Analyzing Adaptation Mechanisms in Artificial Transplantation of Galaxea fascicularis

doi:10.21203/rs.3.rs-4792475/v1

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Analyzing Adaptation Mechanisms in Artificial Transplantation of Galaxea fascicularis

https://doi.org/10.21203/rs.3.rs-4792475/v1

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Coral reefs are among Earth's most biologically diverse and ecologically crucial ecosystems but face severe threats from climate change and human activities. Coral transplantation has become a key strategy for reef restoration. This study focused on transplanting Galaxea fascicularis at northern Wuzhizhou Island, Hainan, assessing physiological characteristics and metabolomic differences between transplanted and parent corals at 1, 6, and 12 months post-transplantation. Findings revealed that transplanted coral survival rates declined rapidly during the first 6 months but then stabilized. An algal bloom in May 2023 increased turbidity, dissolved inorganic nitrogen (DIN), and partial pressure of pCO₂, negatively impacting coral photosynthesis and calcification and increasing physiological stress. From months 6 to 12, environmental conditions improved, with temperature and salinity aligning closely with natural conditions, dissolved oxygen levels recovering, turbidity decreasing significantly, and Ω_arag reaching moderate levels, facilitating stable coral growth and calcification. By 12 months, transplanted corals reached sexual maturity, with notable increases in protein and lipid content. Metabolomic analysis showed that during the short-term (1 month) and mid-term (6 months) post-transplantation periods, the arachidonic acid metabolic pathway was upregulated while the glycerophosphate metabolic pathway was downregulated, enabling corals to cope with environmental stress and resource redistribution. By 12 months, oxidative phosphorylation was upregulated to meet reproductive energy demands. Results demonstrate that G. fascicularis can adapt well to restoration environments and achieve sexual maturity quickly, making it a suitable candidate for reef restoration.

Galaxea fascicularis

Artificial Transplantation

Coral Restoration

Metabolomics

Adaptation Mechanism

Coral reefs are among Earth's most diverse and ecologically crucial ecosystems (Castro-Sanguino et al. 2021), providing essential habitats, coastal protection, fisheries, and tourism benefits (Massei et al. 2023). They face severe threats from climate change, pollution, overfishing, and other disturbances (Niz et al. 2023), leading to widespread coral bleaching and mortality (Andradi-Brown et al. 2020). Coral transplantation is a promising conservation strategy, involving the relocation of healthy coral fragments or larvae to degraded reefs to restore ecological functions (Ferse et al. 2021; Lang et al., 2024). Success depends on environmental conditions and coral species (Williams et al. 2019). Post-transplantation, corals undergo significant physiological and metabolic changes affecting survival and adaptation (Uribe-Castañeda et al. 2018). Understanding these mechanisms is essential for improving transplantation techniques and restoration outcomes.

Metabolomics is an advanced scientific approach that examines the physiological state and response mechanisms of organisms through a comprehensive analysis of their small molecular metabolites (Hu et al. 2020). This technique is instrumental in unveiling the adaptive mechanisms of corals to environmental fluctuations. For instance, Roach et al. (2001) have demonstrated that metabolomic disparities in naturally bleached corals remain consistent over time, identifying betaine lipids as key biomarkers of coral bleaching. Similarly, Zhao et al. (2024) have explored the metabolomic heterogeneity of Acropora hyacinthus under both transplantation and natural conditions, revealing that differential metabolites can drive phenotypic variations, directing more energy towards growth rather than developmental processes. By investigating the metabolomic variations among corals, we can pinpoint individuals with superior adaptability and restoration potential, thereby refining coral transplantation methodologies and bolstering the restoration and preservation of coral reef ecosystems (Schmidt-Roach et al. 2020).

Current research predominantly focuses on the transplantation of branching corals, with relatively limited attention given to massive corals. Boström-Einarsson et al. (2020) have noted that coral reef restoration projects have been implemented in at least 56 countries, utilizing 229 species from 72 coral genera, encompassing approximately 25% of reef-building coral species. However, these projects primarily target fast-growing branching coral species, which, despite their rapid growth, are highly sensitive to environmental disturbances. In contrast, the more resilient but slower-growing massive corals are frequently overlooked (Guest et al. 2023). The slow growth rate of massive corals often results in restoration outcomes that are visually unimpressive and fail to meet immediate expectations, leading to their neglect (Marshall and Baird 2000; Hein et al. 2020). Additionally, the unique structural characteristics of massive corals pose significant challenges during transplantation, further contributing to the lack of research focus on these species (Edwards and Clark 1999). Nevertheless, massive corals play an indispensable role in coral reef ecosystems. Their robust and durable structures provide critical physical support to the reefs, creating habitats and shelter for diverse marine organisms, thereby enhancing biodiversity (Glassom et al. 2004).

Investigating the metabolomic changes in massive corals during transplantation and assessing their long-term performance post-transplantation is essential for evaluating transplantation success, adaptive responses, and long-term survival. In the northern part of Wuzhizhou Island, Hainan, we conducted an experiment involving the transplantation of massive corals. We selected Galaxea fascicularis, the dominant coral species of Wuzhizhou Island, and transplanted it onto our custom-designed restoration device, the "Trapezoidal Reef". Samples were collected at three key intervals, 1 month, 6 months, and 12 months post-transplantation, to analyze the physiological characteristics and metabolomic differences between transplanted and parent G. fascicularis. This study aimed to elucidate the adaptive changes occurring during the transplantation process, providing fundamental scientific data for future transplantation efforts of G. fascicularis and contributing to the broader field of coral reef restoration.

2.1 Experimental Site and Sample Collection

In April 2023, we established a coral reef restoration site in northern Wuzhizhou by installing 12 trapezoidal reef devices (Fig. 1a). Each device featured eight designated transplantation points for massive corals (Fig. 1b). Divers meticulously collected and tagged fragments of G. fascicularis from the natural reef area. Using hammers and chisels, small coral fragments were carefully extracted and transplanted onto the trapezoidal reefs within the restoration area, resulting in a total of 96 transplanted fragments of G. fascicularis.

To assess the transplantation outcomes, we collected samples at 1 month (May 2023), 6 months (October 2023), and 12 months (April 2024) post-transplantation. At each time point, six tagged parent corals and six transplanted corals were retrieved. The collected samples were divided into two portions: one part was immediately preserved in liquid nitrogen for subsequent UPLC-MS/MS analysis, while the other part was used for measuring physiological indicators.

2.2 Measurement of Coral Physiological Indicators

Upon collection, coral samples were immediately transported to the laboratory for analysis. Throughout the experiment, the maximum quantum efficiency of coral (Fv/Fm) was measured using the MINI-PAM-II chlorophyll fluorometer (Walz, Germany). To assess zooxanthellae density, coral surfaces were washed with a Waterpik dental cleaner (Water-pik, WP70-EC, USA). A specific volume of the wash solution (10 mL) was measured and counted using a hemocytometer, with the process repeated eight times to obtain an average value. This method follows the protocol of Li et al. (2006).

Chlorophyll a was extracted using an Addison reagent kit and quantified with a spectrophotometer, as per Fitt et al. (2000). To determine coral tissue content, samples were dried at 60℃ for 24 hours to obtain dry weight and subsequently ashed at 400℃ in a muffle furnace for 4 hours to measure ash weight. The difference in mass pre- and post-ashing represents the coral tissue content. Coral surface area was measured using the aluminum foil method (Stimson 1997).

Carbohydrate content was determined according to Dubois et al. (1956). Ground coral samples were extracted with phenol and concentrated sulfuric acid, and their absorbance was measured at A490 using a spectrophotometer. Absorbance values were converted to concentration using a glucose standard curve. Protein extraction followed the method of Smith et al. (2017). Ground coral samples were processed with a BCA reagent kit, and their absorbance was measured at A562. Concentrations were calculated using a protein standard curve.

Lipid extraction adhered to the protocol by Rodrigues and Grottoli (2007). Approximately 1 g of wet coral sample was extracted with CM solution (methanol/chloroform 1:2, v/v). About 20 mL of CM extract was added to 1 g of coral and incubated in the dark for 24 hours. The organic phase was then evaporated and dried in an oxygen-free environment to determine lipid content. All data were standardized to the coral surface area.

2.3 Metabolome Analysis

2.3.1 Metabolite Extraction

A solid sample of 10 mg was accurately weighed, and metabolites were extracted using 400 µL of methanol (4:1, v/v) solution containing 0.02 mg/mL L-2-chlorophenylalanine as an internal standard. The mixture was allowed to settle at -10℃ and then processed with a high-throughput tissue crusher Wonbio-96c at 50 Hz for 6 minutes, followed by ultrasound at 40 kHz for 30 minutes at 5℃. Samples were then placed at -20℃ for 30 minutes to precipitate proteins. After centrifugation at 13,000 g at 4℃ for 15 minutes, the supernatant was carefully transferred to sample vials for LC-MS/MS analysis.

2.3.2 Quality Control (QC) Sample

As part of the system conditioning and QC process, a pooled QC sample was prepared by mixing equal volumes from all samples. The QC samples were processed and analyzed in the same manner as the analytical samples. This pooled QC sample served as a representative of the entire sample set and was injected at regular intervals (every six samples) to ensure and monitor the stability and reliability of the analysis.

2.3.3 UHPLC-MS/MS Analysis

The UHPLC-MS analysis was conducted using the UHPLC-Q Exactive HF-X system from Thermo Fisher Scientific. Chromatographic separation was achieved using an HSS T3 column (100 mm × 2.1 mm i.d., 1.8 µm), with 2 µL of each sample injected for MS detection. The mobile phases consisted of 0.1% formic acid in water (95:5, v/v) (solvent A) and 0.1% formic acid in acetonitrile: isopropanol (47.5:47.5:5, v/v) (solvent B). The solvent gradient was programmed as follows: from 0 to 3.5 min, 0% B to 24.5% B (0.4 mL/min); from 3.5 to 5 min, 24.5% B to 65% B (0.4 mL/min); from 5 to 5.5 min, 65% B to 100% B (0.4 mL/min); from 5.5 to 7.4 min, 100% B (0.4 mL/min to 0.6 mL/min); from 7.4 to 7.6 min, 100% B to 51.5% B (0.6 mL/min); from 7.6 to 7.8 min, 51.5% B to 0% B (0.6 mL/min to 0.5 mL/min); from 7.8 to 9 min, 0% B (0.5 mL/min to 0.4 mL/min); and from 9 to 10 min, 0% B (0.4 mL/min) to equilibrate the system. The sample injection volume was 2 µL, with a flow rate set at 0.4 mL/min. The column temperature was maintained at 40℃, and all samples were stored at 4℃ during the analysis period.

2.3.4 MS Conditions:

The MS data were collected using a Thermo UHPLC-Q Exactive HF-X Mass Spectrometer equipped with an electrospray ionization (ESI) source, operating in both positive and negative ion modes. The optimal conditions for the mass spectrometer were set as follows: heater temperature at 425℃, capillary temperature at 325℃, sheath gas flow rate at 50 arb, aux gas flow rate at 13 arb, and ion-spray voltage floating (ISVF) at -3,500 V for negative mode and 3,500 V for positive mode. The normalized collision energy was set at 20-40-60 V rolling for MS/MS. The full MS resolution was configured at 60,000, while the MS/MS resolution was set at 7,500. Data acquisition was performed in Data Dependent Acquisition (DDA) mode, with detection conducted over a mass range of 70 − 1,050 m/z.

2.3.5 Data Preprocessing and Annotation

Upon completion of MS detection, the raw LC/MS data were preprocessed using Progenesis QI software. A three-dimensional data matrix in CSV format was exported, containing details such as sample identifiers, metabolite names, and mass spectral response intensities. Internal standard peaks and known false positive peaks, including noise, column bleed, and derivatized reagent peaks, were removed from the data matrix. The data were then further processed to eliminate redundancies and pooled based on peak intensities. Metabolite identification was conducted using databases such as HMDB (http://www.hmdb.ca/), Metlin (https://metlin.scripps.edu/), and the Majorbio Database. The resulting data were uploaded to the Majorbio cloud platform (https://cloud.majorbio.com) for comprehensive analysis.

Metabolic features detected in at least 80% of any sample set were retained after filtration. For samples where metabolite levels fell below the lower limit of quantitation, minimum metabolite values were imputed. Each metabolic feature was normalized by sum to mitigate errors introduced during sample preparation and due to instrument variability. The response intensity of sample MS peaks was normalized using the sum normalization method, producing a standardized data matrix. Variables with a relative standard deviation (RSD) exceeding 30% in QC samples were excluded. A log10 transformation was then applied to the final data matrix for further analysis.

2.3.6 Differential Metabolite Analysis

Following data preprocessing, variance analysis was conducted on the matrix file. Principal component analysis (PCA) and orthogonal partial least squares discriminant analysis (OPLS-DA) were performed using the R package "ropls" (Version 1.6.2). A 7-cycle cross-validation was employed to assess the model's stability and reliability. Additionally, Student's t-test and fold difference analysis were conducted to identify significant differences between groups. Significantly different metabolites were identified based on the variable importance in projection (VIP) obtained from the OPLS-DA model, alongside the p-value from the Student's t-test. Metabolites with a VIP value greater than 1 and a p-value less than 0.05 were deemed statistically significant and selected for further analysis.

Differential metabolites between the groups were summarized and mapped to their corresponding biochemical pathways using metabolic enrichment and pathway analysis, based on database searches such as KEGG (http://www.genome.jp/kegg/). The identified metabolites were categorized according to the pathways they are involved in or the functions they perform. Enrichment analysis was conducted to determine whether a group of metabolites was overrepresented in a particular functional node. This analysis extended the annotation from individual metabolites to groups of metabolites. The statistical significance of enriched pathways was determined using Fisher's exact test, implemented with the "scipy.stats" Python package (https://docs.scipy.org/doc/scipy/).

2.4 Water Quality Sample Collection

To monitor key seawater parameters, an AQUAlogger 310TY turbidity meter, OS310 CTD, and YSI water quality analyzer were deployed to capture data on turbidity, temperature (WT), salinity (SAL), dissolved oxygen (DO), depth (WD), and pH. Seawater samples were collected from the bottom near the reef base in each sampling area using water sampling bottles. These samples were meticulously filtered through 0.45-µm glass fiber membranes and acidified with dilute hydrochloric acid. Subsequently, 100 mL of the filtrate was stored in reagent bottles.

The concentrations of dissolved inorganic nutrients, including NH₄⁺, NO₃^-, NO₂^-, SiO₃^2-, and PO₄^3-, were quantified using a SEAL AA3 automatic nutrient analyzer. Additionally, these samples were analyzed for dissolved inorganic carbon (DIC), partial pressure of carbon dioxide (pCO₂), and aragonite saturation (Ω_arag) using the advanced CO₂ system software by Pierrot et al. (2006).

2.5 Data Analysis

Physiological data were expressed as mean ± S.D., with the exception of metabolic group data. Statistical analyses were performed using Origin 2024b. Initially, the data were assessed to determine if they met the prerequisites for hypothesis testing, which included checking for normality using the Shapiro-Wilk test and testing for homogeneity of variance using Levene's test. For data that satisfied these conditions, an independent-sample t-test was conducted. The significance level was set at P < 0.05.

3.1 Water Quality Monitoring

In May 2023, environmental factors were meticulously measured and analyzed in both the natural and restoration areas of northern Wuzhizhou Island, Hainan (Table S1). A significant event during this period was a large-scale algal bloom, which profoundly impacted various environmental indicators. This bloom led to marked increases in turbidity, dissolved inorganic nitrogen (DIN), and pCO₂ in the restoration area.

By October 2023, and continuing into April 2024, these environmental factors began to stabilize, with most indicators in the restoration area approaching levels observed in the natural area, such as water temperature and salinity. However, notable differences remained; the natural area maintained higher levels of DO and Ω_arag at both time points. These elevated levels of DO and lower turbidity in the natural area facilitated enhanced coral calcification and photosynthesis.

In April 2024, the restoration area showed a significant increase in DO levels, which reached comparable heights to those of the natural area. This improvement supported enhanced coral respiration and metabolic activities, indicating a positive shift in the environmental conditions within the restoration site, fostering better conditions for coral health and growth.

3.2 Survival Rate and Physiological Indicators of Transplanted Corals

The survival rate of transplanted G. fascicularis corals exhibited a notable decline from 100–64.58% within the first 6 months post-transplantation, with no further coral deaths observed between 6 and 12 months (Fig. 2a). A critical factor contributing to coral mortality was the use of plastic ties for attachment. By the 12th month, corals that had shed their ties demonstrated a significantly higher survival rate (Fig. 2b), while those with intact ties experienced nearly 100% mortality (Fig. 2c).

Surviving corals exhibited normal gonadal development, capable of producing mature sperm (Fig. 2d) and eggs (Fig. 2e). Physiological assessments indicated that the Fv/Fm of transplanted G. fascicularis was significantly lower than that of parent corals after 1 month. However, by the 6th month, the Fv/Fm values of transplanted corals recovered, showing no significant difference compared to parent corals (Fig. 2f).

As the transplantation period extended, both zooxanthellae density and coral biomass showed steady accumulation, reaching peak levels in both transplanted and parent corals by the 12th month (Fig. 2g, i). Throughout the study, there were no significant differences in chlorophyll a and carbohydrate content among the groups (Fig. 2h, j). By the 12th month, both transplanted and parent G. fascicularis reached sexual maturity, exhibiting significantly higher protein and lipid content compared to earlier time points (Fig. 2k, l).

3.2 Comparative Analysis of Samples

According to PLS-DA, the metabolic profiles of transplanted corals progressively aligned with those of parent corals over time, indicating a gradual acclimatization (Fig. 3a, d, g). The distance between transplanted and parent coral samples decreased, demonstrating this convergence in metabolic patterns. Concurrently, the number of differential metabolites declined from 422 at 1 month to 343 at 6 months, and finally to 265 at 12 months (Fig. 3b, e, h). This reduction in differential metabolites suggested that the physiological activities of transplanted corals were increasingly mirroring those of the parent corals.

Specific metabolites showed significant changes during this period. Hydroxyethyl methacrylic acid was notably upregulated in the transplanted corals at 1 month (VIP = 5.75, P < 0.001) (Fig. 3c). At 6 months, neamine was significantly upregulated (VIP = 6.48, P < 0.001) (Fig. 3f). By 12 months, 15-keto-prostaglandin F2a exhibited significant upregulation in the transplanted corals (VIP = 5.00, P < 0.001) (Fig. 3i). These findings highlighted the dynamic metabolic adjustments that transplanted corals underwent to adapt to their new environment, ultimately achieving physiological states similar to their parent counterparts.

3.3 KEGG Analysis

KEGG pathway analysis revealed significant enrichment patterns among the upregulated and downregulated differential metabolites at various post-transplantation time points. At 1 month and 6 months post-transplantation, upregulated differential metabolites were predominantly enriched in the arachidonic acid metabolic pathway (Fig. 4a, b). This indicated an early metabolic response to transplantation stress and adaptation processes.

However, by 12 months post-transplantation, the upregulated differential metabolites showed a shift in pathway enrichment, no longer concentrating in the arachidonic acid metabolic pathway. Instead, they were significantly enriched in the oxidative phosphorylation pathway (Fig. 4c). This transition suggested a shift in the metabolic focus of the transplanted corals towards enhanced energy production to support growth and reproductive processes.

Conversely, at all three time points, 1 month, 6 months, and 12 months post-transplantation, the downregulated differential metabolites were consistently enriched in the glycerophospholipid metabolic pathway (Fig. 4a, b, c). This consistent downregulation implied a potential redistribution of resources away from membrane lipid synthesis and maintenance, possibly reallocating metabolic efforts towards other critical functions necessary for adaptation and survival. These KEGG analysis results provided a comprehensive view of the dynamic metabolic adjustments occurring in transplanted corals, highlighting key pathways involved in their acclimation and long-term adaptation processes.

3.4 Analysis of Key Metabolic Pathways and Metabolite Content

Glycerophospholipid metabolism was significantly downregulated across all three sampling periods. Within this pathway, only lysophosphatidylcholine (LPC) exhibited significant changes in expression patterns over time. The arachidonic acid pathway showed significant upregulation at 1 and 6 months post-transplantation, but no notable changes were observed at 12 months. Specifically, metabolites such as 20-Hydroxyeicosatetraenoic acid (20-HETE), 11,12-DiHETrE (11,12-DHET), and 8,9-DiHETrE (8,9-DHET) displayed significant expression changes at the 1- and 6-month marks.

Lecithin emerged as a pivotal metabolite linking glycerophospholipid metabolism and the arachidonic acid pathway (Fig. 5a). In glycerophospholipid metabolism, lecithin is catalyzed by the enzymes lecithin-cholesterol acyltransferase (LCAT) and secretory phospholipase A2 (sPLA2) to produce LPC. Subsequently, LPC is transformed into other metabolites, such as choline, phosphocholine, and sGPC, through various pathways. Within the arachidonic acid pathway, lecithin is converted into arachidonate under the catalytic action of sPLA2. Arachidonate is then metabolized to produce 20-HETE through the action of long-chain fatty acid omega-monooxygenase (CYP4A), phylloquinone omega-hydroxylase (CYP4F), and long-chain fatty acid omega-monooxygenase (CYP4U), while 11,12-DHET and 8,9-DHET are generated via more complex metabolic routes.

Significant differences in LPC content were observed between transplanted and parent corals at 1, 6, and 12 months, with transplanted corals consistently showing downregulated expression (Fig. 5b, c, d). For 20-HETE, significant differences were noted at 1 and 6 months, with upregulated expression in transplanted corals (Fig. 5e, f). Similarly, 11,12-DHET and 8,9-DHET content differed significantly between transplanted and parent corals at 1 and 6 months, with both metabolites showing upregulated expression in the transplanted corals (Fig. 5g, h, i, j). These findings underscored the intricate metabolic adjustments and adaptations occurring in transplanted corals, highlighting the critical roles of glycerophospholipid and arachidonic acid pathways in their physiological acclimation.

Most current coral transplantation efforts focus on asexual reproduction by transplanting coral fragments to restore damaged reefs (Patterson et al. 2016). This study further confirmed the asexual reproduction potential of G. fascicularis. By employing appropriate transplantation techniques and optimizing environmental conditions, G. fascicularis not only adapted swiftly to the new environment but also achieved a commendable survival rate.

Beyond validating the efficacy of asexual reproduction, our study revealed that G. fascicularis could attain sexual maturity within a short transplantation period, specifically within 1 year. This rapid maturation suggested that future restoration efforts could enhance the genetic diversity and overall health of coral communities (Castillo et al. 2024). The ability of G. fascicularis to reproduce both asexually and sexually in a relatively short timeframe provided a dual approach to reef restoration, offering a robust strategy for improving resilience and adaptive capacity in coral ecosystems. These findings underscored the potential for integrated coral restoration strategies that leverage both asexual and sexual reproduction to rebuild and sustain diverse, resilient coral populations. This dual reproductive capability of G. fascicularis could play a pivotal role in future coral restoration projects, contributing to the long-term health and stability of reef ecosystems.

4.1 Survival Rate and Physiological Changes of Transplanted Corals

Despite potential manual operation errors, we maintained transplanted G. fascicularis fragments at approximately 6 cm × 6 cm, while parent colonies exceeded 30 cm in diameter. Unpublished experiments in Wuzhizhou revealed that fragments from larger A. hyacinthus and Acropora microphthalma parent colonies could not reach sexual maturity within 2 years. Similarly, Zhao et al. (2024) have found that transplanted A. hyacinthus prioritizes growth over reproductive development. Ligson et al. (2021) have reported that Acropora verweyi requires 4 years to achieve sexual maturity.

In contrast, G. fascicularis demonstrated remarkable adaptability by developing gonads while ensuring both survival and growth. Wei et al. (2023) have observed that large, wild-collected adult G. fascicularis shows normal gonadal development after 2 years in an artificial environment, consistent with our findings where transplanted G. fascicularis reached sexual maturity within 1 year. Environmental factors such as light, tides, and water flow in Wuzhizhou’s natural environment likely accelerated maturity compared to controlled indoor conditions.

Studies on massive corals such as Favites colemani and Favites abdita (Guest et al. 2023) show that over 50% survive nursery acclimatization, with only a 10–14% decrease in survival 4 years post-transplantation. After 6 years, over 90% of the transplanted corals reach reproductive maturity. These findings suggest that restoring reproductive maturity in large coral populations within 10 years is feasible.

The results of this study indicated that transplanting coral fragments from natural colonies could achieve similar reproductive maturity outcomes at a faster rate and lower cost compared to traditional methods. G. fascicularis, with its strong adaptability and rapid reproductive development, presented a viable candidate for effective coral reef restoration efforts.

In this study, we observed that the survival rate of transplanted corals decreased rapidly within the first 6 months but remained stable between the 6th and 12th months. This trend is commonly seen in coral restoration efforts and suggests that once transplanted corals acclimate to the restoration environment, their physiological state can remain relatively stable (Ligson et al. 2021). Initially, environmental conditions such as a large-scale algal bloom in May 2023 increased turbidity, adversely affecting light penetration and photosynthesis (Palomar et al. 2009). High concentrations of DIN and phosphate (PO₄^3-) promoted algal growth, further degrading water quality (Zhao et al. 2013). Elevated pCO₂ led to water acidification, impacting coral calcification and reducing survival rates (Nakamura et al. 2018). These stresses resulted in a decrease in Fv/Fm and zooxanthellae density, contributing to lower survival rates (Wall et al. 2018).

From the 6th to 12th months, the stabilization of environmental conditions supported consistent coral survival. Favorable changes in temperature and salinity, comparable to those in the natural area, facilitated coral growth (Beck et al. 2022). Improved levels of DO and reduced turbidity in April 2024 restored coral photosynthetic capacity (Carlson et al. 2022). Enhanced Ω_arag levels supported calcification processes (Martinez et al. 2019). As a result, the transplanted corals exhibited significantly higher protein and lipid content compared to natural corals after 12 months (Kaposi et al. 2023; Keister et al. 2023; Jung et al. 2021). Achieving sexual maturity, a crucial indicator of transplantation success, showed that transplanted corals could complete their life cycle and reproduce. Coral eggs and sperm, rich in lipids required for energy and cell structure, benefited from the improved conditions (Padilla-Gamiño et al. 2011).

In the restoration area, the trapezoidal reef provided a relatively stable and suitable growth environment, optimizing light conditions, which likely contributed to the rapid growth and development of transplanted corals (Gomez-Campo et al. 2024). G. fascicularis demonstrated strong adaptability, making it an ideal candidate for coral restoration due to its ability to acclimate within 6 months.

Our field investigation revealed that traditional binding methods might significantly contribute to the mortality of transplanted corals. Although plastic ties are inexpensive and easy to use (Tortolero-Langarica et al. 2019), they inflicted severe physical damage on G. fascicularis. These ties covered the corals' large calices, obstructing their respiration and feeding, which could ultimately lead to death. While some G. fascicularis managed to recover from this trauma, the overall recovery rate remained low. The energy expended on trauma recovery slows growth and increases survival pressure (Kaufman et al. 2021).

In contrast, corals that detached from the ties due to growth breaking the ties, plastic degradation, or ocean currents exhibited higher survival rates and successfully attached to the restoration devices. These corals matured, producing sperm or eggs, which underscored the necessity of improving current binding methods to minimize physical harm and enhance survival rates. This finding highlighted the need for alternative attachment techniques that do not impede the natural physiological processes of the corals.

4.2 Synergistic Effects of Arachidonic Acid Metabolism and Glycerophospholipid Metabolism in Short-term (1 month) and Mid-term (6 months) Adaptation of Transplanted Corals

In this study, we focused on the significant metabolic changes in arachidonic acid and glycerophospholipid pathways during the coral transplantation process. Transplanted G. fascicularis underwent a series of metabolic adjustments to adapt to the new environmental conditions. At 1 and 6 months post-transplantation, the arachidonic acid metabolic pathway was upregulated, while the glycerophospholipid metabolic pathway was significantly downregulated. These two pathways are biochemically interlinked, and alterations in one can induce corresponding changes in the other (Hanna and Hafez 2018). Glycerophospholipids are essential components of cell membranes and are hydrolyzed by PLA2 to produce arachidonic acid and lysophospholipids (Sikorskaya 2023). This process not only involves membrane phospholipid metabolism and remodeling but also impacts numerous signaling pathways.

Our findings revealed a significant increase in arachidonic acid levels in G. fascicularis samples 1 month post-transplantation, with elevated levels persisting at 6 months. This finding underscored the crucial role of the arachidonic acid metabolic pathway in coral adaptation. Arachidonic acid metabolism facilitates stress response, inflammation regulation, antioxidation, and cell protection (Safuan et al. 2021). During the initial transplantation stage, it generates bioactive molecules like prostaglandins, which aid in coral tissue repair and defense against pathogens (Agalias et al. 2020). Additionally, increased levels of 20-HETE were observed at 1 and 6 months post-transplantation. 20-HETE modulates the severity and duration of inflammatory responses, supporting coral tissue survival and health (Lock et al. 2020).

Moreover, the metabolites 11,12-DHET and 8,9-DHET, products of arachidonic acid metabolism, act as antioxidants, playing vital roles in responding to environmental and oxidative stress (Chhonker et al. 2018). These metabolites enhance antioxidant capacity by activating NF-κB and Nrf2 signaling pathways, thereby increasing the expression of cellular antioxidant genes (Zhang et al. 2022). This interplay between arachidonic acid and glycerophospholipid metabolism is critical for the short-term and mid-term adaptation of transplanted corals, facilitating their survival and acclimation in new environments.

On the other hand, the downregulation of glycerophospholipid metabolism plays a crucial role in cell membrane remodeling and the adjustment of energy metabolism in transplanted corals. Experimental results indicate that during the initial phase of transplantation, the synthesis and degradation of glycerophospholipids, such as phosphatidylcholine and phosphatidylethanolamine, proceed rapidly to address cell membrane damage and facilitate reconstruction (Imbs 2013). LPC is a significant intermediate in the glycerophospholipid metabolic pathway, possessing various physiological functions (Stien et al. 2020).

One month post-transplantation, corals begin to acclimate to the new environmental conditions, and the initial intense stress response starts to subside. As cellular oxidative stress levels decrease, the demand for LPC as an antioxidant molecule also diminishes (Tang et al. 2019). Consequently, LPC expression levels begin to downregulate. Cell membrane remodeling, which is critical during the early stages of transplantation, involves a substantial amount of LPC for repair and restructuring (Smith et al. 2009). Once the cell membrane structure stabilizes after the initial month, the need for LPC decreases, leading to its downregulation. This reduction in LPC can also enhance the flexibility of the cell membrane, thereby maintaining its structural stability (Fuller and Rand 2001).

To achieve efficient metabolism in the new environment, cells adjust and optimize metabolic pathways to minimize unnecessary energy expenditure (Matthews et al. 2020). The generation and metabolism of LPC are energy-consuming processes. As cells gradually adapt to the new environment and regain stability, reducing LPC production conserves energy, redirecting resources to other vital physiological functions (Sousa et al. 2020). This adjustment helps restore metabolic balance as the cells acclimate to their new surroundings.

The upregulation of arachidonic acid metabolism and the downregulation of glycerophospholipid metabolism in transplanted coral cells resulted from their synergistic response to environmental stress and optimization of resource allocation. In the early and mid-stages of transplantation, the arachidonic acid metabolic pathway offered robust antioxidant and inflammation-regulating capabilities, aiding cells in coping with environmental changes and repairing damage (Safuan et al. 2021). Concurrently, the downregulation of glycerophospholipid metabolism reflected a resource-conservation strategy after cell membrane stabilization. This adjustment optimized the overall metabolic state by reducing the energy expenditure associated with phospholipid synthesis and degradation (Sousa et al. 2020).

These metabolic adjustments are critical for corals to achieve long-term stable survival in their new environment. Future research can delve deeper into the responses and interactions of these metabolic pathways under varying environmental stresses, aiming to uncover more profound mechanisms. Such insights will provide valuable theoretical support and practical guidance for coral conservation and restoration strategies.

4.3 Changes in Metabolic Patterns of Transplanted Corals 12 Months After Transplantation

Natural corals, due to their long-term adaptation to stable environments, have evolved efficient energy management and utilization mechanisms (Hein et al. 2020). This efficiency allows them to meet the energy demands of sexual maturity without significant metabolic adjustments (Randall et al. 2020). In contrast, transplanted corals must undergo metabolic changes during their initial reproductive phase to meet the high energy demands of sexual maturity. By 12 months post-transplantation, the transplanted G. fascicularis appeared to have fully adapted to their new environment and reached sexual maturity. During this period, corals experience significant metabolic changes to prioritize reproductive activities (Guest et al. 2014). This involves reallocating resources from other physiological functions, such as growth and repair, to reproductive processes (Edwards and Clark 1999). This resource reallocation necessitates adjustments in cellular metabolism to ensure reproductive activities receive prioritized energy supply (Chan et al. 2019).

Experimental data indicate that glycerophospholipid metabolism plays a crucial role in energy storage and allocation in transplanted corals (Boulotte et al. 2023). After 12 months post-transplantation, significant adjustments in glycerophospholipid metabolism were observed, optimizing metabolic pathways to reduce unnecessary energy consumption and allocate more energy to reproductive activities and growth (Wu et al. 2022). These metabolic adjustments enable transplanted corals to effectively utilize energy to support their sexual maturity and reproductive activities (Haydon et al. 2021).

Twelve months post-transplantation, no significant changes were observed in the arachidonic acid metabolic pathway, indicating that the transplanted corals reached a stable state and no longer required additional energy investment in this pathway. The performance of the transplanted corals in the arachidonic acid metabolic pathway was consistent with that of natural corals at this stage. The study results showed that as corals gradually stabilized and reached sexual maturity, the demand for LPC decreased, consistent with the optimization of the metabolic pathways they are involved in, ensuring efficient energy utilization and normal cellular function (Sun et al. 2023).

Additionally, the oxidative phosphorylation pathway is significantly upregulated in transplanted corals, primarily to meet the high energy demands of sexual maturity and reproductive activities (Yang et al. 2024). During sexual maturity, corals require a substantial amount of ATP to support gamete formation, release, and fertilization, all of which are energy-intensive processes (Briggs et al. 2024). Experimental results indicated that in corals 12 months post-transplantation, the activity of the oxidative phosphorylation pathway was enhanced, leading to a significant increase in ATP production. This increased activity supported the division and development of reproductive cells, antioxidant defense, signal transduction, and hormone regulation, all of which require additional energy (Zhang et al. 2021).

The upregulation of the oxidative phosphorylation pathway not only boosts ATP production but also enhances the expression of antioxidant enzymes, helping to neutralize reactive oxygen species (ROS) generated during reproduction, thereby protecting the health of reproductive cells (Braun 2020). Key metabolites in the oxidative phosphorylation pathway, such as riboflavin and ubiquinone-1, are significantly upregulated in transplanted corals. Riboflavin, a precursor to flavin mononucleotide and flavin adenine dinucleotide, serves as a coenzyme in the electron transport chain (Udhayabanu et al. 2017). Ubiquinone-1, a crucial electron carrier, enhances the oxidative phosphorylation process, thereby increasing ATP production to meet high energy demands (Tang et al. 2022). Both riboflavin and ubiquinone-1 possess antioxidant properties, which help enhance antioxidant defense mechanisms, reduce oxidative stress damage to cells, and protect cell health (Pobłocka-Olech et al. 2019; Moller et al. 1996). By adapting their metabolism, transplanted corals can sustain optimal physiological functions, thereby ensuring their health and survival in their new environment.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Ethics approval

This study is original research. The Research Ethics Committee has confirmed that no ethical approval is required.

Funding

This work were financially supported by Major Science and Technology plan of Hainan Province (ZDYF2023SHFZ173), the National Natural Science Foundation of China (42161144006 or 3511/21 and 42076108), the Innovative Talent Foundation of Hainan Province (KJRC2023C39).

Author contributions

He Zhao conceived the ideas and designed methodology; Hongmin Wang, Jingzhao Ke and Junling Zhang collected the data; Yushan Li, Xiangbo Liu and Wentao Zhu analysed the data; Aimin Wang and Xiubao Li led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Acknowledgments

The authors were grateful for constructive suggestions and technical support from the instructors and all the laboratory members.

Data availability

Data will be made available on request.

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Analyzing Adaptation Mechanisms in Artificial Transplantation of Galaxea fascicularis

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Abstract

Figures

1. Introduction

2. Materials and methods

2.1 Experimental Site and Sample Collection

2.2 Measurement of Coral Physiological Indicators

2.3 Metabolome Analysis

2.3.1 Metabolite Extraction

2.3.2 Quality Control (QC) Sample

2.3.3 UHPLC-MS/MS Analysis

2.3.4 MS Conditions:

2.3.5 Data Preprocessing and Annotation

2.3.6 Differential Metabolite Analysis

2.4 Water Quality Sample Collection

2.5 Data Analysis

3. Results

3.1 Water Quality Monitoring

3.2 Survival Rate and Physiological Indicators of Transplanted Corals

3.2 Comparative Analysis of Samples

3.3 KEGG Analysis

3.4 Analysis of Key Metabolic Pathways and Metabolite Content

4. Discussion

4.1 Survival Rate and Physiological Changes of Transplanted Corals

4.3 Changes in Metabolic Patterns of Transplanted Corals 12 Months After Transplantation

Declarations

Conflict of Interest

Ethics approval

Funding

Author contributions

Acknowledgments

Data availability

References

Supplementary Files

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