The microbiome dynamics and interaction of endosymbiotic Symbiodiniaceae and fungi are associated with thermal bleaching susceptibility of coral holobionts

Abstract

The thermal bleaching percentage of coral holobionts shows interspecific differences under heat-stress conditions, which are closely related to the coral-associated microbiome. However, the ecological effects of community dynamics and interactions between Symbiodiniaceae and fungi on coral thermal bleaching susceptibility remain unclear. In this study, we analyzed the diversity, community structure, functions, and potential interaction of Symbiodiniaceae and fungi among 18 coral species from a high thermal bleaching risk atoll using next-generation sequencing. The results showed that heat-tolerant C3u sub-clade and Durusdinium dominated the Symbiodiniaceae community of corals and that there were no core amplicon sequence variants in the coral-associated fungal community. Fungal richness and the abundance of confirmed functional animal-plant pathogens were significantly positively correlated with the coral thermal bleaching percentage. Fungal indicators, including Didymellaceae, Chaetomiaceae, Schizophyllum, and Colletotrichum, were identified in corals. Each coral species had a complex Symbiodiniaceae-fungi interaction network (SFIN), which was driven by the dominant Symbiodiniaceae sub-clades. The SFINs of coral holobionts with low thermal bleaching susceptibility exhibited low complexity and high betweenness centrality. These results indicate that the extra heat tolerance of coral in Huangyan Island may be linked to the high abundance of heat-tolerant Symbiodiniaceae. Fungal communities have high interspecific flexibility, and the increase of fungal diversity and pathogen abundance was correlated with higher thermal bleaching susceptibility of corals. Moreover, fungal indicators were associated with the degrees of coral thermal bleaching susceptibility, including both high and intermediate levels. The topological properties of SFINs suggest that heat-tolerant coral have limited fungal parasitism and strong microbial network resilience.IMPORTANCEGlobal warming and enhanced marine heatwaves have led to a rapid decline in coral reef ecosystems worldwide. Several studies have focused on the impact of coral-associated microbiomes on thermal bleaching susceptibility in corals; however, the ecological functions and interactions between Symbiodiniaceae and fungi remain unclear. We investigated the microbiome dynamics and potential interactions of Symbiodiniaceae and fungi among 18 coral species in Huangyan Island. Our study found that the Symbiodiniaceae community of corals was mainly composed of heat-tolerant C3u sub-clade and Durusdinium. The increase in fungal diversity and pathogen abundance has close associations with higher coral thermal bleaching susceptibility. We first constructed an interaction network between Symbiodiniaceae and fungi in corals, which indicated that restricting fungal parasitism and strong interaction network resilience would promote heat acclimatization of corals. Accordingly, this study provides insights into the role of microorganisms and their interaction as drivers of interspecific differences in coral thermal bleaching.

Keywords: Symbiodiniaceae; coral holobiont; fungi; microbiome dynamics; potential interaction; thermal bleaching susceptibility.

Fig 1

Study area and sampling sites. (a) Distribution of coral reefs or communities in the SCS. The red star denotes HYI; (b) physiognomy of HYI, an isolated atoll in the eastern SCS. The yellow points represent sampling sites; (c) monthly sea surface temperatures (2012–2022). Xinyi Reef (XY; 9°20′−9°21′ N, 115°54′−115°58′ E) and Sanjiao Reef (SJ; 10°10′−10°13′ N, 115°16′−115°19′ E) are located in the Nansha Islands in the low-latitude region of the SCS. Langhua Reef (LH; 16°0′−16°5′ N, 112°26′−112°35′ E), Yuzhuo Reef (YZ; 16°18′−16°21′ N, 111°57′−112°5′ E), and Beijiao (BJ; 17°06′−17°07′ N, 111°28′−111°31′ E) are distributed in the Xisha Islands in the intermediate-latitude region of the SCS. The fringe reefs of Luhuitou (LHT; 18°12′−18°13′ N, 109°28′−109°29′ E) and Weizhou Island (WZ; 21°00′−21°04′ N, 109°04′−109°08′ E) are located in the biogeographical transition zone and subtropical climate zone, respectively, both belonging to the northern part of the SCS. Different colors indicate the results of the Dunn test post-hoc analysis.

Fig 2

The statistical result of environmental factors between outer reef slope and lagoon in of coral reef in Huangyan Island.

Fig 3

The α-diversity of Symbiodiniaceae and fungi of 18 coral species in HYI. The Chao1 richness index of (a) Symbiodiniaceae and (b) fungi of 18 species of corals in HYI; the correlation between the Chao1 richness index of (c) Symbiodiniaceae/ (d) fungi and the degree of coral susceptibility. The asterisk denotes abnormally high value of Chao1 richness index in P. verispora.

Fig 4

The community structure of Symbiodiniaceae among eighteen18 coral species in HYI in the SCS. (a) Relative abundance of genus and sub-clade of Symbiodiniaceae in 18 coral species in HYI; (b) community composition of Symbiodiniaceae of corals in HYI; (c) principal co-ordinates analysis (PCoA) of Bray–Curtis distances of Symbiodiniaceae ASV compositions associated with 18 coral species. Ellipses denote significant differences among 18 coral species [permutational multivariate analysis of variance (PERMANOVA)]; (d) the Venn diagram visualization for ubiquitous and specific Symbiodiniaceae ASV of 18 coral species; (e) abundance and enrichment characteristics of Symbiodiniaceae bio-indicator of 18 coral species in HYI based on ASV data set analyses. The blues and green rectangles denote thermally sensitive and tolerant Symbiodiniaceae sub-clades of Cladocopium, respectively, based on the results of phylogenetic analysis. The red rectangle represents heat-tolerant Symbiodiniaceae sub-clades of Durusdinium.

Fig 5

The community structure of fungi among 18 coral species in HYI in the SCS. (a) Fungal community composition for phylum, genus, and ASV levels of 18 coral species in HYI; (b) PCoA of Bray–Curtis distances of fungal compositions associated with 18 coral species. Ellipses denote significant differences among distinct coral species (PERMANOVA); (c) Venn diagram visualization for ubiquitous and specific fungal ASV of 18 coral species; (d) Abundance and enrichment characteristics of fungal bio-indicator of 18 coral species in HYI.

Fig 6

The relationship between the relative abundance of fungal pathogen function traits and coral thermal bleaching susceptibility. (a) Composition of fungi function group among coral species in HYI. The relative abundance of US, AELPW, PP, AS, AEEPS, APS, WS, PW, and AP was more than 1%; (b) There was a significantly positive correlation between the abundance of animal pathogen of fungi and coral thermal bleaching percentage (%). (c) There was a significantly positive association between the coral thermal bleaching percentage (%) and the abundance of fungal plant pathogen.

Fig 7

The correlation between the topological features of SFIN and coral bleaching susceptibility in HYI. (a) Molecular ecological interaction network of Symbiodiniaceae and fungi for 18 coral species in HYI, with co-occurrence relationships marked by edges of the network. Potential interactions of Symbiodiniaceae are denoted by red, the relationships among fungi in blue, and the co-occurrence association between Symbiodiniaceae and fungi in brown. (b) Percentage of network node for Symbiodiniaceae and fungi. (c) Correlation between complexity of SFIN and coral thermal bleaching percentage (%). (d) Relationship between betweenness centrality of SFIN and coral thermal bleaching percentage (%).