Clinton A Oakley | Victoria University of Wellington (original) (raw)

Papers by Clinton A Oakley

Applied and Environmental Microbiology

Coral reefs are in serious decline, in particular due to the thermally induced dysfunction of the... more Coral reefs are in serious decline, in particular due to the thermally induced dysfunction of the cnidarian-dinoflagellate symbiosis that underlies their success. Yet our ability to react to this crisis is hindered by limited knowledge of how this symbiosis functions.

Frontiers in Microbiology

The mutualistic cnidarian–dinoflagellate symbiosis underpins the evolutionary success of stony co... more The mutualistic cnidarian–dinoflagellate symbiosis underpins the evolutionary success of stony corals and the persistence of coral reefs. However, a molecular understanding of the signalling events that lead to the successful establishment and maintenance of this symbiosis remains unresolved. For example, the phosphatidylinositol (PI) signalling pathway has been implicated during the establishment of multiple mutualistic and parasitic interactions across the kingdoms of life, yet its role within the cnidarian-dinoflagellate symbiosis remains unexplored. Here, we aimed to confirm the presence and assess the specific enzymatic composition of the PI signalling pathway across cnidaria and dinoflagellates by compiling 21 symbiotic anthozoan (corals and sea anemones) and 28 symbiotic dinoflagellate (Symbiodiniaceae) transcriptomic and genomic datasets and querying genes related to this pathway. Presence or absence of PI-kinase and PI-phosphatase orthologs were also compared between a broa...

Journal of Experimental Biology

The establishment and maintenance of the symbiosis between a cnidarian host and its dinoflagellat... more The establishment and maintenance of the symbiosis between a cnidarian host and its dinoflagellate symbionts is central to the success of coral reefs. To explore the metabolite production underlying this symbiosis, we focused on a group of low molecular weight secondary metabolites, biogenic volatile organic compounds (BVOCs). BVOCs are released from an organism or environment, and can be collected in the gas phase, allowing non-invasive analysis of an organism's metabolism (i.e. ‘volatilomics’). We characterised volatile profiles of the sea anemone Aiptasia (Exaiptasia diaphana), a model system for cnidarian–dinoflagellate symbiosis, using comprehensive two-dimensional gas chromatography coupled with time-of-flight mass spectrometry. We compared volatile profiles between: (1) symbiotic anemones containing their native symbiont, Breviolum minutum; (2) aposymbiotic anemones; and (3) cultured isolates of B. minutum. Overall, 152 BVOCs were detected, and classified into 14 groups b...

Advances in Marine Biology

Applied Environmental Metabolomics

The dinoflagellate family Symbiodiniaceae comprises numerous genera and species with large differ... more The dinoflagellate family Symbiodiniaceae comprises numerous genera and species with large differences in diversity, ecology and geographic distribution. An evolutionarily divergent lineage common in temperate symbiotic cnidarians and designated in the literature by several informal names including 'temperate–A', AI, Phylotype A´ (A-prime) and 'Mediterranean A', is here assigned to the genus Philozoon. This genus was proposed by Geddes (1882) in one of the earliest papers that recognized 'yellow cells' as distinct biological entities separate from their animal and protist hosts. Using phylogenetic data from nuclear (rDNA), chloroplast (cp23S) and mitochondrial genes (cob and cox1), as well as morphology (cell size), ecological traits (host affinity) and geographic distributions, we emend the genus Philozoon Geddes and two of its species, P. medusarum&lt...

Journal of Phycology, 2013

Global Change Biology, 2011

Coral reefs of the Florida Keys typically experience seasonal temperatures of 20-31°C. Deviation ... more Coral reefs of the Florida Keys typically experience seasonal temperatures of 20-31°C. Deviation outside this range causes physiological impairment of reef-building corals, potentially leading to coral colony death. In January and February 2010, two closely spaced cold fronts, possibly driven by an unusually extreme Arctic Oscillation, caused sudden and severe seawater temperature declines in the Florida Keys. Inshore coral reefs [e.g., Admiral Reef (ADM)] experienced lower sustained temperatures (i.e., < 12°C) than those further offshore [e.g., Little Grecian Reef (LG), minimum temperature = 17.2°C]. During February and March 2010, we surveyed ADM and observed a mass die-off of reef-building corals, whereas 12 km away LG did not exhibit coral mortality. We subsequently measured the physiological effects of low-temperature stress on three common reef-building corals (i.e., Montastraea faveolata, Porites astreoides, and Siderastrea siderea) over a range of temperatures that replicated the inshore cold-water anomaly (i.e., from 20 to 16 to 12°C and back to 20°C). Throughout the temperature modulations, coral respiration as well as endosymbiont gross photosynthesis and maximum quantum efficiency of photosystem II were measured. In addition, Symbiodinium genotypic identity, cell densities, and chlorophyll a content were determined at the beginning and conclusion of the experiment. All corals were significantly affected at 12°C, but species-specific physiological responses were found indicating different coral and/or Symbiodinium cold tolerances. Montastraea faveolata and P. astreoides appeared to be most negatively impacted because, upon return to 20°C, significant reductions in gross photosynthesis and dark respiration persisted. Siderastrea siderea, however, readily recovered to pre-treatment rates of dark respiration and gross photosynthesis. Visual surveys of inshore reefs corroborated these results, with S. siderea being minimally affected by the cold-water anomaly, whereas M. faveolata and P. astreoides exhibited nearly 100% mortality. This study highlights the importance of understanding the physiological attributes of genotypically distinct coral-Symbiodinium symbioses that contribute to tolerance, recovery, and consequences to an environmental perturbation. These data also document effects of a rarely studied environmental stressor, possibly initiated by remote global climate events, on coral-Symbiodinium symbioses and coral reef communities.

Coral Reefs, 2014

A terminal electron acceptor alternative to mitochondrial cytochrome c oxidase (COX), mitochondri... more A terminal electron acceptor alternative to mitochondrial cytochrome c oxidase (COX), mitochondrial alternative oxidase (AOX), is ubiquitous in higher plants and represented in nearly every algal taxon but is poorly documented in dinoflagellates. AOX competes for electrons with the conventional COX and has been hypothesized to function as a means of reducing oxidative stress in mitochondria, as well as a potential mechanism for ameliorating thermal and other physiological stressors. Here, the presence of an active AOX in cultured Symbiodinium was assayed by the response of oxygen consumption to the AOX inhibitor salicylhydroxamic acid (SHAM) and the COX inhibitor cyanide (CN). CN-insensitive, SHAM-sensitive oxygen consumption was found to account for a large portion (26 %) of Symbiodinium dark respiration and is consistent with high levels of AOX activity. This experimental evidence of the existence of a previously unreported terminal oxidase was further corroborated by analysis of publicly available Symbiodinium transcriptome data. The potential for enhanced AOX expression to play a compensatory role in mediating thermal stress was supported by inhibitor assays of cultured Symbiodinium at low (18 °C), moderate (26 °C), and high (32 °C) temperature conditions. Maximum capacity of the putative AOX pathway as a proportion of total dark oxygen consumption was found to increase from 26 % at 26 °C to 45 % and 53 % at 18 °C and 32 °C, respectively, when cells were acclimated to the treatment temperatures. Cells assayed at 18 and 32 °C without acclimation exhibited either the same or lower AOX capacity as controls, suggesting that the AOX protein is upregulated under temperature stress. The physiological implications for the presence of AOX in the coral/algal symbiosis and its potential role in response to many forms of biotic and abiotic stress, particularly oxidative stress, are discussed.

Coral Reefs, 2014

The symbiosis between hermatypic corals and their dinoflagellate endosymbionts, genus Symbiodiniu... more The symbiosis between hermatypic corals and their dinoflagellate endosymbionts, genus Symbiodinium, is based on carbon exchange. This symbiosis is disrupted by thermally induced coral bleaching, a stress response in which the coral host expels its algal symbionts as they become physiologically impaired. The disruption of the dissolved inorganic carbon (DIC) supply or the thermal inactivation of Rubisco have been proposed as sites of initial thermal damage that leads to the bleaching response. Symbiodinium possesses a highly unusual Form II ribulose bisphosphate carboxylase/oxygenase (Rubisco), which exhibits a lower CO2:O2 specificity and may be more thermally unstable than the Form I Rubiscos of other algae and land plants. Components of the CO2 concentrating mechanism (CCM), which supplies inorganic carbon for photosynthesis, may also be temperature sensitive. Here, we examine the ability of four cultured Symbiodinium strains to acquire and fix DIC across a temperature gradient. Surprisingly, the half-saturation constant of photosynthesis with respect to DIC concentration (KP), an index of CCM function, declined with increasing temperature in three of the four strains, indicating a greater potential for photosynthetic carbon acquisition at elevated temperatures. In the fourth strain, there was no effect of temperature on KP. Finding no evidence for thermal inhibition of the CCM, we conclude that CCM components are not likely to be the primary sites of thermal damage. Reduced photosynthetic quantum yields, a hallmark of thermal bleaching, were observed at low DIC concentrations, leaving open the possibility that reduced inorganic carbon availability is involved in bleaching.

Applied Vegetation Science, 2012

Methods We planted 62 3× 3 m plots on compacted clay subsoil with 20–21 replicates of three, 12 a... more Methods We planted 62 3× 3 m plots on compacted clay subsoil with 20–21 replicates of three, 12 and 24 native species. Plots were sampled non-destructively using a stratified random point-intercept method each summer for 5 yr to determine number of species and percentage cover per species, which were classified as residents (planted), internal non-residents (planted in other plots) or external non-residents. Results A negative relationship between planted species richness and invasion developed by the fourth year after ...

Limnology and Oceanography: Methods, Dec 1, 2012

Conventional means of assessing net photosynthetic rates of microalgae have largely relied upon t... more Conventional means of assessing net photosynthetic rates of microalgae have largely relied upon the use of oxygen electrodes or carbon isotope radiolabeling. These methods are simple but inadequately resolve simultaneous fluxes of the gaseous substrates and products of photosynthesis, CO2, and O2. Fluorometric methods allow for assessment of the photosynthetic efficiency of excitation energy capture by the light-harvesting complexes and electron transport chain, but do not directly measure photosynthetic rates, because ...

Within microeukaryotes, genetic and functional variation sometimes accumulate more quickly than m... more Within microeukaryotes, genetic and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellies), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: speci...

Scientific Data

The Symbiodiniaceae are a taxonomically and functionally diverse family of marine dinoflagellates... more The Symbiodiniaceae are a taxonomically and functionally diverse family of marine dinoflagellates. Their symbiotic relationship with invertebrates such as scleractinian corals has made them the focus of decades of research to resolve the underlying biology regulating their sensitivity to stressors, particularly thermal stress. Research to-date suggests that Symbiodiniaceae stress sensitivity is governed by a complex interplay between phylogenetic dependent and independent traits (diversity of characteristics of a species). Consequently, there is a need for datasets that simultaneously broadly resolve molecular and physiological processes under stressed and non-stressed conditions. Therefore, we provide a dataset simultaneously generating transcriptome, metabolome, and proteome data for three ecologically important Symbiodiniaceae isolates under nutrient replete growth conditions and two temperature treatments (ca. 26 °C and 32 °C). Elevated sea surface temperature is primarily respo...

Jupyter notebook containing code to correlate transcript sequence and protein sequence abundance.... more Jupyter notebook containing code to correlate transcript sequence and protein sequence abundance. Code prepared for manuscript "Proteomics reveals that a thermally tolerant but suboptimal symbiont compromises nutrient exchange functions in a model cnidarian" by Sproles, Oakley et al.

Coral reef ecosystems are metabolically founded on the mutualism between corals and photosyntheti... more Coral reef ecosystems are metabolically founded on the mutualism between corals and photosynthetic dinoflagellates of the genus Symbiodinium. The glass anemone Aiptasia sp. has become a tractable model for this symbiosis, and recent advances in genetic information have enabled the use of mass spectrometry-based proteomics in this model. We utilized label-free liquid chromatography electrospray-ionization tandem mass spectrometry to analyze the effects of symbiosis on the proteomes of symbiotic and aposymbiotic Aiptasia. We identified and obtained relative quantification of more than 3,300 proteins in 1,578 protein clusters, with 81 protein clusters showing significantly different expression between symbiotic states. Symbiotic anemones showed significantly higher expression of proteins involved in lipid storage and transport, nitrogen transport and cycling, intracellular trafficking, endocytosis and inorganic carbon transport. These changes reflect shifts in host metabolism and nutrient reserves due to increased nutritional exchange with the symbionts, as well as mechanisms for supplying inorganic nutrients to the algae. Aposymbiotic anemones exhibited increased expression of multiple systems responsible for mediating reactive oxygen stress, suggesting that the host derives direct or indirect protection from oxidative stress while in symbiosis. Aposymbiotic anemones also increased their expression of an array of proteases and chitinases, indicating a metabolic shift from autotrophy to heterotrophy. These results provide a comprehensive Aiptasia proteome with more direct relative quantification of protein abundance than transcriptomic methods. The extension of "omics" techniques to this model system will allow more powerful studies of coral physiology, ecosystem function, and the effects of biotic and abiotic stress on the coral-dinoflagellate mutualism.

All supplementary figures, tables and methods for the manuscript "Partner switching and meta... more All supplementary figures, tables and methods for the manuscript "Partner switching and metabolic flux in a model cnidarian- dinoflagellate symbiosis"

Scientific Reports

In oligotrophic waters, cnidarian hosts rely on symbiosis with their photosynthetic dinoflagellat... more In oligotrophic waters, cnidarian hosts rely on symbiosis with their photosynthetic dinoflagellate partners (family Symbiodiniaceae) to obtain the nutrients they need to grow, reproduce and survive. For this symbiosis to persist, the host must regulate the growth and proliferation of its symbionts. One of the proposed regulatory mechanisms is arrest of the symbiont cell cycle in the G1 phase, though the cellular mechanisms involved remain unknown. Cell-cycle progression in eukaryotes is controlled by the conserved family of cyclin-dependent kinases (CDKs) and their partner cyclins. We identified CDKs and cyclins in different Symbiodiniaceae species and examined their relationship to homologs in other eukaryotes. Cyclin proteins related to eumetazoan cell-cycle-related cyclins A, B, D, G/I and Y, and transcriptional cyclin L, were identified in the Symbiodiniaceae, alongside several alveolate-specific cyclin A/B proteins, and proteins related to protist P/U-type cyclins and apicomple...

European Journal of Phycology, 2021

Applied and Environmental Microbiology

Frontiers in Microbiology

Journal of Experimental Biology

Advances in Marine Biology

Applied Environmental Metabolomics

Journal of Phycology, 2013

Global Change Biology, 2011

Coral Reefs, 2014

Applied Vegetation Science, 2012

Limnology and Oceanography: Methods, Dec 1, 2012

Scientific Data

Scientific Reports

European Journal of Phycology, 2021