Micronutrient content drives elementome variability amongst the Symbiodiniaceae

Camp, Emma F.; Nitschke, Matthew R.; Clases, David; Vega, Raquel González de; Reich, Hannah; Goyen, Samantha; Suggett, David J.

doi:10.1186/s12870-022-03512-0

Cited by 13 publications

(12 citation statements)

References 86 publications

(161 reference statements)

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“…Intriguingly, the Growth Rate Hypothesis (GRH) predicts a positive relationship between phosphorus (P) content and growth rate in invertebrates, where P content decreases due to allocation to RNA synthesis during the organism's growth 89 . Thus our observations for corals here add to the growing body of evidence refuting the GRH when P is not limiting and can be stored in excess [90][91][92] .…”

Section: Biological Responses To Nursery Propagationsupporting

confidence: 66%

Multiple trait approach to inform ecosystem service value of corals propagated for restoration on the Great Barrier Reef

Lendo,

Camp,

Edmondson

et al. 2023

Preprint

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Coral propagation- and planting-based reef restoration practices are accelerating globally, yet short-term “success” continues to be measured as broad metrics of coral survival and growth, even though goals are often centred on recovering broad ecosystem service values. As such, how restoration activities may impact healthy reef functioning remains uncertain. For example, trade-offs in resource acquisition and partitioning that potentially regulate growth vs survival may yield very different outcomes towards factors governing reef biogeochemical cycles. Here we considered a proof-of-concept “multi-trait” approach to capture how a broader range of functional traits reflect the expression of growth and survival for a key coral species (Acropora cf. hyacinthus) — impacted by recent mass bleaching events — propagated for restoration activities on the Great Barrier Reef (GBR), Australia. We examined a diverse array of bio-physical, bio-chemical, and skeletal traits (n = 91 traits) for wild (donor) colonies and their nursery-derived fragments from a 12-month growth period (Opal Reef, northern GBR). Nursery corals grew 20-25 times faster than their donor (wild) colonies, but both exhibited similar survivorship. Faster growth within nurseries was accompanied by more pigmented colonies (darker-coloured and with more symbionts), and higher photosynthesis, respiration, and calcification rates. However, despite these metabolic changes, biogeochemical properties of the nursery and reef corals (carbohydrates, lipids, proteins, elemental stoichiometry, and skeletal properties) remained largely the same after 12 months, suggesting the bio-energetic value to trophic transfer as well as the structural rigour of corals was unaltered by nursery propagation. Thus, a “multi-trait” approach enables more informed evaluation as to how propagation activities impact diverse ecosystem service values, highlighting the immense importance of this knowledge in choosing coral individuals for restoration. Our example provides confidence to practitioners that key ecosystem service attributes of native corals are largely retained through an intermediate nursery growth phase that can accelerate coral biomass gains.

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Section: Biological Responses To Nursery Propagationsupporting

confidence: 66%

Multiple trait approach to inform ecosystem service value of corals propagated for restoration on the Great Barrier Reef

Lendo,

Camp,

Edmondson

et al. 2023

Preprint

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“…We speculate that these variations might be attributed to the presence of distinct Symbiodiniaceae hosted in C. caespitosa ( Symbiodinium microadriaticum ) and O. patagonica ( Breviolum psygmophylum ) ( Rodolfo-Metalpa et al, 2008 ; Casado-Amezúa et al., 2014 ; Martinez et al, 2021 ; Davies et al, 2023 ). Different Symbiodiniaceae species may exhibit differences in their tolerance to iron exposure, indicating species-specific nutrient requirements ( Reich et al, 2020 ; Camp et al, 2022 ). Species-specific responses to elevated Fe(III) concentration also indicate that unique biogeochemical niches play a key role in the metabolic compatibility of the coral-Symbiodiniaceae symbiosis ( Grima et al, 2022 ).…”

Section: Discussionmentioning

confidence: 99%

Contrasting effects of increasing dissolved iron on photosynthesis and O₂ availability in the gastric cavity of two Mediterranean corals

Dellisanti,

Zhang,

Ferrier-Pagès

et al. 2024

PeerJ

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Iron (Fe) plays a fundamental role in coral symbiosis, supporting photosynthesis, respiration, and many important enzymatic reactions. However, the extent to which corals are limited by Fe and their metabolic responses to inorganic Fe enrichment remains to be understood. We used respirometry, variable chlorophyll fluorescence, and O2 microsensors to investigate the impact of increasing Fe(III) concentrations (20, 50, and 100 nM) on the photosynthetic capacity of two Mediterranean coral species, Cladocora caespitosa and Oculina patagonica. While the bioavailability of inorganic Fe can rapidly decrease, we nevertheless observed significant physiological effects at all Fe concentrations. In C. caespitosa, exposure to 50 nM Fe(III) increased rates of respiration and photosynthesis, while the relative electron transport rate (rETR(II)) decreased at higher Fe(III) exposure (100 nM). In contrast, O. patagonica reduced respiration, photosynthesis rates, and maximum PSII quantum yield (Fv/Fm) across all iron enrichments. Both corals exhibited increased hypoxia (<50 µmol O2 L−1) within their gastric cavity at night when exposed to 50 and 100 nM Fe(III), leading to increased polyp contraction time and reduced O2 exchange with the surrounding water. Our results indicate that C. caespitosa, but not O. patagonica, might be limited in Fe for achieving maximal photosynthetic efficiency. Understanding the multifaceted role of iron in corals’ health and their response to environmental change is crucial for effective coral conservation.

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“…Utilizing organismal metal stoichiometry as a key trait to reveal biochemical niches and predict responses to climate change will improve trait‐based investigations of coral functional ecology (Camp et al ., 2022). Resolving how environmental conditions and different metal sources affect metal stoichiometry will enable such use of metallomes as indicators of abiotic stress and feeding ecology.…”

Section: Future Research Directionsmentioning

confidence: 99%

“…Less appreciated in comparison to the many studies on macronutrients [see reviews by D'Angelo & Wiedenmann (2014), Shantz & Burkepile (2014) and Morris et al . (2019)] is that the family Symbiodiniaceae, and dinoflagellates in general, have higher metal requirements relative to other microalgae (Rodriguez et al ., 2016; Reich et al ., 2020 a ; Camp et al ., 2022). For example, electron transfer between photosystems will not occur unless Fe and Mn are bound to the D1 and D2 photosystem II (PSII) proteins (psbA, psbD; Raven, Evans & Korb, 1999), therefore without these metals, photosynthetic capacity would be effectively eliminated.…”

Section: Introductionmentioning

confidence: 99%

The trace metal economy of the coral holobiont: supplies, demands and exchanges

et al. 2022

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The juxtaposition of highly productive coral reef ecosystems in oligotrophic waters has spurred substantial interest and progress in our understanding of macronutrient uptake, exchange, and recycling among coral holobiont partners (host coral, dinoflagellate endosymbiont, endolithic algae, fungi, viruses, bacterial communities). By contrast, the contribution of trace metals to the physiological performance of the coral holobiont and, in turn, the functional ecology of reef‐building corals remains unclear. The coral holobiont's trace metal economy is a network of supply, demand, and exchanges upheld by cross‐kingdom symbiotic partnerships. Each partner has unique trace metal requirements that are central to their biochemical functions and the metabolic stability of the holobiont. Organismal homeostasis and the exchanges among partners determine the ability of the coral holobiont to adjust to fluctuating trace metal supplies in heterogeneous reef environments. This review details the requirements for trace metals in core biological processes and describes how metal exchanges among holobiont partners are key to sustaining complex nutritional symbioses in oligotrophic environments. Specifically, we discuss how trace metals contribute to partner compatibility, ability to cope with stress, and thereby to organismal fitness and distribution. Beyond holobiont trace metal cycling, we outline how the dynamic nature of the availability of environmental trace metal supplies can be influenced by a variability of abiotic factors (e.g. temperature, light, pH, etc.). Climate change will have profound consequences on the availability of trace metals and further intensify the myriad stressors that influence coral survival. Lastly, we suggest future research directions necessary for understanding the impacts of trace metals on the coral holobiont symbioses spanning subcellular to organismal levels, which will inform nutrient cycling in coral ecosystems more broadly. Collectively, this cross‐scale elucidation of the role of trace metals for the coral holobiont will allow us to improve forecasts of future coral reef function.

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Micronutrient content drives elementome variability amongst the Symbiodiniaceae

Cited by 13 publications

References 86 publications

Multiple trait approach to inform ecosystem service value of corals propagated for restoration on the Great Barrier Reef

Multiple trait approach to inform ecosystem service value of corals propagated for restoration on the Great Barrier Reef

Contrasting effects of increasing dissolved iron on photosynthesis and O₂ availability in the gastric cavity of two Mediterranean corals

The trace metal economy of the coral holobiont: supplies, demands and exchanges

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Micronutrient content drives elementome variability amongst the Symbiodiniaceae

Cited by 13 publications

References 86 publications

Multiple trait approach to inform ecosystem service value of corals propagated for restoration on the Great Barrier Reef

Multiple trait approach to inform ecosystem service value of corals propagated for restoration on the Great Barrier Reef

Contrasting effects of increasing dissolved iron on photosynthesis and O2 availability in the gastric cavity of two Mediterranean corals

The trace metal economy of the coral holobiont: supplies, demands and exchanges

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Product

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Contrasting effects of increasing dissolved iron on photosynthesis and O₂ availability in the gastric cavity of two Mediterranean corals