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Coral microbiome in estuary coral community of Pearl River Estuary: insights into variation in coral holobiont adaptability to low-salinity conditions

BMC Microbiology volume 25, Article number: 278 (2025) Cite this article

Abstract

Background

Low salinity is a crucial environmental stressor that affects estuarine coral ecosystems considerably. However, few studies have focused on the effects of low-salinity conditions on coral-associated microorganisms and the adaptability of coral holobionts.

Methods

We explored the community structure of coral symbiotic Symbiodiniaceae and associated bacteria in low-salinity conditions using samples of six coral species from the Pearl River Estuary and analyzed the adaptability of coral holobionts in estuaries.

Results

The symbiotic Symbiodiniaceae of all six studied coral species were dominated by Cladocopium, but, the Symbiodiniaceae subclades differed among these coral species. Some coral species (e.g., Acropora solitaryensis) had a high diversity of symbiotic Symbiodiniaceae but low Symbiodiniaceae density, with different adaptability to low-salinity stress in the Pearl River Estuary. Other coral species (e.g., Plesiastrea versipora) potentially increased their resistance by associating with specific Symbiodiniaceae subclades and with high Symbiodiniaceae density under low-salinity stress. The microbiome associated with the coral species were dominated by Proteobacteria, Chloroflexi, and Bacteroidetes; however, its diversity and composition varied among coral species. Some coral species (e.g., Acropora solitaryensis) had a high diversity of associated bacteria, with different adaptability owing to low-salinity stress. Other coral species (e.g., Plesiastrea versipora) potentially increased their resistance by having minority bacterial dominance under low-salinity stress.

Conclusions

High Symbiodiniaceae density and high bacterial diversity may be conducive to increase the tolerance of coral holobiont to low-salinity environments. Different coral species have distinct ways of adapting to low-salinity stress, and this difference is mainly through the dynamic regulation of the coral microbiome by corals.

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Introduction

Coral reefs, known as the “rainforests of the ocean,” are distributed in 110 countries and regions worldwide, accounting for approximately 0.17–0.5% of the global ocean and providing habitat for approximately 30% of marine organisms [1, 2]. The association between coral hosts and their microbiome is the basis for coral growth and reef development [3]. Coral holobionts include cnidarian polyps, bacteria, Symbiodiniaceae, archaea, fungi, and other microorganisms [4, 5]. Symbiodiniaceae are critical microorganisms in coral holobionts that use light energy for photosynthesis and provide fixed organic carbon to the coral host [6]. Symbiodiniaceae can utilize the metabolic waste produced by the coral host to replenish its nitrogen, phosphorus, and other vital nutrients [7]. Community-associated bacterial communities play key roles in coral holobionts, including nitrogen [8, 9], carbon [10], sulfur [11, 12], phosphorus fixation [13], intrametallic homeostasis [13], tissue repair [13], and antibiotic production [14]. Many coral-associated bacteria also protect corals from invasion by pathogens and other exogenous bacteria by secreting antibiotics [14, 15].

Corals are generally considered stenohaline, with limited ability to regulate osmotic pressure and adapt to or survive salinity changes [16]. Salinity is a critical environmental factor affecting their growth and distribution, and the suitable salinity range for growth is generally 32–40‰ [17]. Changes in salinity due to climate change may affect the physiology and metabolism of corals [18,19,20]. The corals have poor ability to regulate cellular osmotic pressure [21]. A short-term decline in salinity leads to significant changes in cellular respiration and photosynthesis in the coral symbiont Symbiodiniaceae [22]. Freshwater runoff is a major cause of coral mortality in estuarine coral reefs, particularly in those close to major river systems [22].

Environmental changes caused by global warming and destructive anthropogenic activity exacerbate damage to coral reef ecosystems and predispose coral holobionts to dysbiosis [23, 24], leading to high susceptibility to infections by opportunistic pathogens and coral mortality. Estuarine ecosystems are characterized by complex and variable environments, high biodiversity and productivity, and a high degree of human disturbance [25]. Global climate change has led to an unusual increase in extreme rainfall events in multiple regions [26,27,28], resulting in marine organisms frequently experiencing low-salinity stress in estuarine regions. Low salinity is one of the causes of coral bleaching. Many studies have explored the effects of low salinity on the physiological performance of the early stages of coral; for example, low salinity decreases coral larval recruitment and growth rates [29,30,31]. Low salinity may affect the physiological and biochemical processes, cellular changes, microbiome alterations, as well as the reproductive and survival capabilities of corals [32,33,34]. Low salinity stress can disrupt the symbiotic relationship within the coral holobiont, influencing the adaptability and stability of the coral holobiont [22]. In conclusion, Low-salinity stress can severely impact the growth, reproduction, photosynthesis, and respiration of corals, impair the normal functions of cells, and pose a serious threat to the health of corals [22, 35].

The sea section of the Pearl River Estuary in Guangdong represents the estuary of the Pearl River, the second largest river in China in annual runoff. Facing the South China Sea, the Pearl River Estuary is a typhoon-prone area and is susceptible to storm surges and flooding outbreaks, resulting in a large influx of freshwater into the estuary [36]. Corals in the Pearl River Estuary are affected by the year-round influx of freshwater. In the summer of 2022, record-breaking pre-flood rainfall in South China was lasted from May to June, resulting in a severe coral bleaching event in the coral communities of the Wanshan Islands in the Pearl River Estuary [37]. However, the effects of low-salinity stress on coral holobionts in the Wanshan Islands, and corals’ adaptability to low-salinity environments, are not well studied.

In this study, we aimed to answer two fundamental questions: are there differences in coral microorganisms in the coral communities of the Pearl River Estuary, and how well are the coral holobionts adapted to low salinity. We tested two hypotheses: (1) the compositions of coral microorganisms in the coral communities of the Pearl River Estuary vary in low-salinity conditions when compared with high salinity conditions, and (2) the physiological parameters of corals influence coral adaptability to low-salinity. To answer the two questions, we collected local water quality parameters and the coral symbiotic Symbiodiniaceae density, chlorophyll a (Chl a) content, and microbial diversity throughout the Pearl River Estuary. The findings of this study enhance the understanding of changes in estuarine coral reef communities and facilitate the conservation of estuarine corals and further research.

Experimental procedures

Study area and coral sample collection

The study area was located in the Wanshan Islands, Pearl River Estuary, China (Fig. 1). The Pearl River is the largest river in southern China and comprises Lingdingyang, Jidianmen, Mudianmen, and Huangmaohai. A large amount of freshwater from the Pearl River flows into the South China Sea, resulting in the salinity of seawater in the Pearl River Estuary being lower than the average salinity of seawater. Furthermore, rainstorms decrease seawater salinity in the Pearl River Estuary. In this study, after the rainstorm, two islands, Pingzhou and Miaowan, from the Pearl River Estuary were used for coral sample collection (Fig. 1). Water parameters, including the seawater surface temperature (SST; °C), surface water dissolved oxygen content (DO; mg/L), and salinity (Sal), were measured around the two islands.

Fig. 1
figure 1

Sampling site information. Coral samples and local water environmental parameters were collected in two islands of Pingzhou and Miaowan, from the Wanshan Islands, Pearl River Estuary, China

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In the Wanshan Islands, the dominant coral genera are, for example, Plesiastrea, Platygyra, Porites, Montipora, and Acropora [38]. In this study, 36 samples of six representative coral species, Platygyra daedalea, Plesiastrea versipora, Acropora solitaryensis, Montipora peltiformis, Echinophyllia aspera, and Galaxea fascicularis, were collected from around the two islands at water depths of 3–6 m. Among these samples, there are six samples for each coral species. The coral samples were obtained by scuba divers using hammers and chisels. The coral samples were cleaned using artificial sterile seawater (salinity: 35‰) to ensure they were not disturbed by free-living Symbiodiniaceae and fungi. A portion of the coral samples were 20–50 cm−2 in size, and Symbiodiniaceae density and chlorophyll a (Chl a) content were determined. The remaining coral samples were cut and placed in 5 mL freezing tubes, immediately snap-frozen, and stored in liquid nitrogen for subsequent experiments. The data related to corals in normal salinity were extracted from existing studies and reanalyzed [39,40,41,42,43,44,45,46]. Relevant data comprised Symbiodiniaceae density, Chl a content, symbiotic Symbiodiniaceae and coral-associated bacteria composition, and diversity of coral-associated bacteria. The data from under normal salinity were compared with those from low-salinity conditions, and their differences were observed.

Coral symbiotic Symbiodiniaceae

Measurement of coral symbiotic Symbiodiniaceae density and Chl a content

Coral tissue was removed using a Waterpik™ (3–5 kgf cm−2) containing 0.22 μm filtered seawater, and the volume of the initial slurry was measured in a graduated cylinder. The slurry was homogenized and re-sampled into four 3 mL aliquots. The slurry samples were centrifuged for 5 min (6,500 r·min−1). After discarding the supernatant, the Symbiodiniaceae at the bottom were preserved in 1 mL 5% formaldehyde at 6 °C for 2–4 h before proceeding to the next step of the analysis. Repeated counts of Symbiodiniaceae densities were performed using hemocytometry (n = 8–12). The coral surface area was determined based on the correlation between the weight of the aluminum foil and the surface area [47, 48]. In detail, the aluminum foil was pressed to cover the surface of the coral skeleton, and the foil from the covered area was cut and weighted. A 10 × 10 cm piece of aluminum foil was used to confirm the weight of the foil per square centimeter. The surface area of the coral skeleton was calculated using the weight of the foil covering the surface of the coral skeleton and the weight of the foil per square centimeter. Next, 2 mL of the algal solutions were collected thrice from the same sample bottle in 2 mL centrifuge tubes and centrifuged for 5 min (4,000 r·min−1). The supernatant was slowly removed, 1.5 mL acetone solution was added to the precipitate, and these samples were stored at 4 ℃ for 24 h. The extracted solutions were centrifuged for 5 min (4,000 r·min−1), and 200 μL of the supernatant was collected to determine the absorbance by using a spectrophotometer at wavelengths of 750, 664, 647, and 663 nm. The Mann–Whitney U test was used to analyze the significance of differences between groups (p < 0.05).

Total DNA extraction, Polymerase Chain Reaction (PCR) amplification, and Illumina MiSeq sequencing of coral symbiotic Symbiodiniaceae

The total DNA of coral holobionts was extracted as follows: ~ 50 mg of coral tissue and mucus was sampled, and genomic DNA was extracted using the DNeasy® Plant Kit per the manufacturer’s instructions. The extracted DNA samples were used as PCR templates after the examination of quality and purity. The quality and concentration of DNA were determined using 1.0% agarose gel electrophoresis and a NanoDrop2000 spectrophotometer (Thermo Scientific, United States) and stored at –80 ℃ for further use. PCR amplification of the Symbiodiniaceae ITS2 region of rDNA was performed using the primers F:5′-GAATTGCAGAACTCCGTG-3′ and R:5′-GGGATCCATATATGCTTAAGTTCAGCGGGGT-3′, with a six-nucleotide barcode unique to each sample [49, 50], and a 50 μL reaction volume PCR amplification was performed. The reaction volume contained ~ 50 ng DNA, 25 μL 2 × Taq Platinum Polymerase Chain Reaction Master Mix (Tiangen, China), 200 nM of each primer, and ddH2O added to achieve the final volume. The reaction was conducted for 5 min at 94 °C, 35 cycles of 30 s at 94 °C, 30 s at 51 °C, and 30 s at 72 °C, with a final extension for 5 min at 72 °C, using an ABI GeneAmp® 9700 thermal cycler [51]. Triplicate PCR products were collected from each sample, purified, and quantified using the AxyPrep DNA Gel Extraction Kit and QuantiFluor™ ST Fluorescence Quantification System for sizes between 301 and 340 bp. Purified amplicons were pooled in equimolar amounts and subjected to paired-end sequencing on an Illumina MiSeq platform according to standard protocols (2 × 300).

Analysis of α-diversity and community composition of coral symbiotic Symbiodiniaceae

Strict quality control and sequence filtering were performed to ensure the accuracy of the results. After short and low-quality sequences were removed by the sequencing company, full-length ITS2 rDNA fragments were obtained by applying the paired-end-sequence amalgamation (PEAR) tool to merge overlapping PE reads to generate ITS2 sequences [52]. After identifying a unique sequence, ITS2 tags were demultiplexed into all samples using the QIIME 2 platform [53]. BLASTn was used to compare all ASV sequences with the ITS2 database [54, 55]. The resulting symbiont ITS2 Symbiodiniaceae subclade counts were combined for downstream statistical analyses. The symbiotic Symbiodiniaceae H′ diversity index was calculated using the R software environment (version 4.2.3) and Bray–Curtis to assess the α-diversity in the symbiotic Symbiodiniaceae composition among coral species. Kruskal–Wallis analysis was performed on the α-diversity data based on different corals. A phylogenetic tree of the Symbiodiniaceae was constructed in MEGA 6 by using the maximum likelihood method (based on the Kimura 2-parameter model) [44, 56]. Raw reads were deposited into the NCBI Sequence Read Archive database (Accession Number: PRJNA1086834).

Coral-associated bacteria

Total DNA extraction, PCR amplification, and Illumina MiSeq sequencing of coral-associated bacteria

Approximately 50 mg of coral tissue and mucus was cut with scissors, and the total genomic DNA was extracted from the coral samples by using the TIANamp Marine Animal DNA Kit per the manufacturer’s instructions. The quality and concentration of DNA were determined using 1.0% agarose gel electrophoresis and a NanoDrop2000 spectrophotometer (Thermo Scientific, United States) and stored at –80 ℃ for further use. The total genomic DNA that fulfilled the conditions 1.8 < 260/280 < 2.0 and 260/230 > 2.0 was used as a template. Upstream primers carrying Barcode sequences 338F (5'-ACTCCTACGGGGAGGCAGCAG-3') and 806R (5'-GGACTACHVGGGTWTCTAAT-3') were used with the ABI GeneAmp® 9700 Thermal Cycler for the PCR amplification of the V3–V4 region of the bacterial 16S rRNA gene [48, 57]. An ABI GeneAmp 9700 thermal cycler (Thermo Fisher Scientific, Waltham, MA, United States) was used as a PCR reaction system, and the reactions were conducted under the following conditions: 3 min at 95°C, followed by 35 cycles of 95°C for 30 s, 55°C for 30 s, 72°C for 45 s, and a final extension at 72°C for 10 min. PCRs were run in triplicate per sample, which were conducted using a 20 μL reaction volume of TransGen AP221-02 (TransGen Biotech, Beijing, China) containing: 4 μL 5 × FastPfu Buffer (TransGen Biotech, Beijing, China), 2 μL 2.5 mM dNTPs, 0.8 μL (5 μm) forward primer, 0.8 μL (5 μm) reverse primer, 0.4 μL FastPfu DNA Polymerase (TransGen Biotech, Beijing, China), 0.2 μL BSA and 10 ng template DNA; the final volume was adjusted to 20 μL using ddH2O [55]. Next, 2 μL amplified product was collected, and product integrity was determined using 2% agarose gel electrophoresis at a voltage of 115 V for 45 min to confirm whether the fragment size was between 420 and 460 bp. PCR products were purified using PCR Clean-up Kit according to the manufacturer’s instructions (Yuhua, China), and Qubit 4.0 (Thermo Fisher Scientific, USA) was used to detect and quantify the recovered products. The purified PCR products were constructed using NEXTFLEX ® Rapid DNA-SeqKit: (1) split-link (2) Use magnetic bead screening to remove split-self-connected segments; (3) Enrichment of library templates by PCR amplification; (4) The PCR products were recovered by magnetic beads to obtain the final library. Sequencing was performed using the umimaNextseq2000 platform (Majorbio Biopharm Technology Company, Shanghai, China). Raw reads were deposited into the NCBI Sequence Read Archive database (Accession Number: PRJNA1086806).

Analysis of α-diversity and community composition of associated bacteria

Paired reads of the bacterial 16S rRNA gene output from the Illumina MiSeq platform were merged with overlapping PE reads by using PEAR software to obtain the complete 16S rRNA gene V3–V4 region sequence, which allowed for a maximum mismatch ratio of 0.2. The complete 16S rRNA gene V3–V4 region was homogenized to remove average quality scores of < 20 and bases of < 50 bp. Sequence orientation was based on primer sequences with valid sequences from barcode-identified samples. Non-repetitive sequences were extracted using Uparse. Single sequences and chimeras without repeats were removed, and based on the valid ASV data, they were processed and denoised. Next, species were classified to obtain the ASVs of bacterial samples for the assessment and statistical analysis of bacterial diversity and community composition. The SILVA v138 database was used for the identification of bacterial species. Rarefaction curves construction as well as alpha diversity indices were calculated on rarified data set (30,000 sequences for bacteria) using the Mothur (v1.30.2). Alpha diversity indices were compared with Kruskal Wallis test using the stats package in R (v3.3.1). The bacterial community composition was visualized by NMDS based on Bray–Curtis distance, using the Vegan package in R software (version 4.2.3). PERMANOVA was conducted to test for statistically significant differences in community composition among groups [58].

Results

Water parameters of Wanshan Islands, Pearl River Estuary

The water parameters of the Wanshan Islands in the Pearl River Estuary showed that in July 2022, the SST ranged from 29.44 ± 0.07 °C to 29.72 ± 0.08 °C, DO ranged from 6.65 ± 1.46 to 7.84 ± 0.56 mg/L, and salinity ranged from 23.26 ± 0.05‰ to 24.83 ± 1.03‰. Owing to heavy rainfall in the upper reaches of the Pearl River over several days, a large amount of freshwater was imported into the Pearl River Estuary, resulting in low-salinity conditions. In this study, the average salinity of the sampling sites was 24.4 ± 1.1‰, which is much lower than the normal salinity level (30.61–32.39‰) in the Pearl River Estuary [59], indicating that corals are subjected to low-salinity conditions in the Wanshan Islands.

Coral symbiotic Symbiodiniaceae in Wanshan Islands, Pearl River Estuary

Density and Chl a content of coral symbiotic Symbiodiniaceae

The Symbiodiniaceae density significantly differed among the six coral species (Fig. 2A, p < 0.05, Table S1). The symbiotic Symbiodiniaceae density assessment results showed that P. daedalea had the highest Symbiodiniaceae density (6.91 ± 2.07 × 106 cells/cm2), and E. aspera had the lowest density (3.31 ± 0.88 × 106 cells/cm2). Thus, the densities of other Symbiodiniaceae coral species were between those of P. daedalea and E. aspera.

Fig. 2
figure 2

Symbiodiniaceae density (a) and Chl a content (b) of six coral species from the Wanshan Islands, Pearl River Estuary. ‘a’, ‘b’ and ‘c’ represent the differences between different corals in Symbiodiniaceae density and Chl a conten, respectively (Mann–Whitney U test, P < 0.05)

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Moreover, there was a significant difference in Chl a content among these coral species (p < 0.05). G. fascicularis exhibited the highest Chl a content (14.88 ± 2.19 μg/cm2), which was much higher than those of the other coral species (Fig. 2B). The lowest Chl a content was 4.55 ± 1.56 μg/cm2 for A. solitaryensis, M. peltiformis, P. versipora, P. daedalea, and E. aspera. The Chl a content of E. aspera was between that of A. solitaryensis and G. fascicularis.

Diversity of coral symbiotic Symbiodiniaceae

In this study, 1,535,930 Symbiodiniaceae ITS2 reads were obtained in low-salinity conditions to fulfill the analysis criteria after rigorous screening and quality control. Of the Symbiodiniaceae ASVs, 1,070 valid ASVs were obtained for diversity and community analyses.

The Ace, Chao, Shannon, and Simpson indices for the symbiotic coral Symbiodiniaceae are shown in Fig. 3 and Table S2. The symbiotic Symbiodiniaceae of E. aspera had the highest Shannon index (2.09 ± 0.05), and that of P. daedalea was the lowest (1.27 ± 0.22). Overall, significant differences were observed in the diversity indices among the six coral species (p < 0.05).

Fig. 3
figure 3

Diversity indices of coral symbiotic Symbiodiniaceae of six coral species from the Wanshan Islands, Pearl River Estuary. The statistical differences were calculated by the Kruskal–Wallis H Test followed by pairwise testing using the Mann–Whitney U test (*: 0.01 < p < 0.05; **: 0.001 < p < 0.05; ***: p < 0.001)

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Composition of coral symbiotic Symbiodiniaceae

As shown in the composition diagram (Fig. 4), Cladocopium was the dominant Symbiodiniaceae among the six coral species (relative abundance > 97%, Table S3). Among them, A. solitaryensis, P. daedalea, and G. fascicularis had similar compositions to Symbiodiniaceae, and the abundance of the dominant Cladocopium C1 ranged from 80.4% to 84.5%. The compositions of P. versipora, E. aspera, and M. peltiformis differed from those of A. solitaryensis, P. daedalea, and G. fascicularis. P. versipora had the highest percentage of Cladocopium C1, and the abundance of Cladocopium C1 was lower than that of A. solitaryensis, P. daedalea, and G. fascicularis. Cladocopium Cspc, Cladocopium C44, and Cladocopium C1p were highly abundant (> 5%). The symbiotic Symbiodiniaceae of E. aspera had the highest abundance of Cladocopium C18 (49.7%), followed by Cladocopium C1 (26.4%) and Cladocopium C1p, Cladocopium C16 (> 5%). Cladocopium C3d was dominant in M. peltiformis (79.8%). Cladocopium C21.11 and Cladocopium Cspc also showed a high abundance (> 5%).

Fig. 4
figure 4

Composition of symbiotic Symbiodiniaceae in six coral species from the Wanshan Islands, Pearl River Estuary. The Symbiodiniaceae subclades such as C1, C44, and Cspc,were be classified as the Cladocopium

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A phylogenetic tree of the dominant Symbiodiniaceae subclades in low-salinity conditions was constructed (Fig. 5). Three major groups were suggested for the development of the symbiotic Symbiodiniaceae in six coral species from the Pearl River Estuary. Cladocopium C16, Cladocopium C21.11, and Cladocopium Cspc had close phylogenetic relationships, and the phylogenetic relationships of Cladocopium C65a, Cladocopium C1p, and Cladocopium C72 were closer than those of Cladocopium C44, Cladocopium C1ca, and Cladocopium C1. The symbiotic Symbiodiniaceae composition of M. peltiformis, including Cladocopium C3.14, Cladocopium C21.11, Cladocopium Cspc, and Cladocopium C3d, showed closer phylogenetic relationships. The symbiotic Symbiodiniaceae composition of A. solitaryensis, including Cladocopium Cspc, Cladocopium C72, Cladocopium C1p, Cladocopium C1p.C45, Cladocopium C1ca, Cladocopium C1, and Cladocopium C78a, showed closer phylogenetic relationships.

Fig. 5
figure 5

Phylogenetic tree of coral symbiotic Symbiodiniaceae of six coral species from the Wanshan Islands, Pearl River Estuary

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Diversity and composition of coral-associated bacteria in Wanshan Islands, Pearl River Estuary

Diversity of coral-associated bacteria

In this study, 1,425,904 reads were obtained from the six coral species after rigorous screening and quality control (Table S4). After excluding archaea, chloroplasts, and mitochondrial sequences, in total, 16,112 valid bacterial ASVs were identified. Per these bacterial ASVs, the Shannon index showed that A. solitaryensis had a relatively low level of associated bacterial diversity and that P. versipora and G. fascicularis had higher levels of associated bacterial diversity (Fig. 6). The Shannon index also showed a significant difference in bacterial community diversity between P. versipora and A. solitaryensis (p < 0.001). The bacterial community diversity of P. versipora and M. peltiformis also significantly differed (p < 0.05). The Simpson diversity index was the opposite of that of the Shannon diversity index. The Ace index statistics showed that P. versipora and G. fascicularis had the highest levels of total ASVs (Fig. 6), and A. solitaryensis had the lowest levels of total bacterial species, which differed from those of P. versipora (p < 0.05). In normal salinity, the Sobs index and Shannon index of M. peltiformis and Platygyra were lower than in low-salt conditions. Furthermore, at normal salinity, the Simpson index of M. peltiformis and Platygyra was higher than that of low-salinity conditions. These results indicated increased bacterial diversity in corals in low-salinity conditions.

Fig. 6
figure 6

Diversity indices of coral-associated bacteria of six coral species from the Wanshan Islands, Pearl River Estuary. The statistical differences were calculated by the Kruskal–Wallis H Test followed by pairwise testing using the Mann–Whitney U test (*: 0.01 < p < 0.05; **: 0.001 < p < 0.05; ***: p < 0.001)

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According to the NMDS analysis (Fig. 7), the community composition of the bacteria associated with the six coral species suggested that E. aspera differed significantly (p < 0.05) from the other coral species in associated bacterial community composition. The NMDS analysis also suggested that the associated bacteria community of P. versipora differed significantly from those of the other coral species (p < 0.05). A. solitaryensis, M. peltiformis, P. daedalea, and G. fascicularis had similar bacterial communities.

Fig. 7
figure 7

NMDS analysis of associated bacteria of six coral species from the Wanshan Islands, Pearl River Estuary

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Composition of coral-associated bacteria

At the phylum level, the bacteria associated with A. solitaryensis and P. daedalea were dominated by Proteobacteria (Fig. 8, Table S5). For P. versipora and E. aspera, Chloroflexi were the dominant bacteria; other bacteria, such as Proteobacteria, Bacteroidota, and Actinomycetota, also had relatively high abundances. In the cases of G. fascicularis and M. peltiformis, the dominant bacteria were Proteobacteria, Bacteroidota, and Firmicutes. The bacterial composition of corals in normal salinity differs from that in low-salinity conditions. The bacteria associated with M. peltiformis were dominated by Cyanobacteria, with relative abundances of 92.15% at normal salinity. In normal conditions, the relative abundances of γ-proteobacteria (20%), α-proteobacteria (12%), and Cyanobacteria (39%) in the associated bacteria community of G. fascicularis were relatively high. The dominant bacteria in both low-salt conditions is Proteobacteria, and the dominant bacteria in normal salinity is Cyanobacteria. For Platygyra, Proteobacteria was the dominant phylum, with 71.87% in normal salinity, followed by Firmicutes. This suggests that different corals are affected by low salinity to different degrees and that low-salinity conditions affect the composition of some coral symbiotic bacteria.

Fig. 8
figure 8

Composition of coral-associated bacteria at the phylum level in the Wanshan Islands, Pearl River Estuary

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At the genus level, we selected the top 30 bacteria in terms of total abundance for plotting. Among these six coral species had high abundances of Vibrio (relative abundance: 4.2 ± 4.8%) and Rhodobacteraceae (relative abundance: 3.9 ± 2.6%, Fig. 9, Table S6). G. fascicularis had high abundances of Pseudomonas (relative abundance: 4.6 ± 2.4%), Photobacterium (relative abundance: 4.5 ± 2.4%), and Pseudoalteromonas (relative abundance: 4.5 ± 2.4%). Ruegeria was observed in P. daedalea and M. peltiformis, with relative abundances of 2.9 ± 1.9% and 1.0 ± 1.2%, respectively. At the genus level, in normal salinity, the bacteria associated with M. peltiformis were dominated by Synechococcus CC9902 (89.16%). The dominant genus in Platygyra was Endozoicomonas (52.30%). The results demonstrated that the dominant genus composition of corals differed significantly between normal salinity and low-salinity conditions (Mann–Whitney U test, p < 0.05).

Fig. 9
figure 9

Associated bacterial composition at the genus level of six coral species in the Wanshan Islands, Pearl River Estuary

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Discussion

Adaptation of coral-Symbiodiniaceae holobionts to the low-salinity in the Pearl River Estuary

Owing to the influences of short-term rainstorms and massive freshwater input, low-salinity conditions endure in the Pearl River Estuary. Low-salinity conditions have significant negative impacts on coral-Symbiodiniaceae holobionts, and coral symbiotic Symbiodiniaceae density decreases in low salinity [22, 60]. The symbiotic Symbiodiniaceae density reflects differences in the adaptability of coral species in low-salinity conditions. For example, G. fascicularis can normally survive more than 60 d when exposed to 20‰ salinity [61]; however, the growth rate of Platygyra acuta slows when the salinity is < 26‰ and stops at salinities < 22‰ [30]. In low-salinity conditions, Liu et al. [60] found that the Symbiodiniaceae density and Chl a content of Porites lutea decreased significantly when the surrounding seawater salinity was < 30‰, and the Symbiodiniaceae density and Chl a content decreased dramatically when the salinity decreased from 30‰ to 20‰ until the corals bleached. Similarly, in this study, the density and Chl a content of coral symbiotic Symbiodiniaceae differed significantly in the low-salinity conditions of the estuary, with some corals showing high Symbiodiniaceae densities and Chl a content, such as G. fascicularis; other corals showed low Symbiodiniaceae densities, such as E. aspera. The Symbiodiniaceae density of P. versipora was 6.8 × 106 cells/cm2 [39], and that of M. peltiformis was 4 × 106 cells/cm2 at normal salinity [40]. Both corals exhibited a decrease in Symbiodiniaceae density in low-salinity conditions. The Chl a content of A. solitaryensis was 15.21 μg/cm2, and that of M. peltiformis was approximately 11 μg/cm2 at normal salinity [41, 42]. In this study, the Chl a content of A. solitaryensis was 2.43 μg/cm2, and that of M. peltiformis was 8.09 μg/cm2 in low-salinity conditions. Both corals showed decreases in Chl a content. These findings suggest that low-salinity conditions affect Symbiodiniaceae density and Chl a content, and differences in Symbiodiniaceae density and Chl a content could be responsible for the different adaptations of corals to low-salinity conditions.

Environmental factors drive various types of and different environmental influences in Symbiodiniaceae coral holobionts [62, 63]. Studies have found that the dominant symbiotic Symbiodiniaceae is closely related to the tolerance of coral-Symbiodiniaceae holobionts to environmental stress [64,65,66]. Symbiodiniaceae subclades confer different physiological characteristics and environmental tolerances to coral holobionts [65, 67, 68]. In this study, the dominant symbiotic Symbiodiniaceae subclades in all corals were Cladocopium C1, excluding M. peltiformis and E. aspera. Some corals with Cladocopium C1-dominant species had a lower percentage of Cladocopium C1 than corals in normal salinity conditions, for example, P. versipora with 75% in normal salinity and 41.5% in this experiment [43], and some coral Cladocopium C1 percentage gaps do not vary much, for example, G. fascicularis, with approximately 80% in normal and low-salinity conditions [43]. Cladocopium C1 is a subclade of Symbiodiniaceae with high photosynthetic efficiency [69]. Under the low-salinity stress, corals may establish a symbiotic relationship with highly photosynthetically efficient Symbiodiniaceae to maintain the functioning of the calcium carbonate secretion-storage system [70]. However, some of the dominant symbiotic Symbiodiniaceae subclades change from corals between the normal salinity and low-salinity conditions. In normal conditions, for example, the dominant symbiotic Symbiodiniaceae subclades of the M. peltiformis were Cladocopium C3d, followed by Cladocopium C2r [44]. In low-salinity conditions, the dominant symbiotic Symbiodiniaceae subclades were Cladocopium C3d, followed by Cladocopium Cspc. Notably, some corals were symbiotic with different symbiotic Symbiodiniaceae subclades when experienced low-salinity stress. For example, Cladocopium Cspc and C3d were detected from M. peltiformis in low salinity conditions, but Cladocopium C3d and C2r were detected in normal salinity conditions. Research has observed that M. peltiformis has high susceptibility to environmental influences [45]. The flexible changes in the composition of symbiotic Symbiodiniaceae subclades may be conducive M. peltiformis to survive and adapt to low-salinity stress.

Coral symbiotic Symbiodiniaceae types are typically determined by environmental selection and co-evolution [71]. The results of this study showed that among the six coral species, some of them differed significantly in their Symbiodiniaceae diversity and composition. Coral holobionts can regulate physiological and ecological characteristics (e.g., coral host stress, Symbiodiniaceae densities, Symbiodiniaceae subclades, and bacterial communities) to adapt to external environmental changes [72, 73]. The results suggest that different corals adapt to low salinity by regulating their symbiotic relationship with Symbiodiniaceae. Based on the phylogenetic tree of Symbiodiniaceae, two typical symbiotic Symbiodiniaceae species selected by corals survived in low-salinity conditions. For example, the Symbiodiniaceae subclades of M. peltiformis belong to similar branches of the phylogenetic tree, and those of A. solitaryensis are distributed throughout the phylogenetic tree. This suggests that symbiotic Symbiodiniaceae may be regulated by corals in low-salinity conditions. Some coral species establish symbiotic relationships with specific Symbiodiniaceae subclades (e.g., Cladocopium C1) to increase their photosynthetic rate, and other coral species establish symbiotic relationships with multiple Symbiodiniaceae subclades to enhance their Symbiodiniaceae diversity and tolerance to low-salinity conditions.

Adaptation of coral-bacterial holobionts to low-salinity Pearl River Estuary condition

Salinity is a key factor influencing the diversity and composition of bacterial communities in coastal corals [74, 75]. Microbiome dynamics are linked to coral environmental tolerance [76]. And a high diversity of the bacterial community may contribute to niche complementation and/or functional redundancy [23, 77]. In our study, six studied coral species suggested that the bacterial communities associated with each of them showed significant differences in diversity and composition. Specifically, relatively high bacterial diversity was detected in the P. versipora, while relatively low bacterial diversity in the A. solitaryensis.

Compared with normal salinity environment, bacterial composition of different corals widely changed in low-salinity environment [45, 46]. For example, M. peltiformis showed distinct changes in bacterial composition. At the phylum level, the bacteria associated with M. peltiformis were dominated by Cyanobacteria, with relative abundances of 92.15% in normal salinity environment. At the genus level, the bacteria associated with M. peltiformis were dominated by Synechococcus CC9902 (89.16%) [45]. However, in low-salinity conditions, the dominant ASVs were Proteobacteria at the phylum level. At the genus level, u_Rhodobacteraceae were the dominant bacteria. Synechococcus spp. is conducive coral holobiont to nitrogen fixation [78] and photosynthesis [79], indicating their potential roles in the hologenomic nutrient cycling of corals and the health state of coral hosts. Rhodobacteraceae may also enhance the resilience of corals by absorbing DMSP from Symbiodiniaceae and producing antibacterial compounds against pathogens [80]. Evidently, low salinity can affect changes in the bacterial composition of corals, which further impacts the health of coral holobionts [45]. In contrast, the bacterial composition of G. fascicularis was relatively in stable. Under normal-salinity conditions, the relative abundances of γ-Proteobacteria, α-Proteobacteria, and Cyanobacteria of G. fascicularis were 20%, 12%, and 39% respectively, remaining at a relatively high level [46]. Under low-salinity environment, Proteobacteria becomes were also the dominant bacteria, which is similar to the bacterial composition under normal conditions. This indicates a potential variation between the stability of the microbiome and the susceptibility to bleaching among coral species. The bacterial diversity might be important factors in coral adaptability to low-salinity conditions. Some coral species may survive better than others in low-salinity conditions by maintaining a high level of bacterial diversity. Coral microbiome with high diversity may have high physiological and ecological acclimatization to low-salinity conditions [81].

Community-associated bacterial communities have high flexibility and diverse functions and are closely related to the health of coral symbiotic functionaries. For example, Proteobacteria and Bacteroidetes have a high tolerance to salinity stress [82]. In this study, bacteria from Proteobacteria and Bacteroidetes tended to dominate the coral-associated communities, and their insensitivity to salinity allowed these bacteria to survive better than other bacteria in low-salinity conditions. Rhodobacteraceae were highly abundant in all six coral species, and their ability to grow through photosynthesis, metabolize CO2, and fix nitrogen plays an important role in the carbon and nitrogen cycles of marine ecosystems [83].

In this study, additional differences were observed in the relative abundances of bacterial phyla and genera, reflecting varying adaptability among coral species in low-salinity conditions. Coral-associated bacteria may be related to coral growth, nutrient metabolism, the immune system, antioxidant capacity, resilience, and tolerance [84, 85]. In our study, the coral microbial communities in low-salinity areas revealed that Pseudoalteromonas was extremely abundant in some corals, such as P. daedalea. Pseudoalteromonas has been shown to have significant antagonistic effects on various pathogens [86]. In this study, Pseudoalteromonas and Vibrio were detected in the composition of coral-associated bacteria. Pseudoalteromonas may be conducive to inhibit the growth and reproduction of Vibrio via antagonism, potentially decreasing the risk of disease in corals [87]. Furthermore, a high abundance of Ruegeria was found in P. daedalea and M. peltiformis. Ruegeria is a potential probiotic coral that produces antibiotics that can inhibit the growth of Vibrio [88]. High abundance of Vibrio in low-salinity conditions may interfere with the associated relationship between corals and bacteria [89, 90]; the antagonistic effect of Pseudoalteromonas and the antibiotics produced by Ruegeria could be conducive to inhibiting the growth of Vibrio, maintaining the stability of the relationship and the mutual cooperation between corals and bacteria. Under low-salinity stress, the increased abundance of specific bacterial taxa may contribute to the health and survival of corals [91, 92].

Conclusions

Different coral species have different adaptations to low-salinity stress by regulating the diversity and composition of Symbiodiniaceae and bacteria. Some coral species improved their adaptation to low-salinity stress in the Pearl River Estuary based on a high diversity of symbiotic Symbiodiniaceae and associated bacteria. In contrast, some other coral species may increase their resistance by associating with specific Symbiodiniaceae subclades, with high Symbiodiniaceae density, or minority bacterial dominance under low-salinity stress.

Data availability

The data used in this paper are available from supporting information (SI), and the raw sequences were deposited in the NCBI Sequence Read Archive (SRA) database (https://www.ncbi.nlm.nih.gov/, accession number: Symbiodiniaceae: PRJNA1086834; bacteria: PRJNA1086806).

References

  1. Bellwood DR, Hughes TP, Folke C, Nystrom M. Confronting the coral reef crisis. Nature. 2004;429:827–33. https://doiorg.publicaciones.saludcastillayleon.es/10.1038/nature02691.

    Article  PubMed  CAS  Google Scholar 

  2. Yu KF. Coral reefs in the South China Sea: Their response to and records on past environmental changes. Science China-Earth Science. 2015;55:1217–29. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s11430-012-4449-5.

    Article  CAS  Google Scholar 

  3. van Oppen MJH, Blackall LL. Coral microbiome dynamics, functions and design in a changing world. Nat Rev Microbiol. 2019;17:557–656. https://doiorg.publicaciones.saludcastillayleon.es/10.1038/s41579-019-0223-4.

    Article  PubMed  CAS  Google Scholar 

  4. Rohwer F, Seguritan V, Azam F, Knowlton N. Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser. 2002;243:1–10. https://doiorg.publicaciones.saludcastillayleon.es/10.3354/meps243001.

    Article  Google Scholar 

  5. Garrido AG, Machado LF, Zilberberg C, Leite DCD. Insights into ‘Symbiodiniaceae phycosphere’ in a coral holobiont. Symbiosis. 2021;83:25–39. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s13199-020-00735-3.

    Article  Google Scholar 

  6. Brodersen KE, Lichtenberg M, Ralph PJ, Kühl M, Wangpraseurt D. Radiative energy budget reveals high photosynthetic efficiency in symbiont-bearing corals. J R Soc Interface. 2014;11:20130997. https://doiorg.publicaciones.saludcastillayleon.es/10.1098/rsif.2013.0997.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Falkowski PG, Dubinsky Z, Muscatine L, Poter JW. Light and the Bioenergetics of a Symbiotic Coral. Bioscience. 1984;34:705–9. https://doiorg.publicaciones.saludcastillayleon.es/10.2307/1309663.

    Article  CAS  Google Scholar 

  8. Lema KA, Willis BL, Bourne DG. Corals Form Characteristic Associations with Symbiotic Nitrogen-Fixing Bacteria. Appl Environ Microbiol. 2012;78:3136–44. https://doiorg.publicaciones.saludcastillayleon.es/10.1128/AEM.07800-11.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG. Discovery of Symbiotic Nitrogen-Fixing Cyanobacteria in Corals. Science. 2004;305:997–1000. https://doiorg.publicaciones.saludcastillayleon.es/10.1126/science.1099128.

    Article  PubMed  CAS  Google Scholar 

  10. Kimes NE, Van Nostrand JD, Weil E, Zhou J, Morris PJ. Microbial functional structure of Montastraea faveolata, an important Caribbean reef-building coral, differs between healthy and yellow-band diseased colonies. Environ Microbiol. 2010;12:541–56. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/j.1462-2920.2009.02113.x.

    Article  PubMed  CAS  Google Scholar 

  11. Raina J-B, Tapiolas D, Willis BL, Bourne DG. Coral-Associated Bacteria and Their Role in the Biogeochemical Cycling of Sulfur. Appl Environ Microbiol. 2009;75:3492–501. https://doiorg.publicaciones.saludcastillayleon.es/10.1128/AEM.02567-08.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F. Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol. 2007;9:2707–19. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/j.1462-2920.2007.01383.x.

    Article  PubMed  CAS  Google Scholar 

  13. Zhang YY, Ling J, Yang QS, Wen CQ, Yan QY, Sun HY, Van Nostrand JD, Shi Z, Zhou JZ, Dong JD. The functional gene composition and metabolic potential of coral-associated microbial communities. Sci Rep. 2015;5:16191. https://doiorg.publicaciones.saludcastillayleon.es/10.1038/srep16191.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Ritchie KB. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser. 2006;322:1–14. https://doiorg.publicaciones.saludcastillayleon.es/10.3354/meps322001.

    Article  CAS  Google Scholar 

  15. Rypien KL, Ward JR, Azam F. Antagonistic interactions among coral-associated bacteria. Environ Microbiol. 2010;12:28–39. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/j.1462-2920.2009.02027.x.

    Article  PubMed  CAS  Google Scholar 

  16. Seveso D, Montano S, Strona G, Orlandi I, Galli P, Vai M. Exploring the effect of salinity changes on the levels of Hsp60 in the tropical coral Seriatopora caliendrum. Mar Environ Res. 2013;90:96–103. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.marenvres.2013.06.002.

    Article  PubMed  CAS  Google Scholar 

  17. Ding DS, Patel AK, Singhania RR, Chen CW, Dong CD. Effects of Temperature and Salinity on Growth, Metabolism and Digestive Enzymes Synthesis of Goniopora columna. Biology. 2022;11:436. https://doiorg.publicaciones.saludcastillayleon.es/10.3390/biology11030436.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Blaxter JHS. 1 Pattern and Variety in Development. Fish Physiology. 1998;11:1–58. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/S1546-5098(08)60198-3.

    Article  Google Scholar 

  19. Rombough PJ. The effects of temperature on embryonic and larval development. In: Wood CM, McDonald DG, editors. Global Warming: Implications for Freshwater and Marine Fish. Cambridge University Press: Society for Experimental Biology Seminar Series; 1997. p. 177–224.

    Chapter  Google Scholar 

  20. Hoegh-Guldberg O, Smith GJ. The effect of sudden changes in temperature, light and salinity on the population density and export of Symbiodiniaceae from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Dana. J Exp Mar Biol Ecol. 1989;129:279–303. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/0022-0981(89)90109-3.

    Article  Google Scholar 

  21. Mayfield AB, Gates RD. Osmoregulation in anthozoan-dinoflagellate symbiosis. Comparative biochemistry and physiology. Part A, Molecular & integrative physiology. 2007;147:1–10. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.cbpa.2006.12.042.

    Article  CAS  Google Scholar 

  22. Kuanui P, Chavanich S, Viyakarn V, Omori M, Lin C. Effects of temperature and salinity on survival rate of cultured corals and photosynthetic efficiency of zooxanthellae in coral tissues. Ocean Science Journal. 2015;50:263–8. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s12601-015-0023-3.

    Article  CAS  Google Scholar 

  23. Bourne DG, Morrow KM, Webster NS. Insights into the Coral Microbiome: Underpinning the Health and Resilience of Reef Ecosystems. Annu Rev Microbiol. 2016;70:317–40. https://doiorg.publicaciones.saludcastillayleon.es/10.1146/annurev-micro-102215-095440.

    Article  PubMed  CAS  Google Scholar 

  24. Thurber RV, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F, Dinsdale E, Kelly L, Rohwer F. Metagenomic analysis of stressed coral holobionts. Environ Microbiol. 2009;11:2148–63. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/j.1462-2920.2009.01935.x.

    Article  CAS  Google Scholar 

  25. Mei S, Yu K, Chen B. Salinity Influencing the Formation of Special Niches of Bacterioplankton in Pearl River Estuary, China (in Chinese). Acta Scientiarum Naturalium Universitatis Pekinensis. 2021;57:903–915. https://doiorg.publicaciones.saludcastillayleon.es/10.13209/j.0479-8023.2021.067

  26. Lee T, Chan K, Chan H, Kok M. Projections of extreme rainfall in Hong Kong in the 21st century. Acta Meteor Sin. 2011;25:691–709. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s13351-011-0601-y.

    Article  Google Scholar 

  27. IPCC. 2013. Climate change. The Physical Science Basis. In T. F. Stocker, D. Qin, G. K. Plattner, M. Tignor, S. K. Allen, J. Boschung, et al Contribution of Working Group I to the Fifth Assessment Report. Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (UK and New York, NY, USA.: Cambridge University Press). 2013. https://doiorg.publicaciones.saludcastillayleon.es/10.1101/gr.120618.111

  28. Knutson TR, Sirutis JJ, Zhao M, Tuleya RE, Bender M, Vecchi GA, Villarini G, Chavas D. Global projections of intense tropical cyclone activity for the late twenty-first century from dynamical downscaling of CMIP5/RCP4.5 scenarios. J Clim. 2015;28:7203–24. https://doiorg.publicaciones.saludcastillayleon.es/10.1175/JCLI-D-15-0129.1.

    Article  Google Scholar 

  29. Hoegh-Guldberg O. Climate change, coral bleaching and the future of the world’s coral reefs. Marine And Freshwater Research. 1999;50:839–66. https://doiorg.publicaciones.saludcastillayleon.es/10.1071/mf99078.

    Article  Google Scholar 

  30. Chui APY, Ang PO. Elevated temperature enhances normal early embryonic development in the coral Platygyra acuta under low salinity conditions. Coral Reefs. 2015;34:461–9. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00338-014-1247-x.

    Article  Google Scholar 

  31. Hedouin L, Pilon R, Puisay A. Hyposalinity stress compromises the fertilization of gametes more than the survival of coral larvae. Mar Environ Res. 2015;104:1–9. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.marenvres.2014.12.001.

    Article  PubMed  CAS  Google Scholar 

  32. Kregting LT, Gibbs MT. Salinity controls the upper depth limit of black corals in Doubtful Sound, New Zealand. NZ J Mar Freshwat Res. 2006;40:43–52. https://doiorg.publicaciones.saludcastillayleon.es/10.1080/00288330.2006.9517402.

    Article  CAS  Google Scholar 

  33. Scott A, Harrison PL, Brooks LO. Reduced salinity decreases the fertilization success and larval survival of two scleractinian coral species. Mar Environ Res. 2013;92:10–4. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.marenvres.2013.08.001.

    Article  PubMed  CAS  Google Scholar 

  34. Röthig T, Ochsenkühn MA, Roik A, van der Merwe R, Voolstra CR. Long-term salinity tolerance is accompanied by major restructuring of the coral bacterial microbiome. Mol Ecol. 2016;25:1308–23. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/mec.13567.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Moberg F, Nyström M, Kautsky N, Tedengren M, Jarayabhand P. Effects of reduced salinity on the rates of photosynthesis and respiration in the hermatypic corals Porites lutea and Pocillopora damicornis. Mar Ecol Prog Ser. 1997;157:53–9. https://doiorg.publicaciones.saludcastillayleon.es/10.3354/MEPS157053.

    Article  Google Scholar 

  36. Chen P, Zhang Z, Song Z, Zhang W, Ye R, Li Y. Simulation of storm surge and analysis of the factors around Lingdingyang Bay, Pearl River Estuary: Take typhoon Mangkhut as an example. Marine Sci Bullet. 2023;42:645–657. https://doiorg.publicaciones.saludcastillayleon.es/10.11840/j.issn.1001-6392.2023.06.004

  37. Liu B, Zhu C, Xu K, Ma S, Lu M, Han X, Hua L. Record-breaking pre-flood rainfall over South China in 2022: role of historic warming over the Northeast Pacific and Maritime Continent. Clim Dyn. 2023;61:3147–63. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00382-023-06734-6.

    Article  Google Scholar 

  38. Huang H, You F, Lian J, Zhang C, Yang J, Li X, Yuan T, Zhang Y, Zhou G. Status and conservation strategies of the scleractinian coral community in the Wanshan Islands at Pearl River Estuary. Marine Sci Bullet. 2012;31:189–197. https://doiorg.publicaciones.saludcastillayleon.es/10.11840/j.issn.1001-6392.2012.2.010

  39. Li S, Yu KF, Shi Q, Chen TR, Zhao MX, Zhao JX. Interspecific and spatial differences in the coral symbiotic Symbiodiniaceae density and its effect on coral reef bleaching in the northern part of the South China Sea. Chin Sci Bull. 2007;52:2655–62. https://doiorg.publicaciones.saludcastillayleon.es/10.1360/csb2007-52-22-2655.

    Article  Google Scholar 

  40. Ip JC, Zhang Y, Xie JY, Yeung YH, Qiu JW. Comparative transcriptomics of two coral holobionts collected during the 2017 El Niño heat wave reveal differential stress response mechanisms. Mar Pollut Bull. 2022;182:114017. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.marpolbul.2022.114017.

    Article  PubMed  CAS  Google Scholar 

  41. Li S, Yu KF, Chen TR, Shi Q, Chen TG. Seasonal patterns of densities of symbiotic zooxanthellae in scleractinian corals from Daya Bay, northern South China Sea, and relation to coral bleaching. J Trop Oceanogr. 2011;02:39–45. https://doiorg.publicaciones.saludcastillayleon.es/10.3969/j.issn.1009-5470.2011.02.006.

    Article  CAS  Google Scholar 

  42. Qin Z, Yu K, Wang Y, Xu L, Huang X, Chen B, Li Y, Wang W, Pan Z. Spatial and intergeneric variation in physiological indicators of corals in the South China Sea: Insights into their current state and their adaptability to environmental stress. J Geophys Res Oceans. 2019;124:3317–32. https://doiorg.publicaciones.saludcastillayleon.es/10.1029/2018JC014648.

    Article  Google Scholar 

  43. Chen B, Yu K, Qin Z, Liang J, Wang G, Huang X, Wu Q, Jiang L. Dispersal, genetic variation, and symbiont interaction network of heat-tolerant endosymbiont Durusdinium trenchii: Insights into the adaptive potential of coral to climate change. The Science of the total environment. 2020;723:138026. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.scitotenv.2020.138026.

    Article  PubMed  CAS  Google Scholar 

  44. Tong H, Cai L, Zhou G, Yuan T, Zhang W, Tian R, Huang H, Qian PY. Temperature shapes coral-algal symbiosis in the South China Sea. Sci Rep. 2017;7:40118. https://doiorg.publicaciones.saludcastillayleon.es/10.1038/srep40118.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Zou Y, Ip JC, Xie JY, Yeung YH, Wei L, Guo Z, Zhang Y, Qiu JW. Dynamic changes in bacterial communities in three species of corals during the 2017 bleaching event in subtropical Hong Kong waters. Mar Pollut Bull. 2024;199:116002. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.marpolbul.2023.116002.

    Article  PubMed  CAS  Google Scholar 

  46. Chen B, Yu K, Liao Z, Yu X, Qin Z, Liang J, Wang G, Wu Q, Jiang L. Microbiome community and complexity indicate environmental gradient acclimatisation and potential microbial interaction of endemic coral holobionts in the South China Sea. Sci Total Environ. 2021;765. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.scitotenv.2020.142690.

  47. Li S, Yu K, Shi Q, Chen TR, Zhao MX, Zhao JX. Interspecies and spatial diversity in the symbiotic zooxanthellae density in corals from northern South China Sea and its relationship to coral reef bleaching. Chin Sci Bull. 2008;53:295–303. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s11434-007-0514-4.

    Article  Google Scholar 

  48. Xu LJ, Yu KF, Li S, Liu GH, Tao SC, Shi Q, Chen TR, Zhang HL. Interseasonal and interspecies diversities of Symbiodinium density and effective photochemical efficiency in five dominant reef coral species from Luhuitou fringing reef, northern South China Sea. Coral Reefs. 2017;36:477–87. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00338-016-1532-y.

    Article  Google Scholar 

  49. Lajeunesse TC, Trench RK. Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull. 2000;199:126–34. https://doiorg.publicaciones.saludcastillayleon.es/10.2307/1542872.

    Article  PubMed  CAS  Google Scholar 

  50. Lajeunesse TC, Loh WKW, van Woesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK. Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol Oceanogr. 2003;48:2046–54. https://doiorg.publicaciones.saludcastillayleon.es/10.4319/lo.2003.48.5.2046.

    Article  Google Scholar 

  51. Sun Z, Li GP, Wang CW, Jing YH, Zhu YP, Zhang SM, Liu Y. Community dynamics of prokaryotic and eukaryotic microbes in an estuary reservoir. Sci Rep. 2014;4:6966. https://doiorg.publicaciones.saludcastillayleon.es/10.1038/srep06966.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Zhang JJ, Kobert K, Flouri T, Stamatakis A. PEAR: A fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics. 2014;30:614–20. https://doiorg.publicaciones.saludcastillayleon.es/10.1093/bioinformatics/btt593.

    Article  PubMed  CAS  Google Scholar 

  53. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordo. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6. https://doiorg.publicaciones.saludcastillayleon.es/10.1038/nmeth.f.303.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/S0022-2836(05)80360-2.

    Article  PubMed  CAS  Google Scholar 

  55. Chen B, Yu K, Liang J, Huang W, Wang G, Su H, Qin Z, Huang X, Pan Z, Luo W, Luo Y, Wang Y. Latitudinal Variation in the Molecular Diversity and Community Composition of Symbiodiniaceae in Coral From the South China Sea. Front Microbiol. 2019;10. https://doiorg.publicaciones.saludcastillayleon.es/10.3389/fmicb.2019.01278

  56. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539–42. https://doiorg.publicaciones.saludcastillayleon.es/10.1093/sysbio/sys029.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Mori H, Maruyama F, Kato H, Toyoda A, Dozono A, Ohtsubo Y, Nagata A, Fujiyama A, Tsuda M, Kurokawa K. Design and experimental application of a novel non-degenerate universal primer set that amplifies prokaryotic 16S rRNA genes with a low possibility to amplify eukaryotic rRNA genes. DNA Res. 2013;21:217–27. https://doiorg.publicaciones.saludcastillayleon.es/10.1093/dnares/dst052.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Kim DR, Jeon CW, Cho G, Thomashow LS, Weller DM, Paik M, Lee YB, Kwak YS. Glutamic acid reshapes the plant microbiota to protect plants against pathogens. Microbiome. 2021;9:244. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s40168-021-01186-8.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Ma Y, Zhang W, Li R,Zhu P, Mou J, Liu C, Zhang J, Su X, Liang Y, Zeng F. The spatiotemporal variations of nutrients and its ecological response in the Pearl River Estuary and its adjacent sea areas under the influence of El Niño. Acta Scientiae Circumstantiae. 2023;43:36–46. https://doiorg.publicaciones.saludcastillayleon.es/10.13671/j.hjkxxb.2022.0358

  60. Li L, Li Z, Shen Y, Yang X. Study of stress of four environmental factors on Porites lutea and Goniopora stutchburyi (in Chinese). J Trop Oceanogr. 2013;32:72–7. https://doiorg.publicaciones.saludcastillayleon.es/10.3969/j.issn.1009-5470.2013.03.011.

    Article  CAS  Google Scholar 

  61. Dias M, Ferreira A, Gouveia R, Vinagre C. Synergistic effects of warming and lower salinity on the asexual reproduction of reef-forming corals. Ecol Ind. 2019;98:334–48. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.ecolind.2018.11.011.

    Article  Google Scholar 

  62. Stat M, Carter D, Hoegh-Guldberg O. The evolutionary history of Symbiodinium and scleractinian hosts-Symbiosis, diversity, and the effect of climate change. Perspectives in Plant Ecology Evolution and Systematics. 2006;8:23–43. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.ppees.2006.04.001.

    Article  Google Scholar 

  63. Cantin NE, van Oppen MJH, Willis BL, Mieog JC, Negri AP. Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs. 2009;28:405–14. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00338-009-0478-8.

    Article  Google Scholar 

  64. Ortiz JC, González-Rivero M, Mumby PJ. Can a thermally tolerant symbiont improve the future of Caribbean coral reefs? Glob Change Biol. 2013;19:273–81. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/gcb.12027.

    Article  Google Scholar 

  65. Hume BCC, D’Angelo C, Smith EG, Stevens JR, Burt J, Wiedenmann J. Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world’s hottest sea, the Persian/Arabian Gulf. Sci Rep. 2015;5:8562. https://doiorg.publicaciones.saludcastillayleon.es/10.1038/srep08562

  66. Silverstein RN, Cunning R, Baker AC. Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Glob Change Biol. 2015;21:236–49. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/gcb.12706.

    Article  Google Scholar 

  67. Brading P, Warner ME, Davey PA, Smith DJ, Achterberg EP, Suggett DJ. Differential effects of ocean acidification on growth and photosynthesis among phylotypes of Symbiodinium (Dinophyceae). Limnol Oceanogr. 2011;57:1255. https://doiorg.publicaciones.saludcastillayleon.es/10.4319/lo.2012.57.4.1255.

    Article  CAS  Google Scholar 

  68. Hume BCC, Voolstra CR, Arif C, D’Angelo C, Burt JA, Eyal G, Loya Y, Wiedenmann J. Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proc Natl Acad Sci. 2016;113:4416–21. https://doiorg.publicaciones.saludcastillayleon.es/10.1073/pnas.1601910113.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Baker DM, Andras JP, Jordán-Garza AG, Fogel ML. Nitrate competition in a coral symbiosis varies with temperature among Symbiodinium clades. ISME J. 2013;7:1248–51. https://doiorg.publicaciones.saludcastillayleon.es/10.1038/ismej.2013.12.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Palmas SD, Denis V, Ribas-Deulofeu L, Loubeyres M, Woo S, Hwang SJ, Song JI, Chen CA. Symbiodinium spp. associated with high-latitude scleractinian corals from Jeju Island. South Korea Coral Reefs. 2015;34:919–25. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00338-015-1286-y.

    Article  Google Scholar 

  71. Lesser MP, Falcón LI, Rodríguez-Román A, Enríquez S, Hoegh-Guldberg O, Iglesias-Prieto R. Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar Ecol Prog Ser. 2007;346:143–52. https://doiorg.publicaciones.saludcastillayleon.es/10.3354/meps07008.

    Article  CAS  Google Scholar 

  72. D’Angelo C, Hume BCC, Burt J, Smith EG, Achterberg EP, Wiedenmann J. Local adaptation constrains the distribution potential of heat-tolerant Symbiodinium from the Persian/Arabian Gulf. ISME J. 2015;9:2551–60. https://doiorg.publicaciones.saludcastillayleon.es/10.1038/ismej.2015.80.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Boulotte NM, Dalton SJ, Carroll AG, Harrison PL, Putnam HM, Peplow LM, van Oppen MJH. Exploring the Symbiodinium rare biosphere provides evidence for symbiont switching in reef-building corals. ISME J. 2016;10:2693–701. https://doiorg.publicaciones.saludcastillayleon.es/10.1038/ismej.2016.54.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Campbell BJ, Kirchman DL. Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient. ISME J. 2013;7:210–20. https://doiorg.publicaciones.saludcastillayleon.es/10.1038/ismej.2012.93.

    Article  PubMed  CAS  Google Scholar 

  75. Kirchman DL, Cottrel MT, DiTullio GR. Shaping of bacterial community composition and diversity by phytoplankton and salinity in the Delaware Estuary, USA. Aquat Microb Ecol. 2017;78:93–106. https://doiorg.publicaciones.saludcastillayleon.es/10.3354/ame01805.

    Article  Google Scholar 

  76. Ziegler M, Seneca FO, Yum LK, Palumbi SR, Voolstra CR. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat Commun. 2017;8:14213. https://doiorg.publicaciones.saludcastillayleon.es/10.1038/ncomms14213.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Shade A, Peter H, Allison SD, Baho DL, Berga M, Bürgmann H, Huber DH, Langenheder S, Lennon JT, Martiny JB, Matulich KL, Schmidt TM, Handelsman J. Fundamentals of microbial community resistance and resilience. Front Microbiol. 2012;3:417. https://doiorg.publicaciones.saludcastillayleon.es/10.3389/fmicb.2012.00417.

    Article  PubMed  PubMed Central  Google Scholar 

  78. Teoh F, Shah B, Ostrowski M, Paulsen I. Comparative membrane proteomics reveal contrasting adaptation strategies for coastal and oceanic marine Synechococcus cyanobacteria. Environ Microbiol. 2020;22:1816–28. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/1462-2920.14876.

    Article  PubMed  CAS  Google Scholar 

  79. Kim Y, Jeon J, Kwak MS, Kim GH, Koh I, Rho M. Photosynthetic functions of Synechococcus in the ocean microbiomes of diverse salinity and seasons. PLoS ONE. 2018;13: e0190266. https://doiorg.publicaciones.saludcastillayleon.es/10.1371/journal.pone.0190266.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Reisch CR, Moran MA, Whitman WB. Bacterial Catabolism of Dimethylsulfoniopropionate (DMSP). Front Microbiol. 2011;2:172. https://doiorg.publicaciones.saludcastillayleon.es/10.3389/fmicb.2011.00172.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Alsharif SM, Waznah MS, Ismaeil M, El-Sayed WS. 16S rDNA-based diversity analysis of bacterial communities associated with soft corals of the Red Sea, Al Rayyis, White Head, KSA. J Taibah Univ Sci. 2023;17. https://doiorg.publicaciones.saludcastillayleon.es/10.1080/16583655.2022.2156762

  82. Zhang L. Intermittent aerated membrane bioreactor for high salinity wastewater treatment and microbial community structure analysis. Membrane Science and Technology (in Chinese). Membrane Sci Technol. 2020;40:101–110. https://doiorg.publicaciones.saludcastillayleon.es/10.16159/j.cnki.issn1007-8924.2020.05.014

  83. Bai J, Li H, Zhao Y. Bacterial distribution at different stations in the Northern Yellow Sea (in Chinese). Acta Microbiologica Sinica. 2009;49:343–350. https://doiorg.publicaciones.saludcastillayleon.es/10.13343/j.cnki.wsxb.2009.03.005

  84. Shnit-Orland M, Kushmaro A. Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol. 2009;67:371–80. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/j.1574-6941.2008.00644.x.

    Article  PubMed  CAS  Google Scholar 

  85. Lima LFO, Alker AT, Papudeshi B, Morris MM, Edwards RA, de Putron SJ, Dinsdale EA. Coral and Seawater Metagenomes Reveal Key Microbial Functions to Coral Health and Ecosystem Functioning Shaped at Reef Scale. Microb Ecol. 2023;86:392–407. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00248-022-02094-6.

    Article  PubMed  CAS  Google Scholar 

  86. Yang H, Zhang X, Long H, Li Y, Feng YQ, Xie ZY. Antagonistic Mechanism of Pseudoalteromonas sp. against Vibrio harveyi. Fisheries Sci. 2019;38:833–838. https://doiorg.publicaciones.saludcastillayleon.es/10.16378/j.cnki.1003-1111.2019.06.013

  87. Tang K, Zhan W, Zhou Y, Xu T, Chen X, Wang W, Zeng Z, Wang Y, Wang X. Antagonism between coral pathogen Vibrio coralliilyticus and other bacteria in the gastric cavity of scleractinian coral Galaxea fascicularis. Sci China Earth Sci. 2020;63:157–66. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s11430-019-9388-3.

    Article  CAS  Google Scholar 

  88. Chen J, Liang J, Yu K, Yu X, Ge R, Qin L, Xu Y. Diversity of potential heat-tolerant bacteria associated with two species of scleractinian corals in Weizhou Island (in Chinese). Microbiol China. 2023;50:909−923. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s11430-019-9388-3

  89. Munn CB. The Role of Vibrios in Diseases of Corals. Microbiol Spectr. 2015;3. https://doiorg.publicaciones.saludcastillayleon.es/10.1128/microbiolspec.VE-0006-2014

  90. Sun X, Li Y, Yang Q, Zhang H, Xu N, Tang Z, Wu S, Jiang Y, Mohamed HF, Ou D, Zheng X. Identification of quorum sensing-regulated Vibrio fortis as potential pathogenic bacteria for coral bleaching and the effects on the microbial shift. Front Microbiol. 2023;14:1116737. https://doiorg.publicaciones.saludcastillayleon.es/10.3389/fmicb.2023.1116737.

    Article  PubMed  PubMed Central  Google Scholar 

  91. McDevitt‐Irwin JM, Baum JK, Garren M, Vega Thurber RL. Responses of Coral-Associated Bacterial Communities to Local and Global Stressors. Front Marine Sci. 2017;4. https://doiorg.publicaciones.saludcastillayleon.es/10.3389/fmars.2017.00262

  92. Hussein EI, Juhmani AF, Jacob JH, Telfah MA, Abd Al-razaq MA, Al-Horani FA, Al Zoubi MS, Malkawi HI. Effect of Various Local Anthropogenic Impacts on the Diversity of Coral Mucus-Associated Bacterial Communities. Journal of Marine Science and Engineering. 2022;10:863. https://doiorg.publicaciones.saludcastillayleon.es/10.3390/jmse10070863.

    Article  Google Scholar 

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Acknowledgements

This research was supported by the National Natural Science Foundation of China (42206157, 42030502, 42090041), the Natural Science Foundation of Guangxi Province (2022GXNSFBA035449), and the Self-Topic Project of Guangxi Laboratory on the Study of Coral Reefs in the South China Sea (GXLSCRSCS2022103), and the Central Public-Interest Scientific Institution Basal Research Fund (PM-zx703-202004-143 and PM-zx703-202105-176). 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. The data used in this paper are available from supporting information (SI), and the raw sequences were deposited in the NCBI Sequence Read Archive (SRA) database (https://www.ncbi.nlm.nih.gov/, accession number: Symbiodiniaceae: PRJNA1086834; bacteria: PRJNA1086806).

Funding

This research was supported by the National Natural Science Foundation of China (42206157, 42030502, 42090041), the Natural Science Foundation of Guangxi Province (2022GXNSFBA035449), and the Self-Topic Project of Guangxi Laboratory on the Study of Coral Reefs in the South China Sea (GXLSCRSCS2022103), and the Central Public-Interest Scientific Institution Basal Research Fund (PM-zx703-202004–143 and PM-zx703-202105–176).

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  1. Mengling Lan and Kaixiang Gao contributed equally to this work.

Authors and Affiliations

  1. Guangxi Laboratory On the Study of Coral Reefs in the South China SeaCoral Reef Research Center of ChinaSchool of Marine Sciences, Guangxi University, Nanning, China

    Mengling Lan, Kaixiang Gao, Zhenjun Qin, Zhanhong Li, Ru Meng, Lifei Wei, Biao Chen, Xiaopeng Yu & Kefu Yu

  2. Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, China

    Kefu Yu

  3. South China Institute of Environmental Sciences, MEE, Guangzhou, China

    Lijia Xu & Yongzhi Wang

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  1. Mengling Lan
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Contributions

We have taken appropriate measures to ensure the accuracy and reliability of the data and have followed the principles of scientific integrity in data analysis and result presentation. Z.Q. and K.Y. conceived the research; Z.Q., B.C., X.Y. and Y.Z. contributed the materials; M.L., K.G., Z.L. and R.M. performed all experiments; L.W. and L.X. identified coral species; M.L., K.G., Z.Q., and K.Y. wrote the manuscript; all authors edited and approved the manuscript. The authors declare that they have no conflict of interest.

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Correspondence to Zhenjun Qin or Kefu Yu.

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Lan, M., Gao, K., Qin, Z. et al. Coral microbiome in estuary coral community of Pearl River Estuary: insights into variation in coral holobiont adaptability to low-salinity conditions. BMC Microbiol 25, 278 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12866-025-04013-4

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BMC Microbiology

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