Spatial Changes Of Coral Microbiome And Environmental Adaptation Mechanism In The South China Sea

It is a scientific frontier issue that whether coral reef ecosystems can adapt to climate change and anthropogenic activities in the world.In this study,diverse coral species and their microbiome(Symbiodiniaceae,bacteria and virus)in coral reef(or coral communities;Fangchenggang,Daya Bay and Dongshan Island have not developed into extensive coral reefs in the northern South China Sea,which are defined as coral communities)from distinct latitudinal gradients or climatic zones in the South China Sea(SCS)were obtained,which were used to explore spatial changes of coral microbiome and environmental adaptation mechanism in the SCS.Thus,several important issues were planed to reveal:(1)The spatial distribution pattern of the microbiome in coral reefs water in the SCS;(2)The spatial distribution and phylogenetic pattern of coral endosymbiotic Symbiodiniaceae in the SCS;(3)The spatial variation rule of ubiquitous coral microbiome in the SCS;(4)The spatial change rule of endemic coral microbiome in the SCS;(5)The dispersal and genetic variation of heat-tolerant Symbiodiniaceae in the SCS;(6)The community composition and function characteristics of coral virus community in the relatively high latitude region in the SCS.The study area covers 16 latitudes(7°-23°N),two climatic zones(tropic and subtropic),four ecological zones and 20 coral reefs/communities[High latitude coral Reef/community(HLCC):Dongshan Island,Daya Bay,Leizhou Peninsula,Fangchenggang,Weizhou Island;Biogeographical transition zone(BTZ):Dazhou Island,Luhuitou;Intermediate latitude coral reefs(ILCR):Beijiao,Qilianyu,Yongxing Island,Dong Island,Yuzhuo Reef,Huangguang Reef,Panshiyu,Langhua Reef;Low latitude coral reefs(LLCR):Huangyan Island,Sanjiao Reef,Huayang Reef,Xian'e Reef,Xinyi Reef;].The study analyzed the ecological survey data,environmental factors,coral reef water microbiome,coral endosymbiotic microbiome and population genetic characteristics of heat-tolerant Symbiodiniaceae,and have several main conclusions:(1)Microbiome in coral reef water can affect the environmental adaptability and health condition of corals by having symbioses or parasitism with corals in the SCS.The Symbiodiniaceae communities composition in coral reef water have significant difference among distinct latitudinal gradients,which were dominated by Symbiodinium(34.2±21.4%),Cladocopium(31.1±24.2%),Breviolum(12.6±16.8%),Durusdinium(4.5±10.0%).These Symbiodiniaceae will provide abundant endosymbiotic symbionts to coral hosts with heat-based physiological trauma and improve the environmental adaptability and resilience of corals.Moreover,The bacterial communities composition also have significant difference among distinct latitudinal gradients,which have close associations with environmental factor,coral disease and water pollution.The Erythrobacter was enriched in bacterial community in coral reef water from HLCC,which may assist coral to adapt to high nutrient concentration and turbidity;The Oceanospirillum showed enrichment characteristic in bacterial community in coral reef water from ILCR,which can improve the symbioses stability and disease resistance of coral;Halomona and Cyanobacteria were enriched in bacterial community in coral reef water from LLCR,which may help coral to adapt to heat stress and coral disease.In addition,phage and Circoviridae were enriched in virus community in the subtropical coral reefs/communities water,which may increase the risk of coral disease and decrease the environmental adaptability of coral.In contrast,virus community enrich Herpesviridae and Mimiviridae in the tropical coral reefs water,and these viruses have potential to hasten the collapse of coral-Symbiodiniaceae symbioses in thermal condition.(2)The ? -diversity,community composition and phylogenetic pattern of endosymbiotic Symbiodiniaceae have close associations with latitudinal environment change in the SCS.The ? diversity of Symbiodiniaceae in ILCR and LLCR was significantly higher than that in HLCC,which was affected by geographical isolation(geographical distance)and environmental factors(temperature,nutrient concentration and turbidity)together.This result supports the“center of origin hypothesis”for coral and its endosymbiotic Symbiodiniaceae in the SCS.Moreover,the major dominant Symbiodiniaceae genus shift from Cladcopium in HLCC to Cladcopium+Durusdinium in ILCR and LLCR in the SCS,and the relative abundance of heat-tolerant Symbiodiniaceae sub-clades(D1,C15 and C3u)was increased with latitudes decline.This result indicated that latitudinal temperature change was the main reason for the spatial difference of Symbiodiniaceae community composition.The result of phylogenetic analysis showed that the sub-clades have a close phylogenetic relationship with C1,which was mainly distributed in HLCC.The relative abundance of these sub-clades was negatively correlated with temperature,light intensity,salinity,and was positively correlated with nutrient concentration and turbidity.In contrast,the sub-clades have a close phylogenetic relationship with C3,which was mainly distributed in ILCR and LLCR,the relative abundance trend of these sub-clades showed the opposite pattern to the C1 group.Therefore,the symbionts of Cladocopium,which shared common ancestors,show similar environmental adaptability.(3)There are significantly spatial differences in community composition,functions characteristics and interaction of microbiome in ubiquitous Galaxea fascicularis from the SCS.Heat-tolerant Durusdinium trenchii dominate in Symbiodiniaceae communities of G.fascicularis in tropical coral reefs(65.6±37.5%),which supports that corals have strong heat tolerance.However,C1 sub-clade has high abundance in Symbiodiniaceae community in subtropical coral communities(80.6±2.3%),which may assist coral to adapt to environmental stress with low temperature,high nutrient concentration and high turbidity.The result of Symbiodiniaceae interaction network suggested that D.trenchii was a key species in symbiont interaction network,which can improve stability of coral-Symbiodiniaceae symbioses by inhibiting parasitic symbionts.In contrast,C1 was not involved in the symbiont interaction network.Moreover,the symbiotic bacteria communities of G.fascicularis have high evenness in LLCR and enriched ? -proteobacteria that associated high temperature,which indicated that G.fascicularis has strong heat tolerance in this region.Nevertheless,Cyanobacteria showed enrichment characteristic in the symbiotic bacteria communities of G.fascicularis in HLCC and BTZ,which may assist coral to respond to turbidity stress by providing nitrogen and remedying photosynthesis.In addition,the core bacterial microbiota of G.fascicularis was dominated by pathogenic bacteria,such as Rhodobacteraceae,Vibrio,Sphingomonas,which may increase the risk of coral disease while reduce coral environmental adaptability.(4)There are significantly spatial differences in community composition and functions characteristics of microbiome in tropical endemic dominant Pocillopora verrucosa and subtropical endemic dominant Turbinaria peltata.Heat-tolerant sub-clades D1(71.8±16.1%)and D6(23.9±4.7%)were dominated in Symbiodiniaceae community in P.verrucosa in LLCR,and the abundance of these sub-clades decreases with the increase of latitudes,which indicated that P.verrucosa adapt to thermal stress by having symbiotic with more heat-tolerant Symbiodiniaceae.However,the Symbiodiniaceae community of T.peltata was spatial homogeneous,which was dominated by C1 sub-clade(61.1±8.8%).In addition,the symbiotic bacterial communities of P.verrucosa were dominated by beneficial bacteria Ralstonia in tropical coral reefs,and have stable community composition,which can significantly improve the environmental adaptability of coral.In contrast,P.verrucosa can inhibit coral pathogenic bacteria by increasing the abundance of beneficial bacteria in BTZ,which may improve adaptive capacity of coral to respond to high turbidity and temperature fluctuation.For T.peltata,the bacterial communities of this coral have high flexibility,which links to changing and fluctuating environment in subtropical coral reefs or communities.Moreover,bacterial taxa associated with anthropogenic activity(Escherichia coli and Sphingomonas)were identified in the core bacterial microbiota,which may indicate that large-scale potential anthropogenic disturbances have affected coral habitats in the SCS.(5)The thermal tolerance of coral has close associations with large-scale dispersal,genetic variation and genetic diversity of heat-tolerant D.trenchii in the SCS.Southwest monsoon-driven current may promote the long-distance northward dispersal of D.trenchii that originate from LLCR in the SCS,which can provide source of heat-tolerant symbionts to corals from IICR,BTZ and HLCC.The results of STRUCTURE and genetic variation index(?_PT)analysis showed that the genetic variations in D.trenchii between LLCR and IICR-BTZ inside the SCS may be shaped by sea surface temperature(SST)latitudinal change.In addition,heat-tolerant D.trenchii have high genetic diversity in large spatial scale in the SCS(clone richness:0.85-1.00),which can avoid the negative ecological effects caused by D.trenchii with a single genotype associated with the coral host,and improved thermal adaptability of corals.(6)The community composition,function characteristic and host diversity of virus can directly affect the health condition and environmental adaptability of corals in HLCC.The results of virome of G.fascicularis in the subtropical Daya Bay in the SCS suggested that the members of nucleocytoplasmic large DNA viruses(NCLDVs)have potential to infect endosymbiotic Symbiodiniaceae,and decrease the stability of coral-symbiodiniaceae symbioses in low temperature.The results of phage host prediction found that phage can infect a variety of beneficial bacteria,pathogenic bacteria and opportunistic bacteria inside coral,which will affect the stability and environmental adaptability of coral by changing the dynamic balance,immune response and nutrient cycling of coral-bacteria symbioses.In addition,the functional enrichment characteristic found that viruses can regulate the primary productivity and symbiont horizontal transmission by infecting phytoplankton and Symbiodiniaceae in subtropical coral reef water,respectively.However,phages in coral tissue may affect the environmental adaptability of coral by enhancing the metabolism of the coral symbiotic bacteria through active lysogeny.(7)The ? diversity and community composition of coral microbiome have four spatial change patterns in the SCS:latitude change pattern,climate change pattern,homogenization pattern and heterogenization pattern.The Symbiodiniaceae and bacteria in coral microbiome have diverse community composition and functions,and also have significant spatial difference in the SCS.These characteristics will enhance the adaptability of coral to respond to distinct environmental stress.Although,the studies of virus only were conducted in coral reef water in the SCS and coral in Daya Bay,the results of composition and function of virus suggested that the impact of virus on the health condition and environmental adaptability of corals was negative.This study analyzed the spatial variation rule of the coral microbiome in the SCS,and has reveled the environmental adaptiation mechanism of the coral holobiont to cope with climate change and anthropogenic disturbance from the perspective of the microbiome.