Abstract
Symbiotic dinoflagellates in the genus Symbiodiniaceae play vital roles in promoting resilience and increasing stress tolerance in their coral hosts. While much of the world’s coral succumb to the stresses associated with increasingly severe and frequent thermal bleaching events, live coral cover in Papua New Guinea (PNG) remains some of the highest reported globally despite the historically warm waters surrounding the country. Yet, in spite of the high coral cover in PNG and the acknowledged roles Symbiodiniaceae play within their hosts, these communities have not been characterized in this global biodiversity hotspot. Using high-throughput sequencing of the ITS2 rDNA gene, we profiled the endosymbionts of four coral species, Diploastrea heliopora, Pachyseris speciosa, Pocillopora acuta, and Porites lutea, across six sites in PNG. Our findings reveal patterns of Cladocopium and Durusdinium dominance similar to other reefs in the Coral Triangle, albeit with much greater intra- and intergenomic variation. Host- and site-specific variations in Symbiodiniaceae type profiles were observed across collection sites, appearing to be driven by environmental conditions. Notably, the extensive intra- and intergenomic variation, coupled with many previously unreported sequences, highlight PNG as a potential hotspot of symbiont diversity. This work represents the first characterization of the coral-symbiont community structure in the PNG marine biodiversity hotspot, serving as a baseline for future studies.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Papua New Guinea, located on the eastern edge of the biologically diverse Coral Triangle [1], is a global marine biodiversity hotspot with over 500 coral and 860 fish species across more than 600 islands [2,3,4]. Embedded within the West Pacific Warm Pool, PNG is characterized by some of the warmest seawaters of the global ocean [5]. Compared to its Indo-Pacific and Australian neighbors, PNG has warmer seas with water temperatures regularly reaching 29 to 30 °C, resulting in over 10 times more thermal stress events (e.g., degree heating weeks ≥ 4) [6, 7]. Yet, live coral cover in PNG is among the highest in the world with a reported countrywide average of 50%, surpassing the global average of below 30% [8]. This resilience is a testament to the ability of corals from PNG to adapt to challenging thermal conditions and recover from past stressors such as thermally induced bleaching, crown-of-thorns starfish invasion, and sedimentation [4, 8].
However, recent overexploitation of marine resources in PNG has resulted in coral cover plummeting from 75% to less than 10% in some locations [9,10,11]. The hundreds of isolated islands in PNG and the associated transportation difficulties make trade inaccessible, causing an estimated 85% of the country’s nine million population to depend almost entirely on the surrounding coral reefs for food and other daily needs [8]. This reliance and decline in coral cover has reduced fish abundance by more than half, and if left unchecked, it is predicted that many other marine food sources will also be reduced [12]. Such declines will have negative ecological impacts on marine ecosystems and create hardships for the communities that rely upon them.
The survival and resilience of coral reefs and their associated communities is largely contingent on the mutualistic relationship formed between the coral hosts and their dinoflagellate endosymbionts. Originating from the highly diverse family Symbiodiniaceae (Phylum: Myzozoa), these photosynthetic endosymbionts provide the coral host up to 90% of its nutritional requirements through photosynthate translocation [13, 14]. Symbiodiniaceae also play important roles in coral skeletal calcification [15, 16] and nutrient conservation and recycling [17]. In return, the algal symbionts receive respiratory CO2 and nitrogenous waste products, and gain access to downwelling light and protection from grazers [18]. This endosymbiotic relationship is paramount in coral reef ecosystems, with the expulsion of symbiont during thermally induced coral bleaching, a key cause of extensive coral mortality and reef degradation globally [8].
Corals are often dominated by one or two Symbiodiniaceae species at a given time [19,20,21] and can adapt to warmer waters by restructuring towards heat-tolerant Symbiodiniaceae [22,23,24,25]. For instance, in response to stressors such as bleaching, corals can shuffle the proportion of their heat-tolerant symbionts [26], and/or switch to different symbionts acquired from the environment [27]. To survive the historically high sea surface temperatures of the West Pacific Warm Pool, the corals of PNG have likely adopted similar strategies to help alleviate the impact of thermal stress events. Characterizing the coral-associated Symbiodiniaceae partners is an important step in understanding how this resilience facilitates the high coral cover in PNG. Among the eleven formally described genera today [28,29,30,31], Symbiodinium, Cladocopium, and Durusdinium (formerly Clade A, C, D) are the most common in Indo-Pacific corals [32]. Briefly, Symbiodinium thrives in high light or variable light conditions [33]; Cladocopium is ecologically diverse, associated with various hosts [34], and often provides their juvenile coral hosts with faster growth rates than other symbionts [35, 36]; while Durusdinium is recognized for its tolerance to large temperature and turbidity fluctuations [37]. While it currently boasts a high coral cover, PNG is predicted to experience accelerated warming relative to the global average [6, 7], and these rising sea surface temperatures coupled with high temperature anomalies in the region will make coral bleaching in PNG more frequent and severe [38]. Without knowing how the Symbiodiniaceae communities in PNG are currently structured, it becomes impossible to assess the direction and magnitude of any future changes.
Here, we characterized the endosymbionts of four coral species, Diploastrea heliopora, Pachyseris speciosa, Pocillopora acuta, and Porites lutea, across six sites in PNG by profiling the ITS2 rDNA marker. These corals were selected because they are readily identifiable, abundant, and have contrasting life histories. In short, both Porites lutea and Diploastrea heliopora are stress-tolerant, broadcast spawners with predominantly gonochoric polyps [39,40,41]; Pachyseris speciosa is a generalist, gonochoric spawning coral [41, 42]; while Pocillopora acuta is a fast-growing, opportunistic, and weedy hermaphrodite with a mixed mode of reproduction [42, 43]. As the first study to characterize coral-Symbiodiniaceae communities in PNG, this work will provide important insights and serve as an important baseline for future research.
Methods
Coral Sampling
Four coral species, Diploastrea heliopora, Pachyseris speciosa, Pocillopora acuta, and Porites lutea, were sampled in September 2018 from six sites across Papua New Guinea (PNG), namely, Kavieng, Rabaul, Kimbe Bay, Madang, Motupore Island, and Milne Bay (Fig. 1). All corals were collected from inshore reefs at depths between 5 and 10 m. Twenty samples per coral species were collected from each site. Samples were collected from visibly healthy individuals showing no signs of bleaching or disease. As per Wainwright et al. [44], collected samples were placed in separate sealed containers filled with seawater and kept in the shade until they could be preserved in 100% molecular-grade ethanol.
DNA Library Preparation and Sequencing
DNA was extracted from all samples using the DNeasy Blood and Tissue Kit (Qiagen) according to the manufacturer’s protocol. We followed the library preparation of Soon et al. [45] using the SYM_VAR primer pair for Symbiodiniaceae ITS2 amplification (Table S1) [46]. Polymerase chain reaction (PCR) was performed using 1 µL of sample DNA diluted 1:10 with PCR grade water, 0.5 µL of forward and reverse primers each, 6.25 µL of 2 × KAPA HiFi HotStart ReadyMix, and water to make a final volume of 12.5 µL per reaction mix. The PCR cycling conditions began with an initial step of 95 °C for 3 min followed by 25 cycles of 95 °C for 30 s, 55 °C for 30 s, and 72 °C for 30 s, before a final extension step at 72 °C for 5 min. PCR products were purified using AMPure XP magnetic beads (Agencourt) prior to indexing. Adaptor-index PCR was then performed using 2 µL of amplicon from the previous round, 0.5 µL of each uniquely indexed primer, 6.25 µL of 2 × KAPA HiFi HotStart ReadyMix, and water to a total volume of 12.5 µL per reaction. The PCR cycling conditions were 95 °C for 3 min for initial denaturation, followed by 8 cycles of 95 °C for 30 s, 55 °C for 30 s, and 72 °C for 30 s, with a final extension step at 72 °C for 5 min (see Table S1 for full details and primer sequences).
Successful PCR amplification for each step was verified by running 1 µL of each PCR product on a 1% agarose gel. Sample normalization was performed using the SequelPrep Normalization Plate Kit (Invitrogen, Carlsbad, CA, USA) to achieve a concentration of 1–2 ng/µL per reaction. Samples were then pooled and libraries were sequenced on the Illumina MiSeq platform (V3 chemistry, 300-bp paired-end reads, 30% PhiX spike) by Macrogen Inc.
Bioinformatics
Sequence data was processed using the SymPortal framework [47]. Demultiplexed and paired forward and reverse FASTQ files were submitted to SymPortal for sequence filtering and quality control. Contiguous sequences generated from Mothur were then screened with maximum ambiguities allowed set to 0 and maximum homopolymer set to 5 to discard reads generated from sequencing errors. Distinct sequences were identified, with singletons and doubletons excluded from further analysis. Non-Symbiodiniaceae sequences were then removed by searching against the SymPortal reference database on a sample-by-sample basis with BLASTn. Sequences were classified as Symbiodiniaceae if they shared identity > 80% and coverage > 95% to any sequence in the database using default settings. Size screening was performed with minimum and maximum cut-offs of 184 bp and 310 bp, respectively. Finally, the minimum entropy decomposition (MED) nodes were determined within a given set of sequences by the nucleotide positions most informative in distinguishing between these sequences to generate relative abundance data. SymPortal identifies and generates defining intragenomic variants (DIVs) as distinct sequences repeatedly found across multiple samples. These DIVs are subsequently used to characterize ITS2 type profiles, representing a set of co-occurring DIVs [47]. Samples containing fewer than 10,000 sequencing reads were excluded and rarefaction curves were plotted for the remaining samples to ensure that adequate sequencing depth had been attained (Fig. S1).
Environmental Data
Environmental data associated with the collection sites was extracted from Bio-ORACLE v2.1 [48]. All data layers were from the surface at a resolution of 5 arcmin, or approximately 9.2 km at the equator, and the long-term averages of each parameter at each site were extracted from their respective layers. Fourteen parameters were first obtained as baseline environmental conditions at each collection site. These were sea surface temperature, photosynthetically active radiation (PAR), pH, salinity, cloud cover, water clarity, chlorophyll a concentration, current velocity, dissolved oxygen levels, primary productivity, and silicate, calcite, nitrate, and phosphate concentrations. Multicollinearity was performed with the GGally package in R [49] to remove parameters with pairwise collinearity values greater than 0.7, and environmental parameters with the most biological significance to coral and Symbiodiniaceae physiology were retained (e.g., parameters related to photosynthesis and thermal tolerance). Four Bio-ORACLE parameters were retained and used for subsequent analyses: mean sea surface temperature (SST) (°C), mean photosynthetically active radiation (E m−2 d−1), mean pH, and mean salinity (PSS) (Table S2). Additionally, the number of thermal stress events that were likely to cause coral bleaching between 1985 and 2023, measured by degree heating weeks that reached or exceeded 4 °C-weeks [50], were obtained from NOAA Coral Reef Watch [51] (Fig. S2, Table S3).
Statistical Analyses
All statistical analyses were conducted in R [52]. To investigate both sequence and ecological beta diversity, we used both the sequence data and the defining intragenomic variant (DIV) compositions generated from SymPortal respectively. For sequence beta-diversity, a principal coordinate analysis (PCoA) plot with UniFrac distances was constructed to visualize the sample and type-profile clustering of Durusdinium and Cladocopium genotypes separately. Permutational analysis of variance (PERMANOVA) with 999 permutations was also conducted on the between-sample UniFrac distances to investigate how the type profiles were structured by host and site effects. To minimize spurious correlations, ecological beta-diversity analyses were conducted following the Compositional Dataset (CoDa) analysis framework [53] using the robust Aitchison distance metric [54] with the vegdist function from the vegan package [55]. A principal component analysis (PCA) plot was first constructed to visualize the Symbiodiniaceae DIV compositions hosted by the four coral species. PERMANOVA with 999 permutations was then conducted via the adonis2 function in the vegan package to investigate whether DIV compositions were significantly structured by coral species and collection site, and their interaction effect. Following results showing significant differences across coral species, analyses were then conducted separately for each coral species. Compositions of DIVs were first visualized via PCA for each host species. PERMANOVA was then conducted to further assess if these compositions were significantly different across collection sites. Using the envfit function from the vegan package, the four retained environmental parameters were fitted onto the PCA for each coral species to assess the correlation between these parameters and the compositions of Symbiodiniaceae DIV. Statistically significant environmental parameters in structuring the Symbiodiniaceae DIV compositions were then verified with PERMANOVA. The betadisper function was used to test for differences in within-group dispersions. The raw R code used for the analyses has been deposited in https://github.com/mingshengg/png_symbionts.
Results
Of the 480 samples processed and sequenced, 413 with read counts exceeding 10,000 were retained (Table S4). This resulted in an average per sample read count of 130,028 for Diploastrea heliopora, 166,819 for Pachyseris speciosa, 201,772 for Pocillopora acuta, and 141,485 for Porites lutea. All sequencing data have been deposited at the National Center for Biotechnology Information (BioProject ID: PRJNA977103).
The 413 coral samples collected from four coral species yielded a total of 1684 Symbiodiniaceae defining intragenomic variants (DIVs), resulting in 78 Symbiodiniaceae type profiles (set of co-occurring DIVs) from four genera, Symbiodinium, Cladocopium, Durusdinium, and Gerakladium. Specifically, there were 37 Cladocopium, 37 Durusdinium, 3 Gerakladium, and 1 Symbiodinium predicted type profiles. Notably, 34 of the 37 Durusdinium type profiles had D1 as the majority sequence, followed mostly by D4. Overall, Durusdinium and Cladocopium type profiles predominated in all 413 samples, constituting an average of 54.37 ± 2.29% (mean ± SE) and 45.60 ± 2.29% of the type profile compositions respectively (Fig. 2). Both Pachyseris speciosa and Pocillopora acuta were strongly associated with Cladocopium and Durusdinium type profiles. Specifically, Pachyseris speciosa hosted a higher proportion of Cladocopium (73.44 ± 3.98%) compared to Durusdinium profiles (26.48 ± 3.98%), while Pocillopora acuta hosted more Durusdinium (82.70 ± 2.39%) than Cladocopium profiles (17.29 ± 2.39%). Diploastrea heliopora comprised mostly of Durusdinium profiles (97.49 ± 1.04%) while Porites lutea was dominated almost entirely by Cladocopium profiles (99.39 ± 0.26%). While Symbiodinium DIVs were detected as background Symbiodiniaceae (< 1% abundance) in all coral species except Diploastrea heliopora, only one Porites lutea sample harbored Symbiodinium type profile at 1.58% relative abundance. Likewise, Gerakladium DIVs were also detected in the background of several samples across all four coral species but only three samples harbored Gerakladium type profiles. While Fugacium DIVs were detected, they were removed from subsequent analyses as they did not co-occur to form any type profiles, and were only detected in one sample at very low relative abundances, which suggests that they are unlikely to form stable associations with corals. Fugacium is also generally regarded as a free-living genus and a surface associate of corals rather than an endosymbiont [28, 56, 57], and has rarely been identified in other works across the Indo-Pacific region (e.g., absent in [58,59,60]). However, since rDNA copy number in Cladocopium can be five times more than Durusdinium [61], interpretation in the relative abundances of sequence reads especially in mixed endosymbiont communities with both Cladocopium and Durusdinium should be treated with due caution.
Of the 78 identified type profiles, 33 contained DIVs that have not been deposited in the SymPortal database, with 10 type profiles having those as the majority sequence (Fig. 3). Sixty-one of the 78 type profiles were host-specific, with 30 of these further exclusively found at one sampling site (Fig. S3). For instance, the D1/D6-D2.2-D4_1407_D-D2 type profile was only found in Diploastrea heliopora, and was only identified in 18 samples from Milne Bay. Averaged across all sites, each coral sample hosted 1.53 ± 0.03 type profiles or 25.54 ± 0.53 DIVs. While 25 of the 1684 identified DIVs were present in at least one sample of each coral species (9 Cladocopium and 16 Durusdinium DIVs; Table S7), only the C15h type profile was found across all four coral species, occurring only in 22 samples.
The number of species-specific, site-specific, and genera distribution of type profiles of each coral species is summarized in Table 1. Notably, among the four studied coral species, Pachyseris speciosa exhibited the lowest symbiont specificity, hosting the greatest number of type profiles, and type profiles that were host- and site-specific (Table 1), whereas Porites lutea had the highest symbiont specificity with the least total and site-specific type profiles, with all 91 samples dominated by Cladocopium profiles with C15 as the majority sequence. Across the 99 Pocillopora acuta samples, there was an average of 2.14 ± 0.05 type profiles, with only three samples having one type profile, and the remaining 96 associated with both Cladocopium and Durusdinium type profiles.
Between-sample and between-ITS2 type profile principal coordinate (PCoA) plots were constructed to highlight host-specificity and intergenomic variation of Cladocopium and Durusdinium sequences (Fig. 4). The Cladocopium between-sample PCoA plot highlights that, generally, Cladocopium found in Pachyseris speciosa, Pocillopora acuta, and Porites lutea display host-specificity, with sequences from each coral species occupying distinct spaces on the PCoA plot (Fig. 4a). This was also exemplified with PERMANOVA as host species explained the most variation in the between-sample UniFrac distances (R2 value = 0.6378, p-value < 0.001, Table S5). Notably, Porites lutea displays a very high symbiont specificity, as indicated by the genotypes clustering tightly to occupy a small distinct space on the PCoA plot. In contrast, the Cladocopium genotypes found in Pachyseris speciosa and Pocillopora acuta show much higher intergenomic variation, with many genotypes having high levels of genetic similarity to the Cladocopium specific to other coral species, whereas Cladocopium sequences in Diploastrea heliopora samples did not display any host-specificity and overlapped either with those found in Pachyseris speciosa or Porites lutea. Likewise, the Durusdinium between-sample PCoA plot indicates that the predicted Durusdinium sequences also have considerable intergenomic variation and exhibit host-specificity, albeit to a much lower extent as genotypes are generally all clustered in the middle of the PCoA plot. This was also highlighted through PERMANOVA, where host species still explained the most variation but to a lesser extent when compared to the Cladocopium between-sample UniFrac distances (R2 value = 0.29839, p-value < 0.001).
The PCoA plot of Cladocopium sequences across type profiles highlights distinct groupings of type profiles with the same majority sequence (Fig. 4b). For instance, type profiles with majority sequence C15 have very high levels of genetic similarity and are clustered together to occupy a small space. Additionally, there were type profiles with different majority sequences with high genetic similarities, such as type profiles with C1, C3, C21, C27, C40, and C66 as their majority sequences. Conversely, Durusdinium type profiles, except for a few previously not reported sequences, are all clustered together with D1 as the majority sequence.
Principal component analysis (PCA) and PERMANOVA were conducted to investigate whether Symbiodiniaceae DIV compositions differed significantly across coral species. The PCA plot of the 413 Symbiodiniaceae DIV compositions across all four coral host species had 69.22% of the variance explained by the principal component axis 1 (PC1) and 20.31% by the principal component axis 2 (PC2) (Fig. 5a). The 95% confidence ellipses showed that the compositions were generally distinct across coral species despite the overlapping regions. Further analysis via PERMANOVA with robust Aitchison distances revealed that the host species was the most significant driver of Symbiodiniaceae community structure, alongside the collection site and the interaction between species and collection site (Table 2).
Since the compositions of Symbiodiniaceae DIVs were species-specific, PCA and PERMANOVA were then conducted separately for each coral species to investigate site-specific patterns. The PCA illustrated slight site-specific clustering in Symbiodiniaceae DIV compositions (Fig. 5b), while PERMANOVA showed significant site-specific effects for all four coral species (Table S6). The compositions of DIVs in Pachyseris speciosa were the most dissimilar across sites (pseudo F statistic = 9.9317), followed by Diploastrea heliopora (pseudo F statistic = 5.9356), Pocillopora acuta (pseudo F statistic = 3.0647), and lastly Porites lutea (pseudo F statistic = 2.9279). The PC1 for Pachyseris speciosa also explained the least variance at 59.7% while the PC1 for Porites lutea explained the most variance at 87.8%. This illustrates that the composition of Symbiodiniaceae DIVs of Pachyseris speciosa had much greater variance across samples and sites compared to that of Porites lutea, contributing to the larger dispersion across-site as observed with PERMANOVA. However, within-site dispersions were heterogenous as demonstrated by betadisper in Porites lutea (F = 23.218, p-value < 0.001), Pachyseris speciosa (F = 6.4078, p-value < 0.001), and Pocillopora acuta (F = 6.9907, p-value < 0.001). Only Diploastrea heliopora had homogenous within-site dispersions (F = 0.4542, p-value = 0.810). While PERMANOVA may be affected by heterogeneity, especially for unbalanced designs [62], differences in sample sizes across sites for each coral species were small and their PCAs still showed relatively distinct structuring across sites, which suggests significant differences in Symbiodiniaceae compositions.
Results from a consensus approach with PERMANOVA and PCA showed that the Symbiodiniaceae compositions of the four corals were also shaped by environmental variables (Table 3). The number of degree heating week events reaching or exceeding 4 °C-weeks (DHW ≥ 4), sea surface temperature, photosynthetically available radiation (PAR), and salinity were significant in structuring the Symbiodiniaceae type profiles across all four coral species. The Symbiodiniaceae types of Diploastrea heliopora, Pachyseris speciosa, and Pocillopora acuta were further structured by pH levels. In particular, PAR was the most influential factor in structuring the Symbiodiniaceae compositions of Diploastrea heliopora, Pocillopora acuta, and Porites lutea, while DHW ≥ 4 was the most influential for Pachyseris speciosa.
Discussion
Consistent with other reef systems in the region, the corals in Papua New Guinea (PNG) are dominated by Cladocopium and Durusdinium, but demonstrate significant intra- and intergenomic variation. Across the 413 individuals from four coral species, 1684 defining intragenomic variants (DIVs) and 78 type profiles were identified, with 33 of these containing previously unreported DIVs. This prominent diversity largely stems from a very high host- and site-specificity, with 61 type profiles exclusive to a coral species, and 30 of these further exclusive to a sampling site. In addition to host- and site-specific effects, environmental factors also contribute to the structuring of the symbiont partners in coral hosts. In particular, photosynthetically active radiation (PAR) emerged as the most influential environmental variable in structuring the Symbiodiniaceae in Diploastrea heliopora, Pocillopora acuta, and Porites lutea, while the number of thermal anomaly events that can cause bleaching (measured as number of degree heating weeks, DHW, reaching or exceeding 4 °C-weeks) was the most influential for Pachyseris speciosa. Altogether, this work represents the first profiling of the Symbiodiniaceae communities of corals across PNG and provides evidence that the Symbiodiniaceae harbored by the corals here are remarkably diverse in comparison to other sites within the region.
The 413 coral fragments from four coral species sampled across six reef sites in PNG identified four symbiont genera, Cladocopium, Durusdinium, Gerakladium, and Symbiodinium. Consistent with other Indo-Pacific reef systems [21, 58, 59, 63], Cladocopium and Durusdinium endosymbionts are dominant in PNG corals. Meanwhile, Symbiodinium and Gerakladium defining intragenomic variants (DIVs) were present at low background levels across several coral samples, although only Gerakladium type profiles were identified by SymPortal. Similar observations of Gerakladium and Symbiodinium at low background levels have been reported in corals of reef systems across the Coral Triangle such as Malaysia and Singapore [21, 64]. The dominance patterns of Cladocopium and Durusdinium were also consistent with previous research on the same coral species, particularly the dominance of Durusdinium in Diploastrea heliopora and Cladocopium in Porites lutea [21, 58, 59, 65, 66], indicating a pronounced preference for specific Symbiodiniaceae and highlighting the role of the coral host in structuring its endosymbiont community.
This work identified a total of 1684 unique Symbiodiniaceae DIVs and 77 type profiles across 413 samples collected from four species of coral, far surpassing the numbers reported in prior studies within the Asia–Pacific region. For example, 263 samples across three coral species in Singapore identified only 15 type profiles [59], while 60 samples across 30 different coral species from Hong Kong only identified 13 type profiles [67]. While this study had a broader sampling range, a recurring observation in coral-Symbiodiniaceae communities across the region is the prevalence of certain type profiles across coral hosts and/or sampling sites [68,69,70]. A clear illustrative example is the Cladocopium type profile C3u/C3/C115/C27-C3bn; this profile was found consistently across all six sampling sites and five coral species in research performed in Singapore [71]. In contrast, the type profiles identified in PNG exhibited marked host- and site-specificity. For instance, among the 11 type profiles unique to Diploastrea heliopora, nine were further exclusive to a specific sampling site where they were dominant within their host. Illustratively, the type profile D1/D6-D2.2-D4-1407_D-D2 was only found in 18 Diploastrea heliopora samples from Milne Bay at an average relative abundance of 98.62 ± 1.11%. This pattern of host- and site-specificity contributes to the high diversity of type profiles in PNG corals.
Type profiles are generally considered to represent distinct genotypes of Symbiodiniaceae and are indicative of putative taxa [47]. However, the tight clustering of type profiles, especially those with the same majority sequence in the principal coordinate analysis (PCoA) plots suggests that each cluster likely represents groups of closely related strains instead of distinct species. For example, almost all Durusdinium type profiles formed a tight cluster on the PCoA plot with D1 as the majority sequence followed by D4 sequences, indicative of D. trenchii [72]. This suggests that these Durusdinium type profiles represent closely related strains of D. trenchii rather than putative taxa. Likewise, many of the Cladocopium type profiles with C1 or C40 as their majority sequences likely represent the recently described C. vulgare and C. madreporum, respectively, common across many species of corals throughout the Indo-Pacific [73]. Regardless, these type profiles exhibited marked intergenomic variation across distinct hosts and sampling sites to be characterized as distinct type profiles. Similar patterns of high intergenomic variation and host species-specific genotypes in D. trenchii were also observed in Red Sea corals [74].
In addition to the high number of type profiles identified here, the number of DIVs hosted by each coral sample was also far greater than in other studies. For example, Pocillopora acuta samples in our study harbored an average of 36.49 ± 0.66 DIVs, while those collected across Malaysia and Singapore had 10.8 to 24.2 DIVs [21, 64]. Since each DIV represents an ITS2 intragenomic variant, this underscores the greater intragenomic sequence diversity within the corals of PNG compared to other Indo-Pacific reef systems. This extensive intra- and intergenomic variation, coupled with many previously unreported sequences, suggests that coral-Symbiodiniaceae diversity in PNG surpasses that of other reef systems across the region. Reefs considered resilient often harbor homogenous Symbiodiniaceae communities with low diversities, a consequence of these communities shifting towards stress-tolerant taxa with each bleaching event [24, 75, 76]. Despite being situated in the West Pacific Warm Pool and having experienced multiple bleaching events [4, 8], the corals in PNG have seemingly evaded the typical Symbiodiniaceae community restructuring and instead persist in maintaining endosymbiont communities with high intra- and intergenomic variations. However, these endosymbiont restructuring events are crucial for enhancing the corals’ ability to thrive in high temperature conditions [77]. The observed diversity in PNG could therefore potentially render its reefs more susceptible to future bleaching events, especially if they become more severe and frequent [38]. On the contrary, coral-Symbiodinium symbioses can become less stable with each restructuring event, and the high genetic and community-level variation present in PNG may help the corals persist in changing climates [78,79,80]. In all cases, this emphasizes the need for greater protection and more research in hotspots with apparent high symbiont diversity like PNG.
Expectedly, the structure of Symbiodiniaceae partners was largely determined by the coral host, with sampling sites playing a comparatively minor role. This was substantiated by the concordance between the variance allocated in the PERMANOVA results, the host-specific clustering of the predicted genotypes especially in Cladocopium, and the low number of type profiles shared across coral hosts. Between-sample PCoA plots show that Cladocopium genotypes from one coral host can display intermediate to very high levels of genetic similarity with those from another coral host, despite the generally pronounced host-specificity. These Cladocopium may have originated from nearby corals of different species [81], especially since spawning corals, like those studied here, primarily acquire their algal endosymbionts horizontally, which are then selectively regulated by the host to give rise to the observed specificity [82, 83]. Alternatively, these sequences may represent hybrids between endosymbionts specific to two distinct coral hosts, considering the growing evidence of sexual reproduction within Symbiodiniaceae [84,85,86]. Whether these genotypes represent distinct species or hybrids will necessitate the use of additional markers, but these novel genotypes could represent physiologically advantageous symbionts that have adapted to their specific environments [87, 88]. Whereas Diploastrea heliopora were largely associated with Durusdinium symbionts, its background Cladocopium sequences overlapped with those of Porites lutea and Pachyseris speciosa, suggesting that these Cladocopium symbionts are host-generalists and associate across different coral hosts [73].
Although the number of DHW ≥ 4 events was significant in shaping the Symbiodiniaceae of all four examined coral species, it was the most influential variable only in Pachyseris speciosa. Degree heating weeks (DHW) is defined as the accumulation of temperature anomalies exceeding the monthly maximum mean sea surface temperature [89]. Symbiont cell morphology and cell division rates can start to alter at 2 °C-weeks [90], transcriptional changes in Symbiodiniaceae can occur at 3 °C-weeks [91], while 4 °C-weeks and beyond is associated with ecologically significant bleaching levels and breakdown of coral assemblage structure [89, 92, 93]. In fact, DHW consistently reached or exceeded 8 °C-weeks in PNG, which is thought to result in reef-wide bleaching and coral mortalities [94]. Yet, these bleaching and symbiont restructuring events were only the most significant in Pachyseris speciosa, and combined with the still high intra- and intergenomic Symbiodiniaceae diversity in PNG, seems to suggest that the thermal anomaly events did not result in severe recurring bleaching events and the symbiont community homogenization that follows [19, 76, 95]. Whether the high symbiont diversity is conferring thermal resilience to the corals requires a more thorough investigation, but without long-term investigation of local stressors, it is difficult to predict in situ bleaching events and if or how the reef-wide symbiont communities are restructured [96, 97].
Algal symbionts of the other three coral species were largely structured by PAR. Specific symbionts can thrive in distinct photic environments [98], with specific Symbiodiniaceae thriving in high-light environments, while others prefer darker conditions [99]. High light exposure can also synergistically cause bleaching with heat stress, exacerbating bleaching intensity [100] and accelerating shifts in Symbiodiniaceae [101]. Culture-based experiments have further demonstrated how different Symbiodiniaceae members have varying tolerance to thermal and light stress [102], which when coupled with host-specific interactions could have marked effects on coral physiological performance [103]. Nevertheless, the within-group distributions of Pachyseris speciosa, Pocillopora acuta, and Porites lutea were also highly significant, suggesting intraspecific variation [63] and/or fine-scale environmental differences such as depth [104] also played a significant role in shaping the coral’s endosymbiont partners even within the same sites. For a more comprehensive investigation of Symbiodiniaceae structuring and assembly, future studies should combine large-scale datasets such as thermal anomalies, light levels, and upwelling [105], with fine-scale variables such as reef structure, depth, and turbidity [106, 107] to monitor long-term temporal and spatial stability of these Symbiodiniaceae communities.
In conclusion, our study sheds light on the diverse Symbiodiniaceae communities associated with corals in PNG. We found that the Symbiodiniaceae communities here were broadly similar to neighboring regions such as the Great Barrier Reef and the wider Coral Triangle. However, PNG reefs hosted Symbiodiniaceae communities with much greater intra- and intergenomic variation compared to other reef systems across the Indo-Pacific region, suggesting the possibility of PNG as a hotspot of coral endosymbiont diversity. The genera Cladocopium and Durusdinium emerged as the dominant symbionts, with their dominance patterns mainly influenced by host-specificity and site-specific environmental factors. Coral-Symbiodiniaceae compositions were further shaped by the unique suite of environmental variables present at each sampling site. The reefs of PNG and the associated warm water masses of the West Pacific Warm Pool could offer a glimpse into how the reefs of the Coral Triangle will adapt to ongoing climate warming.
Data Availability
All sequences associated with this work have been deposited at the National Center for Biotechnology Information under BioProject ID: PRJNA977103. Codes used for the analyses are available on GitHub, https://github.com/mingshengg/png_symbionts.
References
Hoeksema BW (2007) Delineation of the Indo-Malayan centre of maximum marine biodiversity: the Coral Triangle. In: Renema W (ed) Biogeography, time, and place: distributions, barriers, and islands. Springer, Netherlands, Dordrecht, pp 117–178
Fricke R, Allen GR, Andréfouët S et al (2014) Checklist of the marine and estuarine fishes of Madang District, Papua New Guinea, western Pacific Ocean, with 820 new records. Zootaxa 3832:1–247. https://doi.org/10.11646/zootaxa.3832.1.1
Fricke R, Allen GR, Amon D, et al (2019) Checklist of the marine and estuarine fishes of New Ireland Province, Papua New Guinea, western Pacific Ocean, with 810 new records. Zootaxa 4588:zootaxa.4588.1.1. https://doi.org/10.11646/zootaxa.4588.1.1
Moritz C, Vii J, Long WL et al (2018) Status and trends of coral reefs of the Pacific. https://gcrmn.net/wp-content/uploads/2022/06/Status-and-Trends-of-Coral-Reefs-of-the-Pacific-2018.pdf
Cravatte S, Delcroix T, Zhang D et al (2009) Observed freshening and warming of the western Pacific Warm Pool. Clim Dyn 33:565–589. https://doi.org/10.1007/s00382-009-0526-7
Peñaflor EL, Skirving WJ, Strong AE et al (2009) Sea-surface temperature and thermal stress in the Coral Triangle over the past two decades. Coral Reefs 28:841–850. https://doi.org/10.1007/s00338-009-0522-8
Lough JM (2012) Small change, big difference: sea surface temperature distributions for tropical coral reef ecosystems, 1950–2011. J Geophys Res Oceans 117. https://doi.org/10.1029/2012JC008199
Souter D, Planes S, Wicquart J, et al (2020) Status of coral reefs of the world: 2020 report. Glob Coral Ref Monit Netw GCRWM Int Coral Reef Initiat ICRI. https://doi.org/10.59387/WOTJ9184
Jones GP, McCormick MI, Srinivasan M, Eagle JV (2004) Coral decline threatens fish biodiversity in marine reserves. Proc Natl Acad Sci 101:8251–8253
Haywood MDE, Dennis D, Thomson DP, Pillans RD (2016) Mine waste disposal leads to lower coral cover, reduced species richness and a predominance of simple coral growth forms on a fringing coral reef in Papua New Guinea. Mar Environ Res 115:36–48. https://doi.org/10.1016/j.marenvres.2016.02.003
Turak E, DeVantier L, Szava-Kovats R, Brodie J (2021) Impacts of coastal land use change in the wet tropics on nearshore coral reefs: case studies from Papua New Guinea. Mar Pollut Bull 168:112445. https://doi.org/10.1016/j.marpolbul.2021.112445
Butler JRA, Skewes T, Mitchell D et al (2014) Stakeholder perceptions of ecosystem service declines in Milne Bay, Papua New Guinea: is human population a more critical driver than climate change? Mar Policy 46:1–13. https://doi.org/10.1016/j.marpol.2013.12.011
Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460. https://doi.org/10.2307/1297526
Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. Ecosyst World 25:75–87
Gattuso J-P, Allemand D, Frankignoulle M (1999) Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry 1. Am Zool 39:160–183. https://doi.org/10.1093/icb/39.1.160
Dellaert Z, Vargas PA, La Riviere PJ, Roberson LM (2022) Uncovering the effects of symbiosis and temperature on coral calcification. Biol Bull 242:62–73. https://doi.org/10.1086/716711
Wang J-T, Douglas AE (1998) Nitrogen recycling or nitrogen conservation in an alga–invertebrate symbiosis? J Exp Biol 201:2445–2453. https://doi.org/10.1242/jeb.201.16.2445
Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261. https://doi.org/10.1128/MMBR.05014-11
Jain SS, Afiq-Rosli L, Feldman B et al (2020) Homogenization of endosymbiont communities hosted by equatorial corals during the 2016 mass bleaching event. Microorganisms 8:1370. https://doi.org/10.3390/microorganisms8091370
Tan YTR, Wainwright BJ, Afiq-Rosli L et al (2020) Endosymbiont diversity and community structure in Porites lutea from Southeast Asia are driven by a suite of environmental variables. Symbiosis 80:269–277. https://doi.org/10.1007/s13199-020-00671-2
Ong JH, Wainwright BJ, Jain SS et al (2022) Species and spatio-environmental effects on coral endosymbiont communities in Southeast Asia. Coral Reefs 41:1131–1145. https://doi.org/10.1007/s00338-022-02254-7
Oliver TA, Palumbi SR (2011) Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30:429–440. https://doi.org/10.1007/s00338-011-0721-y
Howells EJ, Abrego D, Meyer E et al (2016) Host adaptation and unexpected symbiont partners enable reef-building corals to tolerate extreme temperatures. Glob Change Biol 22:2702–2714. https://doi.org/10.1111/gcb.13250
Palacio-Castro AM, Smith TB, Brandtneris V et al (2023) Increased dominance of heat-tolerant symbionts creates resilient coral reefs in near-term ocean warming. Proc Natl Acad Sci 120:e2202388120. https://doi.org/10.1073/pnas.2202388120
Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689. https://doi.org/10.1146/annurev.ecolsys.34.011802.132417
Cunning R, Silverstein RN, Baker AC (2015) Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change. Proc R Soc B Biol Sci 282:20141725. https://doi.org/10.1098/rspb.2014.1725
Boulotte NM, Dalton SJ, Carroll AG et al (2016) Exploring the Symbiodinium rare biosphere provides evidence for symbiont switching in reef-building corals. ISME J 10:2693–2701. https://doi.org/10.1038/ismej.2016.54
LaJeunesse TC, Parkinson JE, Gabrielson PW et al (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570-2580.e6. https://doi.org/10.1016/j.cub.2018.07.008
LaJeunesse TC, Wiedenmann J, Casado-Amezúa P et al (2022) Revival of Philozoon Geddes for host-specialized dinoflagellates, ‘zooxanthellae’, in animals from coastal temperate zones of northern and southern hemispheres. Eur J Phycol 57:166–180. https://doi.org/10.1080/09670262.2021.1914863
Nitschke MR, Craveiro SC, Brandão C et al (2020) Description of Freudenthalidium gen. nov. and Halluxium gen. nov. to formally recognize Clades Fr3 and H as genera in the family Symbiodiniaceae (Dinophyceae). J Phycol 56:923–940. https://doi.org/10.1111/jpy.12999
Pochon X, LaJeunesse TC (2021) Miliolidium n. gen, a new symbiodiniacean genus whose members associate with soritid Foraminifera or are free-living. J Eukaryot Microbiol 68:e12856. https://doi.org/10.1111/jeu.12856
Gong S, Chai G, Sun W et al (2021) Global-scale diversity and distribution characteristics of reef-associated Symbiodiniaceae via the cluster-based parsimony of internal transcribed spacer 2 sequences. J Ocean Univ China 20:296–306. https://doi.org/10.1007/s11802-021-4364-5
Shoguchi E, Beedessee G, Tada I et al (2018) Two divergent Symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes. BMC Genomics 19:458. https://doi.org/10.1186/s12864-018-4857-9
Beltrán VH, Puill-Stephan E, Howells E et al (2021) Physiological diversity among sympatric, conspecific endosymbionts of coral (Cladocopium C1acro) from the Great Barrier Reef. Coral Reefs 40:985–997. https://doi.org/10.1007/s00338-021-02092-z
Cantin NE, van Oppen MJH, Willis BL et al (2009) Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28:405–414. https://doi.org/10.1007/s00338-009-0478-8
Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494. https://doi.org/10.1126/science.1095733
Hoadley KD, Lewis AM, Wham DC et al (2019) Host-symbiont combinations dictate the photo-physiological response of reef-building corals to thermal stress. Sci Rep 9:9985. https://doi.org/10.1038/s41598-019-46412-4
Sully S, Burkepile DE, Donovan MK et al (2019) A global analysis of coral bleaching over the past two decades. Nat Commun 10:1264. https://doi.org/10.1038/s41467-019-09238-2
Guest JR, Baird AH, Goh BPL, Chou LM (2012) Sexual systems in scleractinian corals: an unusual pattern in the reef-building species Diploastrea heliopora. Coral Reefs 31:705–713. https://doi.org/10.1007/s00338-012-0881-4
Shlesinger Y, Goulet TL, Loya Y (1998) Reproductive patterns of scleractinian corals in the northern Red Sea. Mar Biol 132:691–701
Darling ES, Alvarez-Filip L, Oliver TA et al (2012) Evaluating life-history strategies of reef corals from species traits. Ecol Lett 15:1378–1386. https://doi.org/10.1111/j.1461-0248.2012.01861.x
Kerr AM, Baird AH, Hughes TP (2010) Correlated evolution of sex and reproductive mode in corals (Anthozoa: Scleractinia). Proc R Soc B Biol Sci 278:75–81. https://doi.org/10.1098/rspb.2010.1196
Smith HA, Moya A, Cantin NE, et al (2019) Observations of simultaneous sperm release and larval planulation suggest reproductive assurance in the coral Pocillopora acuta. Front Mar Sci 6. https://doi.org/10.3389/fmars.2019.00362
Wainwright BJ, Zahn GL, Afiq-Rosli L et al (2020) Host age is not a consistent predictor of microbial diversity in the coral Porites lutea. Sci Rep 10:14376. https://doi.org/10.1038/s41598-020-71117-4
Soon N, Quek ZBR, Pohl S, Wainwright BJ (2023) More than meets the eye: characterizing the cryptic species complex and Symbiodiniaceae communities in the reef-dwelling nudibranch Pteraeolidia ‘semperi’ (Nudibranchia: Aeolidioidea) from Singapore. J Molluscan Stud 89:eyad011. https://doi.org/10.1093/mollus/eyad011
Hume BCC, Ziegler M, Poulain J et al (2018) An improved primer set and amplification protocol with increased specificity and sensitivity targeting the Symbiodinium ITS2 region. PeerJ 6:e4816. https://doi.org/10.7717/peerj.4816
Hume BCC, Smith EG, Ziegler M et al (2019) SymPortal: a novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling. Mol Ecol Resour 19:1063–1080. https://doi.org/10.1111/1755-0998.13004
Assis J, Tyberghein L, Bosch S et al (2018) Bio-ORACLE v2.0: extending marine data layers for bioclimatic modelling. Glob Ecol Biogeogr 27:277–284. https://doi.org/10.1111/geb.12693
Schloerke B, Crowley J, Cook D (2018) Package ‘GGally.’ Ext ‘ggplot2’See 713. https://ggobi.github.io/ggally/authors.html#citation
Eakin CM, Morgan JA, Heron SF et al (2010) Caribbean corals in crisis: record thermal stress, bleaching, and mortality in 2005. PLoS ONE 5:e13969. https://doi.org/10.1371/journal.pone.0013969
NOAA Coral Reef Watch updated daily (2018) NOAA Coral Reef Watch Version 3.1 Daily Global 5km Satellite Coral Bleaching Degree Heating Week Product, Jun. 3, 2013-Jun. 2, 2014. NOAA Coral Reef Watch, College Park, Maryland, USA. https://ftp.star.nesdis.noaa.gov/pub/sod/mecb/crw/data/5km/v3.1/nc/v1.0/daily/dhw/. Accessed 2020-09-01
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Gloor GB, Macklaim JM, Pawlowsky-Glahn V, Egozcue JJ (2017) Microbiome datasets are compositional: and this is not optional. Front Microbiol 8:2224. https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2017.02224/full
Martino C, Morton JT, Marotz CA et al (2019) A novel sparse compositional technique reveals microbial perturbations. mSystems 4:e00016-19
Oksanen J, Blanchet FG, Friendly M et al (2019) vegan: Community Ecology Package
González-Pech RA, Bhattacharya D, Ragan MA, Chan CX (2019) Genome evolution of coral reef symbionts as intracellular residents. Trends Ecol Evol 34:799–806. https://doi.org/10.1016/j.tree.2019.04.010
Fujise L, Suggett DJ, Stat M et al (2021) Unlocking the phylogenetic diversity, primary habitats, and abundances of free-living Symbiodiniaceae on a coral reef. Mol Ecol 30:343–360. https://doi.org/10.1111/mec.15719
Chankong A, Kongjandtre N, Senanan W, Manthachitra V (2020) Community composition of Symbiodiniaceae among four scleractinian corals in the eastern Gulf of Thailand. Reg Stud Mar Sci 33:100918. https://doi.org/10.1016/j.rsma.2019.100918
Quek ZBR, Tanzil JTI, Jain SS et al (2023) Limited influence of seasonality on coral microbiomes and endosymbionts in an equatorial reef. Ecol Indic 146:109878. https://doi.org/10.1016/j.ecolind.2023.109878
Tonk L, Sampayo EM, Weeks S et al (2013) Host-specific interactions with environmental factors shape the distribution of Symbiodinium across the Great Barrier Reef. PLoS ONE 8:e68533. https://doi.org/10.1371/journal.pone.0068533
Saad OS, Lin X, Ng TY, et al (2020) Genome size, rDNA copy, and qPCR assays for Symbiodiniaceae. Front Microbiol 11. https://doi.org/10.3389/fmicb.2020.00847
Anderson MJ, Walsh DCI (2013) PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol Monogr 83:557–574. https://doi.org/10.1890/12-2010.1
Leveque S, Afiq-Rosli L, Ip YCA et al (2019) Searching for phylogenetic patterns of Symbiodiniaceae community structure among Indo-Pacific Merulinidae corals. PeerJ 7:e7669. https://doi.org/10.7717/peerj.7669
Lee LK, Leaw CP, Lee LC et al (2022) Molecular diversity and assemblages of coral symbionts (Symbiodiniaceae) in diverse scleractinian coral species. Mar Environ Res 179:105706. https://doi.org/10.1016/j.marenvres.2022.105706
LaJeunesse TC, Pettay DT, Sampayo EM et al (2010) Long-standing environmental conditions, geographic isolation and host–symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeogr 37:785–800. https://doi.org/10.1111/j.1365-2699.2010.02273.x
Robbins SJ, Singleton CM, Chan CX et al (2019) A genomic view of the reef-building coral Porites lutea and its microbial symbionts. Nat Microbiol 4:2090–2100. https://doi.org/10.1038/s41564-019-0532-4
Saad OS, Lin X, Ng TY et al (2022) Species richness and generalists–specialists mosaicism of symbiodiniacean symbionts in corals from Hong Kong revealed by high-throughput ITS sequencing. Coral Reefs 41:1–12. https://doi.org/10.1007/s00338-021-02196-6
Camp EF, Edmondson J, Doheny A et al (2019) Mangrove lagoons of the Great Barrier Reef support coral populations persisting under extreme environmental conditions. Mar Ecol Prog Ser 625:1–14. https://doi.org/10.3354/meps13073
Botté ES, Cantin NE, Mocellin VJL et al (2022) Reef location has a greater impact than coral bleaching severity on the microbiome of Pocillopora acuta. Coral Reefs 41:63–79. https://doi.org/10.1007/s00338-021-02201-y
Leinbach SE, Speare KE, Strader ME (2023) Reef habitats structure symbiotic microalgal assemblages in corals and contribute to differential heat stress responses. Coral Reefs 42:205–217. https://doi.org/10.1007/s00338-022-02316-w
Smith EG, Gurskaya A, Hume BCC et al (2020) Low Symbiodiniaceae diversity in a turbid marginal reef environment. Coral Reefs 39:545–553. https://doi.org/10.1007/s00338-020-01956-0
LaJeunesse TC, Wham DC, Pettay DT et al (2014) Ecologically differentiated stress-tolerant endosymbionts in the dinoflagellate genus Symbiodinium (Dinophyceae) Clade D are different species. Phycologia 53:305–319. https://doi.org/10.2216/13-186.1
Butler CC, Turnham KE, Lewis AM et al (2023) Formal recognition of host‐generalist species of dinoflagellate (Cladocopium, Symbiodiniaceae) mutualistic with Indo‐Pacific reef corals. J Phycol
Hume BCC, Mejia-Restrepo A, Voolstra CR, Berumen ML (2020) Fine-scale delineation of Symbiodiniaceae genotypes on a previously bleached central Red Sea reef system demonstrates a prevalence of coral host-specific associations. Coral Reefs 39:583–601. https://doi.org/10.1007/s00338-020-01917-7
Howe-Kerr LI, Bachelot B, Wright RM et al (2020) Symbiont community diversity is more variable in corals that respond poorly to stress. Glob Change Biol 26:2220–2234. https://doi.org/10.1111/gcb.14999
Quigley KM, Ramsby B, Laffy P et al (2022) Symbioses are restructured by repeated mass coral bleaching. Sci Adv 8:eabq8349. https://doi.org/10.1126/sciadv.abq8349
Silverstein RN, Cunning R, Baker AC (2015) Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Glob Change Biol 21:236–249. https://doi.org/10.1111/gcb.12706
Fabina NS, Putnam HM, Franklin EC et al (2013) Symbiotic specificity, association patterns, and function determine community responses to global changes: defining critical research areas for coral-Symbiodinium symbioses. Glob Change Biol 19:3306–3316. https://doi.org/10.1111/gcb.12320
Baker AC (2004) Symbiont diversity on coral reefs and its relationship to bleaching resistance and resilience. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin, Heidelberg, pp 177–194
Baskett ML, Gaines SD, Nisbet RM (2009) Symbiont diversity may help coral reefs survive moderate climate change. Ecol Appl 19:3–17. https://doi.org/10.1890/08-0139.1
Williamson OM, Allen CE, Williams DE et al (2021) Neighboring colonies influence uptake of thermotolerant endosymbionts in threatened Caribbean coral recruits. Coral Reefs 40:867–879. https://doi.org/10.1007/s00338-021-02090-1
Hartmann AC, Baird AH, Knowlton N, Huang D (2017) The paradox of environmental symbiont acquisition in obligate mutualisms. Curr Biol 27:3711-3716.e3. https://doi.org/10.1016/j.cub.2017.10.036
Quigley KM, Willis BL, Bay LK (2017) Heritability of the Symbiodinium community in vertically- and horizontally-transmitting broadcast spawning corals. Sci Rep 7:8219. https://doi.org/10.1038/s41598-017-08179-4
Pettay DT, Wham DC, Pinzón JH, Lajeunesse TC (2011) Genotypic diversity and spatial–temporal distribution of Symbiodinium clones in an abundant reef coral. Mol Ecol 20:5197–5212. https://doi.org/10.1111/j.1365-294X.2011.05357.x
Brian JI, Davy SK, Wilkinson SP (2019) Multi-gene incongruence consistent with hybridisation in Cladocopium (Symbiodiniaceae), an ecologically important genus of coral reef symbionts. PeerJ 7:e7178. https://doi.org/10.7717/peerj.7178
Figueroa RI, Howe-Kerr LI, Correa AMS (2021) Direct evidence of sex and a hypothesis about meiosis in Symbiodiniaceae. Sci Rep 11:18838. https://doi.org/10.1038/s41598-021-98148-9
Byler KA, Carmi-Veal M, Fine M, Goulet TL (2013) Multiple symbiont acquisition strategies as an adaptive mechanism in the coral Stylophora pistillata. PLoS ONE 8:e59596. https://doi.org/10.1371/journal.pone.0059596
Bhattacharya D, Stephens TG, Chille EE et al (2023) Facultative lifestyle drives diversity of coral algal symbionts. Trends Ecol Evol. https://doi.org/10.1016/j.tree.2023.10.005
Liu G, Heron SF, Eakin CM et al (2014) Reef-scale thermal stress monitoring of coral ecosystems: new 5-km global products from NOAA Coral Reef Watch. Remote Sens 6:11579–11606. https://doi.org/10.3390/rs61111579
Gierz S, Ainsworth TD, Leggat W (2020) Diverse symbiont bleaching responses are evident from 2-degree heating week bleaching conditions as thermal stress intensifies in coral. Mar Freshw Res 71:1149–1160. https://doi.org/10.1071/MF19220
Cunning R, Baker AC (2020) Thermotolerant coral symbionts modulate heat stress-responsive genes in their hosts. Mol Ecol 29:2940–2950. https://doi.org/10.1111/mec.15526
Skirving WJ, Heron SF, Marsh BL et al (2019) The relentless march of mass coral bleaching: a global perspective of changing heat stress. Coral Reefs 38:547–557. https://doi.org/10.1007/s00338-019-01799-4
Hughes TP, Kerry JT, Baird AH et al (2018) Global warming transforms coral reef assemblages. Nature 556:492–496. https://doi.org/10.1038/s41586-018-0041-2
Kayanne H (2017) Validation of degree heating weeks as a coral bleaching index in the northwestern Pacific. Coral Reefs 36:63–70. https://doi.org/10.1007/s00338-016-1524-y
Jones AM, Berkelmans R, van Oppen MJH et al (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc R Soc B Biol Sci 275:1359–1365. https://doi.org/10.1098/rspb.2008.0069
McClanahan TR, Darling ES, Maina JM et al (2019) Temperature patterns and mechanisms influencing coral bleaching during the 2016 El Niño. Nat Clim Change 9:845–851. https://doi.org/10.1038/s41558-019-0576-8
Claar DC, Starko S, Tietjen KL et al (2020) Dynamic symbioses reveal pathways to coral survival through prolonged heatwaves. Nat Commun 11:6097. https://doi.org/10.1038/s41467-020-19169-y
Iglesias-Prieto R, Trench RK (1994) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density. Mar Ecol Prog Ser Oldendorf 113:163–175
Innis T, Cunning R, Ritson-Williams R et al (2018) Coral color and depth drive symbiosis ecology of Montipora capitata in Kāne‘ohe Bay, O‘ahu, Hawai‘i. Coral Reefs 37:423–430. https://doi.org/10.1007/s00338-018-1667-0
Lesser MP, Farrell JH (2004) Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23:367–377. https://doi.org/10.1007/s00338-004-0392-z
Wang C, Zheng X, Li Y et al (2022) Symbiont shuffling dynamics associated with photodamage during temperature stress in coral symbiosis. Ecol Indic 145:109706. https://doi.org/10.1016/j.ecolind.2022.109706
Lesser MP (2019) Phylogenetic signature of light and thermal stress for the endosymbiotic dinoflagellates of corals (Family Symbiodiniaceae). Limnol Oceanogr 64:1852–1863. https://doi.org/10.1002/lno.11155
Abrego D, Ulstrup KE, Willis BL, van Oppen MJH (2008) Species–specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc R Soc B Biol Sci 275:2273–2282. https://doi.org/10.1098/rspb.2008.0180
de Souza MR, Caruso C, Ruiz-Jones L et al (2022) Community composition of coral-associated Symbiodiniaceae differs across fine-scale environmental gradients in Kāne‘ohe Bay. R Soc Open Sci 9:212042. https://doi.org/10.1098/rsos.212042
Zhu W, Liu X, Zhu M et al (2023) Coastal upwelling under anthropogenic influence drives the community change, assembly process, and co-occurrence pattern of coral associated microorganisms. J Geophys Res Oceans 128:e2022JC019307. https://doi.org/10.1029/2022JC019307
Lenihan HS, Adjeroud M, Kotchen MJ et al (2008) Reef structure regulates small-scale spatial variation in coral bleaching. Mar Ecol Prog Ser 370:127–141. https://doi.org/10.3354/meps07622
Carlson RR, Li J, Crowder LB, Asner GP (2022) Large-scale effects of turbidity on coral bleaching in the Hawaiian islands. Front Mar Sci 9. https://doi.org/10.3389/fmars.2022.969472
Acknowledgements
Research was performed under all national guidelines and regulations under permit number: AA 927408.
Funding
This work was supported by Yale-NUS grants A-0007214–00-00, A0007210-00–00, and A-8001384–00-00.
Author information
Authors and Affiliations
Contributions
MSN performed data analysis and wrote the first draft. NS contributed to analysis and writing. LAR performed field work and logistics. IK performed field work and logistics. RRM performed logistics and permitting. YC draft writing. BJW conceived and designed the study, performed field and lab work, funding acquisition, permitting, logistics, writing, and data analysis. All authors approved this manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Ng, M.S., Soon, N., Afiq-Rosli, L. et al. Highly Diverse Symbiodiniaceae Types Hosted by Corals in a Global Hotspot of Marine Biodiversity. Microb Ecol 87, 92 (2024). https://doi.org/10.1007/s00248-024-02407-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00248-024-02407-x