Microbiome community and complexity indicate environmental gradient acclimatisation and potential microbial interaction of endemic coral holobionts in the South China Sea
Graphical abstract
Introduction
Coral reefs are diverse symbiotic ecosystems supporting an immense biodiversity while providing important ecosystems to a wide range of living organisms, including humans (Blackall et al., 2015; Hughes et al., 2017). However, coral reefs transitioning through the Anthropocene (Hughes et al., 2017) must contend with climate change, often undergoing configurational transformations caused by rising temperatures (Hughes et al., 2018; Stuart-Smith et al., 2018). The collapse of coral reefs that has occurred since the 1970s has largely been attributed to climate change, which has caused the coral cover to significantly decline by approximately 50–80% worldwide (Gardner et al., 2003; Bruno and Selig, 2007; Silverstein et al., 2015; Hughes et al., 2018). Biogeographical evidence showed that the global coral recruitment has declined by 85% throughout the tropics, but has increased by 78% in the sub-tropics (Price et al., 2019). Several studies have suggested that in some areas, such as eastern Australia (Booth et al., 2007; Figueira and Booth, 2010), Japan (Yamano et al., 2011), the western Mediterranean (Serrano et al., 2013), and the northern part of the South China Sea (SCS) (Tkachenko and Soong, 2017; Qin et al., 2019a, Qin et al., 2019b; Yu et al., 2019), sub-tropical coral reefs may be potential zones of refuge for tropical coral resisting the oceans' increasing temperatures (Beger et al., 2014). Studies on environmental tolerance and acclimatisation of dominant tropical and sub-tropical coral species are essential for assessing the environmental gradient acclimatisation of coral coping with climate change.
The environmental tolerance of coral are closely associated with coral host and microbiome, which includes endosymbiotic Symbiodiniaceae, bacteria, viruses, fungi, and archaea (Hernandez-Agreda et al., 2017; Brener-Raffalli et al., 2018; Osman et al., 2020). The coral host has a dynamic relationship with these diverse partners, collectively termed the coral holobiont (Brener-Raffalli et al., 2018). Certain corals adapt to different environmental stresses by restructuring their microbiome (particularly the structures of the Symbiodiniaceae and bacteria) (McDevitt-Irwin et al., 2017; LaJeunesse et al., 2018; Ziegler et al., 2019). Symbiodiniaceae, originated and diversified approximately 140–200 million years ago (coinciding with the adaptive radiation of calcifying corals during the middle Jurassic Period) (Simpson et al., 2011; LaJeunesse et al., 2018), have an abundant taxa with distinct eco-physiological and environmental tolerance (Lajeunesse et al., 2010; LaJeunesse et al., 2018; Chen et al., 2019a, Chen et al., 2019b; Qin et al., 2019a, Qin et al., 2019b). Several corals can adapt to new environmental regimes by shuffling or switching their Symbiodiniaceae (Baker et al., 2004; Fabricius et al., 2004; Stat et al., 2006). For example, the heat-tolerant Durusdinium trenchii is frequently involved in coral switching and shuffling adjustments in natural reefs (Pettay et al., 2015), contributing to the survival of the endangered Orbicella faveolata during thermal bleaching in the Florida Keys in 2015 (Manzello et al., 2018). In addition, bacterial communities influence the acclimatisation and adaptation of holobionts to environmental regime or stress responses (Ziegler et al., 2017; Ziegler et al., 2019). Several studies have reported that distinct bacterial communities can help coral respond to sea surface temperature (SST) variations (Ziegler et al., 2017; Brener-Raffalli et al., 2018; Osman et al., 2020), eutrophication (Ziegler et al., 2016; Ziegler et al., 2019), high turbidity (Ziegler et al., 2016), and low pH (Morrow et al., 2014). Corals also have symbiotic relationship with several beneficial bacteria, which can protect against pathogen invasion by secreting antibiotics (Ritchie, 2006; Rypien et al., 2010), inhibiting pathogen metabolism (Ritchie, 2006; Rypien et al., 2010), or consuming the pathogens itself (Welsh et al., 2015). Coral holobionts also have a core bacterial microbiome (present in 30 to 100% of the individuals of a coral species) that is associated with improved environmental adaptation and ecological function of the holobiont (Hernandez-Agreda et al., 2016; Brener-Raffalli et al., 2018). Core bacterial microbiomes have high specificities (Hernandez-Agreda et al., 2017; Hernandez-Agreda et al., 2018); thus, variation in the abundance of core microbiomes provides an insight into the adaptive strategy of coral holobionts in response to environmental stress in different habitats. Therefore, knowing the endosymbiotic Symbiodiniaceae and bacterial community structure, along with its variations, is critical to understand the coral holobiont acclimatisation toward distinct environmental regimes and the tolerance of corals to climate change.
Coral microbial communities not only affect the acclimatisation and immune response of the coral host (van Oppen and Blackall, 2019) but also interact with each other. The results of fluorescence in situ hybridisation (FISH) analyses showed that Actinobacter and Ralstonia have a close relationship with Symbiodiniaceae (Ainsworth et al., 2015). While other studies found that Endozoicomonas can protect Symbiodiniaceae from bleaching pathogens (Pantos et al., 2015; Neave et al., 2017). Altermonas and Cyanobacteria also provide nitrogen to the Symbiodiniaceae of coral larvae (Lesser et al., 2004; Ceh et al., 2013). Previous studies have reported that microbiomes are highly structured and form complex interconnected microbial networks in which microbes associate with each other either directly or indirectly through processes such as competition, facilitation, and inhibition (Barberán et al., 2012; Wagg et al., 2019; Chen et al., 2020). However, the drivers of potential Symbiodiniaceae-bacteria interactions (SBIs) and their association with microbial diversity remain unknown. This information helps to assess the symbiosis stability and acclimatisation of coral holobionts.
The SCS is on the northern edge of the ‘Coral Triangle’ (Spalding, 2001). Tropical atolls are widely distributed from the Zengmu Reef, (~4° N) near the equator, to the Dongsha Islands, (~20° N) in the northern SCS (Yu, 2012; Tkachenko and Soong, 2017; Chen et al., 2020). Several fringe reefs and coral communities are distributed along the northern edge of the SCS in sites including the Leizhou Peninsula (~20–21° N), Hong Kong (~21–22° N), and Dongshan Island (~23° N), and their distribution is controlled by the sub-tropical climate (Chen et al., 2009; Ng and Ang, 2016; Chen et al., 2019a, Chen et al., 2019b). The SCS covers 19 degrees of latitude, and corals throughout the SCS are exposed to environmental effects of not only different latitudinal gradients but also different climate zones (tropical and sub-tropical; Yu, 2012). Due to the Qiongdong cold upwelling, the eastern region of Hainan Island (18° 30′–20° 30′ N) exhibits sub-tropical features, including an increase in macroalgae cover (Chen et al., 2019a, Chen et al., 2019b) and sub-tropical coral species (Wu et al., 2013). Thus, the eastern region of Hainan Island can be defined as a biogeographical transition zone (BTZ), which is likely to become a refuge for tropical corals avoiding thermal stress (Beger et al., 2014). Moreover, investigating the genetic flow of coral hosts (Porites lutea, Galaxea fascicularis) highlights a high northern migration rate in the SCS (Su, 2017; Huang et al., 2018). Therefore, the SCS provides a suitable natural environment for studying the microbiome-driven latitudinal and climatic acclimatisation of coral holobionts associated with host's phylogeny.
This study aimed to explored the community structures of Symbiodiniaceae and bacteria associated with two endemic dominant coral species, namely Pocillopora verrucosa and Turbinaria peltate, collected from 15 coral habitats across 14 degrees of latitude. We characterised the latitudinal and climatic environmental factors to determine how microbial communities are linked to distinct environmental regimes and explained the associations between coral acclimatisation and microbial community shifts. Furthermore, network modelling inference was used to analyse the microbial co-occurrence network, which helps to explore potential SBIs and their key drivers in the coral holobionts. The results of this study will expand our understanding of the symbiosis stability and flexibility, acclimatisation, and potential microbial interactions of coral holobionts in response to global climate change.
Section snippets
Sample collection, coral cover, and environmental characteristics
One hundred seventy-five tropical dominant Pocillopora verrucosa samples were collected from tropical coral habitats (TCH) and BTZ in the SCS (Table 1), and 44 sub-tropical dominant Turbinaria peltata samples were collected from three coral communities in the northern part of the SCS (Table 1). Only adult coral colonies were collected to control for the effect of age on microbiota composition (van Oppen and Blackall, 2019). Coral fragments (~2–3 cm2) were obtained by hammer and chisel from a
Regional environmental differences and coral cover
Statistical analysis of the environmental index (NASA Giovanni satellite 2009–2019) revealed that the SST, Chl a, and Kd differed across coral habitats in the SCS (Figs. 1 and S1). The SST varied appreciably along the latitudinal gradient and decreased with increased latitude. Significant differences were observed in the SST among the HLCC (DS, DY and WZ, range from 23.06 ± 4.273C to 25.8 ± 4.300 °C), BTZ (DZ, 27.238 ± 2.342 °C), ILCR (BJ, QIY, YX, DD, HG, PS, and LH, range from 27.867 ± 1.796
Symbiodiniaceae community structure of coral holobionts is linked to latitudinal environmental regimes in the SCS
Results of the environmental factor analysis showed that variation in SST was associated with changes in the latitudinal gradient, which corresponded to the shifts in the Symbiodiniaceae community structures (Fig. 1, Fig. 3). These results suggest that Symbiodiniaceae communities of P. verrucosa have strong geographical patterns in distinct latitudinal environmental regimes, which may be shaped by SST. Many other studies have similarly found that the spatial distribution pattern of the
Conclusions
Our study reveals distinctive characteristics of microbiome acclimatisation for two endemic coral species in the SCS. The Symbiodiniaceae community structure of tropical dominant P. verrucosa was linked to latitudinal environmental regimes in the SCS; meanwhile, the acclimatisation of coral-Symbiodiniaceae symbioses was primarily driven by SST with latitudinal gradient shifts. However, bacteria communities showed high flexibility in BTZ, which may be associated with high turbidity and SST
Funding
This work was supported by the National Natural Science Foundation of China [Nos. 42030502 and 91428203]; the Guangxi Scientific Projects [Nos. AD17129063 and AA17204074]; the BaGui Scholars Program Foundation [No. 2014BGXZGX03]; and the Innovation Project of Guangxi Graduate Education [No. YCBZ2018006].
CRediT authorship contribution statement
Biao Chen: Conceptualization, Methodology, Resources, Data curation, Visualization, Validation, Writing - original draft. Kefu Yu: Conceptualization, Resources, Methodology, Validation, Writing - review & editing, Project administration, Funding acquisition. Zhiheng Liao: Software, Formal analysis, Visualization, Writing - review & editing. Xiaopeng Yu: Software, Formal analysis, Visualization, Writing - review & editing. Zhenjun Qin: Software, Formal analysis, Visualization, Writing - review &
Declaration of competing interest
The authors declare that they have no competing interests.
Acknowledgements
We thank Zhixian Li for improving the quality of the English writing.
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