some downregulation and inactivation of PSII, but high repair of PSII and induction of reversible PSII nonphotochemical quenching, with some LDR. Together, these data demonstrate a range of strategies for balancing light harvesting and utilization across diatom species, which reflect their adaptation to sustain photosynthesis under environments with inherently different light regimes

The future of coral reefs subject to rapid climate change: Lessons from natural extreme environments

Global climate change and localized anthropogenic stressors are driving rapid declines in coral reef health. In vitro experiments have been fundamental in providing insight into how reef organisms will potentially respond to future climates. However, such experiments are inevitably limited in their ability to reproduce the complex interactions that govern reef systems. Studies examining coral communities that already persist under naturally-occurring extreme and marginal physicochemical conditions have therefore become increasingly popular to advance ecosystem scale predictions of future reef form and function, although no single site provides a perfect analog to future reefs. Here we review the current state of knowledge that exists on the distribution of corals in marginal and extreme environments, and geographic sites at the latitudinal extremes of reef growth, as well as a variety of shallow reef systems and reef-neighboring environments (including upwelling and CO 2 vent sites). We also conduct a synthesis of the abiotic data that have been collected at these systems, to provide the first collective assessment on the range of extreme conditions under which corals currently persist. We use the review and data synthesis to increase our understanding of the biological and ecological mechanisms that facilitate survival and success under sub-optimal physicochemical conditions. This comprehensive assessment can begin to: (i) highlight the extent of extreme abiotic scenarios under which corals can persist, (ii) explore whether there are commonalities in coral taxa able to persist in such extremes, (iii) provide evidence for key mechanisms required to support survival and/or persistence under sub-optimal environmental conditions, and (iv) evaluate the potential of current sub-optimal coral environments to act as potential refugia under changing environmental conditions. Such a collective approach is critical to better understand the future survival of corals in our changing environment. We finally outline priority areas for future research on extreme and marginal coral environments, and discuss the additional management options they may provide for corals through refuge or by providing genetic stocks of stress tolerant corals to support proactive management strategies

Taxonomic variability in the electron requirement for carbon fixation across marine phytoplankton.

Fast Repetition Rate fluorometry (FRRf) has been increasingly used to measure marine primary productivity by oceanographers to understand how carbon (C) uptake patterns vary over space and time in the global oceans. As FRRf measures electron transport rates through photosystem II (ETRPSII ), a critical, but difficult-to-predict conversion factor termed the "electron requirement for carbon fixation" (Φe,C ) is needed to scale ETRPSII to C-fixation rates. Recent studies have generally focused on understanding environmental regulation of Φe,C , while taxonomic control has been explored by only a handful of laboratory studies encompassing a limited diversity of phytoplankton species. We therefore assessed Φe,C for a wide range of marine phytoplankton (n=17 strains) spanning multiple taxonomic and size-classes. Data mined from previous studies were further considered to determine whether Φe,C variability could be explained by taxonomy versus other phenotypic traits influencing growth and physiological performance (e.g., cell size). We found that Φe,C exhibited considerable variability (~4-10 mol e- · [mol C]-1 ), and was negatively correlated with growth rate (R2 = 0.7, p < 0.01). Diatoms exhibited a lower Φe,C compared to chlorophytes during steady-state, nutrient-replete growth. Inclusion of meta-analysis data did not find significant relationships between Φe,C and class, or growth rate, although confounding factors inherent to methodological inconsistencies between studies likely contributed to this. Knowledge of empirical relationships between Φe,C and growth rate coupled with recent improvements in quantifying phytoplankton growth rates in-situ, facilitate up-scaling of FRRf campaigns to routinely derive Φe,C needed to assess ocean C-cycling

Engineering strategies to decode and enhance the genomes of coral symbionts

© 2017 Levin, Voolstra, Agrawal, Steinberg, Suggett and van Oppen. Elevated sea surface temperatures from a severe and prolonged El Niño event (2014-2016) fueled by climate change have resulted in mass coral bleaching (loss of dinoflagellate photosymbionts, Symbiodinium spp., from coral tissues) and subsequent coral mortality, devastating reefs worldwide. Genetic variation within and between Symbiodinium species strongly influences the bleaching tolerance of corals, thus recent papers have called for genetic engineering of Symbiodinium to elucidate the genetic basis of bleaching-relevant Symbiodinium traits. However, while Symbiodinium has been intensively studied for over 50 years, genetic transformation of Symbiodinium has seen little success likely due to the large evolutionary divergence between Symbiodinium and other model eukaryotes rendering standard transformation systems incompatible. Here, we integrate the growing wealth of Symbiodinium next-generation sequencing data to design tailored genetic engineering strategies. Specifically, we develop a testable expression construct model that incorporates endogenous Symbiodinium promoters, terminators, and genes of interest, as well as an internal ribosomal entry site from a Symbiodinium virus. Furthermore, we assess the potential for CRISPR/Cas9 genome editing through new analyses of the three currently available Symbiodinium genomes. Finally, we discuss how genetic engineering could be applied to enhance the stress tolerance of Symbiodinium, and in turn, coral reefs