Microbiome community and complexity indicate environmental gradient acclimatisation and potential microbial interaction of endemic coral holobionts in the South China Sea

https://doi.org/10.1016/j.scitotenv.2020.142690Get rights and content

Highlights

  • Coral microbial communities are linked to latitudinal/climatic environmental regime.

  • Core microbiome abundance change may lead to microbiota function variation.

  • Anthropogenic bacteria in core microbiome suggest large-scale human activity.

  • Microbial α diversity is closely associated with co-occurrence network complexity

  • Potential SBI may be driven by Cladocopium, γ-proteobacteria, and α-proteobacteria.

Abstract

Regional acclimatisation and microbial interactions significantly influence the resilience of reef-building corals facing anthropogenic climate change, allowing them to adapt to environmental stresses. However, the connections between community structure and microbial interactions of the endemic coral microbiome and holobiont acclimatisation remain unclear. Herein, we used generation sequencing of internal transcribed spacer (ITS2) and 16S rRNA genes to investigate the microbiome composition (Symbiodiniaceae and bacteria) and associated potential interactions of endemic dominant coral holobionts (Pocillopora verrucosa and Turbinaria peltata) in the South China Sea (SCS). We found that shifts in Symbiodiniaceae and bacterial communities of P. verrucosa were associated with latitudinal gradient and climate zone changes, respectively. The C1 sub-clade consistently dominated the Symbiodiniaceae community in T. peltata; yet, the bacterial community structure was spatially heterogeneous. The relative abundance of the core microbiome among P. verrucosa holobionts was reduced in the biogeographical transition zone, while bacterial taxa associated with anthropogenic activity (Escherichia coli and Sphingomonas) were identified in the core microbiomes. Symbiodiniaceae and bacteria potentially interact in microbial co-occurrence networks. Further, increased bacterial, and Symbiodiniaceae α-diversity was associated with increased and decreased network complexity, respectively. Hence, Symbiodiniaceae and bacteria demonstrated different flexibility in latitudinal or climatic environmental regimes, which correlated with holobiont acclimatisation. Core microbiome analysis has indicated that the function of core bacterial microbiota might have changed in distinct environmental regimes, implying potential human activity in the coral habitats. Increased bacterial α diversity may lead to a decline in the stability of coral-microorganism symbioses, whereas rare Symbiodiniaceae may help to retain symbioses. Cladocopium, γ-proteobacteria, while α-proteobacteria may have been the primary drivers in the Symbiodiniaceae-bacterial interactions (SBIs). Our study highlights the association between microbiome shift in distinct environmental regimes and holobiont acclimatisation, while providing insights into the impact of SBIs on holobiont health and acclimatisation during climate change.

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.

n

References (119)

  • C. Arif et al.

    Assessing Symbiodinium diversity in scleractinian corals via next-generation sequencing-based genotyping of the ITS2 rDNA region

    Mol. Ecol.

    (2014)
  • A.C. Baker et al.

    Coral reefs: corals' adaptive response to climate change

    Nature

    (2004)
  • D.M. Baker et al.

    Nitrate competition in a coral symbiosis varies with temperature among Symbiodinium clades

    ISME J.

    (2013)
  • A.L. Barabási et al.

    Network biology: understanding the cell’s functional organization

    Nat. Rev. Genet.

    (2004)
  • A. Barberán et al.

    Using network analysis to explore co-occurrence patterns in soil microbial communities

    ISME J.

    (2012)
  • M. Beger et al.

    Conserving potential coral reef refuges at high latitudes

    Divers. Distrib.

    (2014)
  • Y. Benjamini et al.

    Controlling the fals ediscovery rate:a practical and powerful approach to multiple testing

    J. R. Stat. Soc. Ser. B Methodol.

    (1995)
  • L.L. Blackall et al.

    Coral-the world's most diverse symbiotic ecosystem

    Mol. Ecol.

    (2015)
  • E. Bolyen et al.

    Author correction: reproducible, interactive, scalable and extensible microbiome data science using QIIME 2

    Nat. Biotechnol.

    (2019)
  • A.J. Boucot

    The complexity and stability of ecosystems

    Nature

    (1985)
  • N.M. Boulotte et al.

    Exploring the Symbiodinium rare biosphere provides evidence for symbiont switching in reef-building corals

    ISME J.

    (2016)
  • D. Bourne et al.

    Changes in coral-associated microbial communities during a bleaching event

    ISME J

    (2008)
  • K. Brener-Raffalli et al.

    Thermal regime and host clade, rather than geography, drive Symbiodinium and bacterial assemblages in the scleractinian coral Pocillopora damicornis sensu lato

    Microbiome

    (2018)
  • M.B. Brown

    400: a method for combining non-independent, one-sided tests of significance

    Biometrics

    (1975)
  • J.F. Bruno et al.

    Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons

    PLoS One

    (2007)
  • J. Ceh et al.

    Nutrient cycling in early coral life stages: Pocillopora damicornis larvae provide their algal symbiont (Symbiodinium) with nitrogen acquired from bacterial associates

    Ecol. Evol

    (2013)
  • T. Chen et al.

    Twenty-five years of change in scleractinian coral communities of Daya bay (northern South China Sea) and its response to the 2008 AD extreme cold climate event

    Sci. Bull.

    (2009)
  • X. Chen et al.

    Atmospheric nitrogen deposition increases the possibility of macroalgal dominance on remote coral reefs

    J. Geophys. Res. Biogeosci.

    (2019)
  • B. Chen et al.

    Latitudinal variation in the molecular diversity and community composition of Symbiodiniaceae in coral from the South China Sea

    Front. Microbiol.

    (2019)
  • A.W. Coleman et al.

    Molecular delineation of species and syngens in Volvocacean green algae (Chlorophyta)

    J. Phycol.

    (2010)
  • J.Y. Ding et al.

    Genomic insight into the host–Endosymbiont relationship of Endozoicomonas montiporae CL-33T with its coral host

    Front. Microbiol.

    (2016)
  • S. English et al.

    Survey Manual for Tropical Marine Resources

    (1997)
  • N.S. Fabina et al.

    Symbiotic specificity, association patterns, and function determine community responses to global changes: defining critical research areas for coral-Symbiodinium symbioses

    Glob. Chang. Biol.

    (2013)
  • K.E. Fabricius et al.

    Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories

    Mol. Ecol.

    (2004)
  • K. Faust et al.

    Microbial co-occurrence relationships in the human microbiome

    PLoS Comput. Biol.

    (2012)
  • W.F. Figueira et al.

    Increasing ocean temperatures allow tropical fishes to survive overwinter in temperate waters

    Glob. Chang. Biol.

    (2010)
  • J.C. Finney et al.

    The relative significance of host–habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium

    Microb. Ecol.

    (2010)
  • M.R. Gaither et al.

    Preservation of corals in salt-saturated DMSO buffer is superior to ethanol for PCR experiments

    Coral Reefs

    (2011)
  • T.A. Gardner et al.

    Long-term region-wide declines in Caribbean corals

    Science

    (2003)
  • F.E.J. Harrell

    Hmisc: harrell miscellaneous

    R Package Version.

    (2008)
  • A. Hernandez-Agreda et al.

    The microbial signature provides insight into the mechanistic basis of coral success across reef habitats

    mBio

    (2016)
  • A. Hernandez-Agreda et al.

    Rethinking the coral microbiome: simplicity exists within a diverse microbial biosphere

    mBio

    (2018)
  • W. Huang et al.

    Genetic diversity and large-scale connectivity of the scleractinian coral Porites lutea in the South China Sea

    Coral Reefs

    (2018)
  • T.P. Hughes et al.

    The wicked problem of China’s disappearing coral reefs

    Conserv. Biol.

    (2013)
  • T.P. Hughes et al.

    Coral reefs in the Anthropocene

    Nature

    (2017)
  • T.P. Hughes et al.

    Spatial and temporal patterns of mass bleaching of corals in the Anthropocene

    Science

    (2018)
  • B.C.C. Hume et al.

    Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world's hottest sea, the Persian/Arabian Gulf

    Sci. Rep.-UK

    (2015)
  • C. Jessen et al.

    In-situ effects of eutrophication and overfishing on physiology and bacterial diversity of the red sea coral Acropora hemprichii

    PLoS One

    (2013)
  • A. Jousset et al.

    Where less may be more: how the rare biosphere pulls ecosystems strings

    ISME J.

    (2017)
  • E.V. Kennedy et al.

    Symbiodinium biogeography tracks environmental patterns rather than host genetics in a key Caribbean reef-builder, Orbicella annularis

    P. Roy. Soc. B-Biol.

    (2016)
  • Cited by (32)

    View all citing articles on Scopus
    View full text