Coral reefs are marine biodiversity hotspots that are home to 25% of known marine species (Knowlton et al., 2010). This trophic foundation of coral reefs is critically supported by the mutualistic relationship between corals and dinoflagellates in the family Symbiodiniaceae (LaJeunesse et al., 2018). Through photosynthesis, Symbiodiniaceae provide fixed carbon and nutrients essential to the coral hosts. Under stress conditions, such as an episodic increase of water temperature or declining water quality, the coral-Symbiodiniaceae symbiosis can be disrupted (i.e. the phenomenon of coral bleaching), leading to coral death, and in the extreme, potential collapse of coral reef ecosystems (Hoegh-Guldberg, 1999). Corals are under threat from warming and acidifying oceans due in part to global climate change and anthropogenic activities (Suggett and Smith, 2020). Earlier research has revealed that coral tolerance to environmental changes is linked to the coral’s natural capacity to recover and adapt, and the coral’s association with symbionts that are robust against stressors (Voolstra et al., 2021b). A coral holobiont comprises the coral animal host and the associated microbial symbionts that together sustain a functional ecological unit. A sound understanding of how these biotic components respond to stressors enables an effective assessment of coral resilience to changing environments.

Genomic data provide an excellent analysis platform for deciphering the molecular mechanisms that underpin responses to stressors in coral holobionts (Fuller et al., 2020; Rose et al., 2021; Shinzato et al., 2021; Dougan et al., 2022a). Hologenome data, or genome data generated from all interacting biotic components of a holobiont, have been proven useful for taxonomic and functional assessment of the prokaryotic microbial community in the holobionts of humans, other animals, and plants (Alberdi et al., 2022). In recent studies of coral holobionts, hologenome data are generated by sequencing genomic DNA extracted from coral tissues, enabling recovery of whole-genome sequences from the coral host, and assessment of the host genotype ( Figure 1 ); see recent reviews (Voolstra et al., 2021a; Riginos et al., 2024) for more detail. These samples are dominated by the host DNA (e.g. >90% sequenced reads derived from the coral genome) and are therefore often inadequate for the recovery of symbiont genomes at low data yield, particularly when Symbiodiniaceae genomes (1–3Gbp; (LaJeunesse et al., 2005; Saad et al., 2020) are larger than most coral genomes (<1Gbp; (Cowen and Putnam, 2022; Noel et al., 2023). For this reason, amplicon sequencing of the phylogenetic markers, e.g. the internally transcribed spacer 2 (ITS2) sequences, is commonly used for Symbiodiniaceae profiling among these samples (Hume et al., 2019; Quigley et al., 2022; Thomas et al., 2022). Although this approach is useful for characterising Symbiodiniaceae diversity, technical biases, such as primer misamplification and incomplete sampling of genetic variation, remain a challenge, calling for the use of multiple, carefully selected markers, enriched by genomic resources of Symbiodiniaceae (Davies et al., 2023).

Until recently, genomic resources of Symbiodiniaceae have been scarce, due in part to the technical challenges associated with the large genome sizes and genomic features atypical in eukaryotes (González-Pech et al., 2019; González-Pech et al., 2021; Lin et al., 2021). The advancement and increased affordability of sequencing technologies, in combination with the development of customised analytical workflows for dinoflagellate genomes (Chen et al., 2020, 2024), have empowered the development of genomic resources for Symbiodiniaceae and other dinoflagellate taxa (González-Pech et al., 2021; Dougan et al., 2023). These data have revealed remarkable sequence and structural divergence among Symbiodiniaceae genomes (Shoguchi et al., 2013; Lin et al., 2015; Aranda et al., 2016; González-Pech et al., 2021), phylogenetic diversity hidden behind subtly different morphologies (Dougan et al., 2022b; Shah et al., 2023a), and novel insights of genome evolution into how Symbiodiniaceae diversified to become symbionts that sustain coral reef health (Dougan et al., 2022a; Bhattacharya et al., 2023; Shah et al., 2023b).

Generation of these genome data thus far has been largely restricted to monoclonal cultures of Symbiodiniaceae cells isolated from (or nearby) hosts, for the ease of obtaining high-quality DNA and the need of generating high-quality genome assemblies as reference. As such, the available genomic resources represent only a small proportion of known Symbiodiniaceae diversity ( Figure 2A ). Technological challenges remain since many Symbiodiniaceae taxa, especially the host-specific taxa, are culture recalcitrant due to their narrow growth requirements (Krueger and Gates, 2012). In addition, genomes from ex hospite cell cultures may not necessarily be genetically representative of their in hospite counterparts (Maruyama et al., 2021). In this regard, coral hologenome data offer direct access to Symbiodiniaceae diversity that is more ecologically relevant, bypassing the need for cell cultures.

In this article, we review the emerging computational methods for investigating Symbiodiniaceae community of coral holobionts using hologenome datasets, and discuss how these data are useful for assessing genomic diversity and function of in hospite and/or host-specific Symbiodiniaceae.

The microbial fraction of coral hologenome data provides a snapshot of the microbial symbionts from coral populations in the wild, but this fraction is usually small (5–10%) given that these data were derived directly from coral tissue (Kitchen et al., 2019; Baums et al., 2022). Although this microbial data fraction may be perceived as “contaminant” sequences in the analysis of host genome or genotype(s), it serves as a “gold mine” that provide direct access to genome data of in hospite microbial symbionts including host-specific Symbiodiniaceae. Importantly, the use of these data bypasses the amplification of marker genes in amplicon sequencing, and thus free from technical biases associated with DNA amplification. These genome-scale data also enable the recovery of genetic information regarding functional and metabolic capacity (e.g. via encoded gene functions) of microbial symbionts, which is inaccessible using the amplicon sequencing of phylogenetic marker genes. In this regard, a robust culture-independent approach leveraging coral hologenome data is highly desirable for assessing the diversity of the symbiont community and its function in the holobiont.

Increasingly, large-scale hologenome datasets are generated from coral holobiont research. For instance, datasets were generated from hundreds of DNA samples collected across environmental gradients in a region to investigate the adaptation and speciation processes of the target coral species (Cooke et al., 2020; Fuller et al., 2020; Bongaerts et al., 2021; Rose et al., 2021; Zhang et al., 2022). Although each dataset is commonly generated by a shallow sequencing approach (e.g. 3–10× coverage of the coral genome) to maximise cost effectiveness of such studies at scale, these large number of hologenome datasets in combination enable better recovery of the coral genome, and importantly, genome data from the microbial fraction.

Host-depleted sequences from the coral hologenome data (i.e. non-coral sequence reads) are generally assumed to be derived from the microbial symbionts, from which the Symbiodiniaceae genomic reads can be retrieved bioinformatically. Here, we discuss recently adopted bioinformatic approaches used to assess Symbiodiniaceae diversity using these host-depleted coral hologenome data, which we broadly categorised as assembly-based ( Figure 1B ) and read-based approaches ( Figures 1C, D ). We discuss how these approaches complement each other, and how these approaches can be used in combination to assess Symbiodiniaceae diversity among coral holobionts relative to conditions of water quality in a case study.

The access to genome data of in hospite and/or host-specific Symbiodiniaceae remains challenging. Coral hologenome datasets present a “gold mine” for recovering genome data from the symbionts as well as the host. Although the microbial fraction remains small in each coral hologenome dataset, these datasets in large numbers may provide sufficient data yield for recovering this fraction. Importantly, the analysis of these data enables direct and more-comprehensive diversity assessment of in hospite Symbiodiniaceae. Scalable approaches, such as alignment-free read-based approaches, are key for analysing large number (e.g. >100) of datasets, thereby enabling genomic investigations of in hospite Symbiodiniaceae relative to their coral host. Integration of these genomic-scale data will provide novel insights into the biology and ecology of coral-Symbiodiniaceae partnerships (e.g. symbiosis specificity and flexibility).

The use of these approaches relies on the availability of high-quality marker genes and genomes as reference. Curated databases for symbiodiniacean marker genes thus far have been largely restricted to ITS2 (Hume et al., 2019) that is known to vary even within a genome (Thornhill et al., 2007). As more genome data from Symbiodiniaceae become available, other suitable (phylogenetic) marker genes can be identified and functionally validated. Such resources, proven useful for assessing prokaryote diversity (Chaumeil et al., 2019), will enhance our capacity in assessing Symbiodiniaceae diversity (including characterising unknown taxa), more accurately at finer resolution (Davies et al., 2023).

The development of these resources for Symbiodiniaceae will benefit from having genome-scale data from more broadly sampled taxa, both taxonomically and ecologically (Ishida et al., 2023). The integration (i.e. co-assembly) of microbial fraction of coral hologenome datasets en masse presents an innovative strategy for recovering genomes of Symbiodiniaceae taxa in hospite, which have been largely inaccessible due to the technical challenges associated with maintaining these taxa in lab cultures. Leveraging already existing coral hologenome datasets, this strategy complements other approaches that adopt more-advanced sequencing technologies and more-elaborate experimental designs yet to be optimised for Symbiodiniaceae, such as adaptive sampling sequencing (Martin et al., 2022) to enrich for microbial fraction in a metagenome/hologenome sample, and single-cell sequencing (Delmont et al., 2022) to recover genome data from DNA of a single cell.

Comparative genomic analyses of broadly sampled Symbiodiniaceae taxa will clarify the structural and functional features related to their diversification and niche specialisation. These genomic resources will facilitate other omics studies, e.g. integrating transcriptomics, proteomics, and/or metabolomics (Camp et al., 2022), to elucidate their function in a coral holobiont (Williams et al., 2023), and in deciphering the molecular regulatory mechanisms that underpin gene expression (Liew et al., 2017; Roy et al., 2018; Dougan et al., 2022a).

Due to the high cost and intricacy of coral sampling strategies associated with generating large number of coral hologenome datasets, concerted efforts through large international research consortia, e.g. the Aquatic Symbiosis Genomics Project (McKenna et al., 2021) funded by the Moore Foundation, and the Reef Adaptation and Restoration Program (McLeod et al., 2022) funded by the Australian Commonwealth Government, are essential for such an endeavour. The “gold mine” of microbial fraction from these datasets is highly valuable for research of coral symbiosis, particularly in our quest to understand how Symbiodiniaceae have diversified to sustain symbiosis with corals and other marine organisms.

HI: Conceptualization, Formal analysis, Visualization, Writing – original draft, Writing – review & editing. CR: Conceptualization, Supervision, Writing – review & editing. CXC: Conceptualization, Supervision, Visualization, Writing – review & editing.