Abstract
Variously shaped corals, such as branching and massive corals, exhibit divergent environmental susceptibility properties. The susceptibility potential of these corals may be regulated by specific symbiotic Symbiodiniaceae and bacteria. In this study, we investigated seawater characteristics between the north and south zones at the Wuzhizhou Island (WZZ), sampled branching coral Acropora hyacinthus, lamellar coral Montipora informis, and massive coral (Galaxea fascicularis and Porites lutea). Physiological characteristics were measured, and amplicon sequencing was performed to Symbiodiniaceae and bacterial community structure analysis. Corals experienced severe anthropogenic disturbance, with more than 1.4-fold increase in DIN, including \({{\text{NH}}}_{4}^{+}\), \({{\text{NO}}}_{3}^{-}\), and \({{\text{NO}}}_{2}^{-}\) in the north of the WZZ Island compared to the southern region. However, massive corals (G. fascicularis and P. lutea) showed relatively less disruption in both their symbiont composition and physiological responses. Notably, M. informis displayed distinct variations, with disturbances in the northern region resulted in a decline in the density of symbiotic micro-algae associated with Cladocopium sp. C26 due to elevated concentrations of ammonium and nitrate. The four coral species hosted different symbionts within the same area. P. lutea hosted Cladocopium sp. C15 with the lowest density of symbiotic micro-algae, along with the lowest Fv/Fm and YII values compared to other corals in the southern zone. G. fascicularis exhibited high abundance of Durusdinium sp. D1 and D4, which showed strong correlation with Fv/Fm. In southern M. informis, Cladocopium sp. C26 was identified as the predominant symbiotic micro-algae that displayed a significant positive correlation with YII. The bacterial community composition and metabolism functional attribution predicted by PICRUSt differed between A. hyacinthus, M. informis, and massive corals (G. fascicularis, P. lutea). Comprehensive analysis revealed different susceptibility properties among branching, lamellar, and massive corals under anthropogenic disturbance associated with changes in Symbiodiniaceae and bacterial community.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The raw sequence data reported in this paper have been deposited in the Genome Sequence Archive (Genomics, Proteomics & Bioinformatics 2021) (Chen et al. 2021) in National Genomics Data Center (Nucleic Acids Res 2022) (Members and Partners 2022), China National Center for Bioinformation / Beijing Institute of Genomics, Chinese Academy of Sciences (CRA009587, CRA009588) that are publicly accessible at https://ngdc.cncb.ac.cn/gsa.
Abbreviations
- ASV:
-
Amplicon sequence variant
- DIN:
-
Dissolved inorganic nitrogen
- KO:
-
KEGG ortholog
- NMDS:
-
Non-metric multidimensional scaling
- OTU:
-
Operational taxonomic unit
- PcoA:
-
Principal coordinates analysis
- WZZ:
-
Wuzhizhou
References
Au AC, Zhang L, Chung SS, Qiu JW (2014) Diving associated coral breakage in Hong Kong: differential susceptibility to damage. Mar Pollut Bull 85(2):789–796. https://doi.org/10.1016/j.marpolbul.2014.01.024
Bernasconi R, Stat M, Koenders A, Huggett MJ (2018) Global networks of Symbiodinium-bacteria within the coral holobiont. Microb Ecol 77(3):794–807. https://doi.org/10.1007/s00248-018-1255-4
Bourne DG, Morrow KM, Webster NS (2016) Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu Rev Microbiol 70:317–340. https://doi.org/10.1146/annurev-micro-102215-095440
Carballo-Bolanos R, Denis V, Huang YY, Keshavmurthy S, Chen CA (2019) Temporal variation and photochemical efficiency of species in Symbiodinaceae associated with coral Leptoria phrygia (Scleractinia; Merulinidae) exposed to contrasting temperature regimes. PLoS ONE 14(6):e0218801. https://doi.org/10.1371/journal.pone.0218801
Chen S, Zhou Y, Chen Y, Gu J (2018) Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34(17):i884–i890. https://doi.org/10.1093/bioinformatics/bty560
Chen B, Yu K, Qin Z, Liang J, Wang G, Huang X, Wu Q, Jiang L (2020) Dispersal, genetic variation, and symbiont interaction network of heat-tolerant endosymbiont Durusdinium trenchii: Insights into the adaptive potential of coral to climate change. Sci Total Environ 723:138026. https://doi.org/10.1016/j.scitotenv.2020.138026
Chen T, Chen X, Zhang S, Zhu J, Tang B, Wang A, Dong L, Zhang Z, Yu C, Sun Y, Chi L, Chen H, Zhai S, Sun Y, Lan L, Zhang X, Xiao J, Bao Y, Wang Y, Zhang Z, Zhao W (2021) The genome sequence archive family: toward explosive data growth and diverse data types. Genom Proteom Bioinf 19(4):578–583. https://doi.org/10.1016/j.gpb.2021.08.001
Claar DC, McDevitt-Irwin JM, Garren M, Vega Thurber R, Gates RD, Baum JK (2020a) Increased diversity and concordant shifts in community structure of coral-associated Symbiodiniaceae and bacteria subjected to chronic human disturbance. Mol Ecol 29(13):2477–2491. https://doi.org/10.1111/mec.15494
Claar DC, Starko S, Tietjen KL, Epstein HE, Cunning R, Cobb KM, Baker AC, Gates RD, Baum JK (2020b) Dynamic symbioses reveal pathways to coral survival through prolonged heatwaves. Nat Commun 11:6097. https://doi.org/10.1038/s41467-020-19169-y
de Souza MR, Caruso C, Ruiz-Jones L, Drury C, Gates R, Toonen RJ (2022) Community composition of coral-associated Symbiodiniaceae differs across fine-scale environmental gradients in K’ne’ohe Bay. R Soc Open Sci 9(9):212042. https://doi.org/10.1098/rsos.212042
Doney SC (2010) The growing human footprint on coastal and open-ocean biogeochemistry. Science 328(5985):1512–1516. https://doi.org/10.1126/science.1185198
Edgar RC (2013) UPARSE: highly accuraIOTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998. https://doi.org/10.1038/nmeth.2604
Fabricius KE, Cooper TF, Humphrey C, Uthicke S, De’ath G, Davidson J, LeGrand H, Thompson A, Schaffelke B (2012) A bioindicator system for water quality on inshore coral reefs of the great barrier reef. Mar Pollut Bull 65(4–9):320–332. https://doi.org/10.1016/j.marpolbul.2011.09.004
Fisher PL, Malme MK, Dove S (2011) The effect of temperature stress on coral—Symbiodinium associations containing distinct symbiont types. Coral Reefs 31(2):473–485. https://doi.org/10.1007/s00338-011-0853-0
Ge R, Liang J, Yu K, Chen B, Yu X, Deng C, Chen J, Xu Y, Qin L (2021) Regulation of the coral-associated bacteria and symbiodiniaceae in Acropora valida under ocean acidification. Front Microbiol 12:767174. https://doi.org/10.3389/fmicb.2021.767174
Gong S, Chai G, Xiao Y, Xu L, Yu K, Li J, Liu F, Cheng H, Zhang F, Liao B, Li Z (2018) Flexible symbiotic associations of symbiodinium with five typical coral species in tropical and subtropical reef regions of the northern south China Sea. Front Microbiol 9:2485. https://doi.org/10.3389/fmicb.2018.02485
Grottoli AG, Warner ME, Levas SJ, Aschaffenburg MD, Schoepf V, McGinley M, Baumann J, Matsui Y (2014) The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob Chang Biol 20(12):3823–3833. https://doi.org/10.1111/gcb.12658
Heru K, Chitrasak K, Matanee P, Suppakarn J, Kobchai P, Jamal O, Suchana C, Voranop V, Naraporn S (2021) Microbiomes of healthy and bleached corals during a 2016 thermal bleaching event in the upper gulf of Thailand. Front Mar Sci. https://doi.org/10.3389/fmars.2021.643962
Hochart C, Paoli L, Ruscheweyh HJ, Salazar G, Boissin E, Romac S, Poulain J, Bourdin G, Iwankow G, Moulin C, Ziegler M, Porro B, Armstrong EJ, Hume BCC, Aury JM, Pogoreutz C, Paz-García DA, Nugues MM, Agostini S, Banaigs B, Boss E, Bowler C, de Vargas C, Douville E, Flores M, Forcioli D, Furla P, Gilson E, Lombard F, Pesant S, Reynaud S, Thomas OP, Troublé R, Wincker P, Zoccola D, Allemand D, Planes S, Thurber RV, Voolstra CR, Sunagawa S, Galand PE (2023) Ecology of Endozoicomonadaceae in three coral genera across the Pacific Ocean. Nat Commun 14:3037. https://doi.org/10.1038/s41467-023-38502-9
Hopkinson BM, Morel FM (2009) The role of siderophores in iron acquisition by photosynthetic marine microorganisms. Biometals 22:659–669. https://doi.org/10.1007/s10534-009-9235-2
Huang J, Wang F, Zhao H, Xu H, Liu S, Xu Q, Wang A, Li X (2020) Reef benthic composition and coral communities at the Wuzhizhou Island in the south China sea: the impacts of anthropogenic disturbance. Estuar, Coast Shelf S 243:106863. https://doi.org/10.1016/j.ecss.2020.106863
Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs J-PA, Hoey AS, Hoogenboom M, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359(6371):80–83. https://doi.org/10.1126/science.aan8048
Huse SM, Dethlefsen L, Huber JA, Mark Welch D, Relman DA, Sogin ML (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4(11):e1000255. https://doi.org/10.1371/journal.pgen.1000255
Jones A, Berkelmans R (2010) Potential costs of acclimatization to a warmer climate: growth of a reef coral with heat tolerant vs sensitive symbiont types. PLoS One 5(5):e10437. https://doi.org/10.1371/journal.pone.0010437
Keshavmurthy S, Meng PJ, Wang JT, Kuo CY, Yang SY, Hsu CM, Gan CH, Dai CF, Chen CA (2014) Can resistant coral-Symbiodinium associations enable coral communities to survive climate change? A study of a site exposed to long-term hot water input. PeerJ 2:e327. https://doi.org/10.7717/peerj.327
Keshavmurthy S, Chen TR, Liu PJ, Wang JT, Chen CA (2022) Learning from the past is not enough to survive present and future bleaching threshold temperatures. Sci Total Environ 852:158379. https://doi.org/10.1016/j.scitotenv.2022.158379
Kuang W, Li J, Zhang S, Long L (2015) Diversity and distribution of Actinobacteria associated with reef coral Porites lutea. Front Microbiol 6:1094. https://doi.org/10.3389/fmicb.2015.01094
LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:126–134. https://doi.org/10.2307/1542872
LaJeunesse TC, Loh WKW, Woesik RV, Hoegh-Guldberg O, Schmidt GW, Fitt WK (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol Oceanogr 48:2046–2054. https://doi.org/10.4319/lo.2003.48.5.2046
Li S, Yu K, Chen T, Shi Q, Zhang H (2011) Assessment of coral bleaching using symbiotic zooxanthellae density and satellite remote sensing data in the Nansha Islands South China sea. Chin Sci Bull 56(10):1031–1037. https://doi.org/10.1007/s11434-011-4390-6
Li J, Zou Y, Yang J, Li Q, Bourne DG, Sweet M, Liu C, Guo A, Zhang S (2022) Cultured bacteria provide insight into the functional potential of the coral-associated microbiome. mSystems 7(4):e0032722. https://doi.org/10.1128/msystems.00327-22
Liang J, Yu K, Wang Y, Huang X, Huang W, Qin Z, Pan Z, Yao Q, Wang W, Wu Z (2017) Distinct bacterial communities associated with massive and branching scleractinian corals and potential linkages to coral susceptibility to thermal or cold stress. Front Microbiol 8:979. https://doi.org/10.3389/fmicb.2017.00979
Liang J, Deng C, Yu K, Ge R, Xu Y, Qin Z, Chen B, Wang Y, Su H, Huang X, Huang W, Wang G, Gong S (2021) Cross-linked regulation of coral-associated dinoflagellates and bacteria in Pocillopora sp. during high-temperature stress and recovery. Microorganisms. https://doi.org/10.3390/microorganisms9091972
Littman R, Willis BL, Bourne DG (2011) Metagenomic analysis of the coral holobiont during a natural bleaching event on the great barrier reef. Environ Microbiol Rep 3(6):651–660. https://doi.org/10.1111/j.1758-2229.2010.00234.x
Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Manullang C, Millyaningrum IH, Iguchi A, Miyagi A, Tanaka Y, Nojiri Y, Sakai K (2020) Responses of branching reef corals Acropora digitifera and Montipora digitata to elevated temperature and pCO(2). PeerJ 8:e10562. https://doi.org/10.7717/peerj.10562
Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19(2):155–163. https://doi.org/10.1007/s003380000086
Matthews JL, Raina JB, Kahlke T, Seymour JR, van Oppen MJH, Suggett DJ (2020) Symbiodiniaceae-bacteria interactions: rethinking metabolite exchange in reef-building corals as multi-partner metabolic networks. Environ Microbiol 22(5):1675–1687. https://doi.org/10.1111/1462-2920.14918
McDevitt-Irwin JM, Baum JK, Garren M, Vega Thurber RL (2017) Responses of coral-associated bacterial communities to local and global stressors. Front Mar Sci 4:262. https://doi.org/10.3389/fmars.2017.00262
Members C-N (2022) Database resources of the national genomics data center, China national center for bioinformation in 2022. Nucleic Acids Res 50(D1):D27–D38. https://doi.org/10.1093/nar/gkab951
Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJ (2009) The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS ONE 4(7):e6364. https://doi.org/10.1371/journal.pone.0006364
Nitschke MR, Rosset SL, Oakley CA, Gardner SG, Camp EF, Suggett DJ, Davy SK (2022) The diversity and ecology of Symbiodiniaceae: A traits-based review. Adv Mar Biol 92:55–127. https://doi.org/10.1016/bs.amb.2022.07.001
Nordemar I, Nyström M, Dizon R (2003) Effects of elevated seawater temperature and nitrate enrichment on the branching coral Porites cylindrica in the absence of particulate food. Mar Biol 142:669–677. https://doi.org/10.1007/s00227-002-0989-0
Osman EO, Suggett DJ, Voolstra CR, Pettay DT, Clark DR, Pogoreutz C, Sampayo EM, Warner ME, Smith DJ (2020) Coral microbiome composition along the northern Red Sea suggests high plasticity of bacterial and specificity of endosymbiotic dinoflagellate communities. Microbiome 8(1):8. https://doi.org/10.1186/s40168-019-0776-5
Palmer C, Jimenez C, Bassey G, Ruiz E, Villalobos Cubero T, Chavarria Diaz MM, Harrison XA, Puschendorf R (2022) Cold water and harmful algal blooms linked to coral reef collapse in the eastern tropical Pacific. PeerJ 10:e14081. https://doi.org/10.7717/peerj.14081
Patel ZZ, Kumar D, Puvar A, Joshi H, Joshi C, Tipre DR, Joshi M (2023) Exploring bacteriome diversity of coral Goniopora sp. and Favia favus from the Gulf of Kutch, Gujarat. J Sea Res 192:102361. https://doi.org/10.1016/j.seares.2023.102361
Qin Z, Yu K, Liang Y, Chen B, Huang X (2020) Latitudinal variation in reef coral tissue thickness in the south China sea: potential linkage with coral tolerance to environmental stress. Sci Total Environ 711:134610. https://doi.org/10.1016/j.scitotenv.2019.134610
Quigley KM, Davies SW, Kenkel CD, Willis BL, Matz MV, Bay LK (2014) Deep-sequencing method for quantifying background abundances of Symbiodinium types: exploring the rare symbiodinium biosphere in reef-building corals. PLoS ONE 9(4):e94297. https://doi.org/10.1371/journal.pone.0094297
Ramanan R, Kim BH, Cho DH, Oh HM, Kim HS (2016) Algae–bacteria interactions: evolution, ecology and emerging applications. Biotechnol Adv 34:14–29. https://doi.org/10.1016/j.biotechadv.2015.12.003
Ren Y, Yu G, Shi C, Liu L, Guo Q, Han C, Zhang D, Zhang L, Liu B, Gao H, Zeng J, Zhou Y, Qiu Y, Wei J, Luo Y, Zhu F, Li X, Wu Q, Li B, Fu W, Tong Y, Meng J, Fang Y, Dong J, Feng Y, Xie S, Yang Q, Yang H, Wang Y, Zhang J, Gu H, Xuan H, Zou G, Luo C, Huang L, Yang B, Dong Y, Zhao J, Han J, Zhang X, Huang H (2022) Majorbio cloud: a one-stop, comprehensive bioinformatic platform for multiomics analyses. iMeta. https://doi.org/10.1002/imt2.12
Rodgers KS, Richards Dona A, Stender YO, Tsang AO, Han JHJ, Weible RM, Prouty N, Storlazzi C, Graham AT (2021) Rebounds, regresses, and recovery: a 15-year study of the coral reef community a’ Pila’a’ Kaua’i after decades of natural and anthropogenic stress events. Mar Pollut Bull 171:112306. https://doi.org/10.1016/j.marpolbul.2021.112306
Schoepf V, Grottoli AG, Levas SJ, Aschaffenburg MD, Baumann JH, Matsui Y, Warner ME (2015) Annual coral bleaching and the long-term recovery capacity of coral. Proc Biol Sci 282:1819. https://doi.org/10.1098/rspb.2015.1887
Setter RO, Franklin EC, Mora C (2022) Co-occurring anthropogenic stressors reduce the timeframe of environmental viability for the world’s coral reefs. Plos Biol 20(10):e3001821. https://doi.org/10.1371/journal.pbio.3001821
Shi T, Niu G, Kvitt H, Zheng X, Qin Q, Sun D, Ji Z, Tchernov D (2021) Untangling ITS2 genotypes of algal symbionts in zooxanthellate corals. Mol Ecol Resour 21(1):137–152. https://doi.org/10.1111/1755-0998.13250
Stat M, Pochon X, Franklin EC, Bruno JF, Casey KS, Selig ER, Gates RD (2013) The distribution of the thermally tolerant symbiont lineage (Symbiodinium clade D) in corals from Hawaii: correlations with host and the history of ocean thermal stress. Ecol Evol 3(5):1317–1329. https://doi.org/10.1002/ece3.556
van Oppen MJH, Blackall LL (2019) Coral microbiome dynamics, functions and design in a changing world. Nat Rev Microbiol 17(9):557–567. https://doi.org/10.1038/s41579-019-0223-4
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267. https://doi.org/10.1128/AEM.00062-07
Xu L, Yu K, Li S, Liu G, Tao S, Shi Q, Chen T, Zhang H (2017) Interseasonal and interspecies diversities of Symbiodinium density and effective photochemical efficiency in five dominant reef coral species from Luhuitou fringing reef, northern south china Sea. Coral Reefs 36(2):477–487. https://doi.org/10.1007/s00338-016-1532-y
Xu H, Feng B, Xie M, Ren Y, Xia J, Zhang Y, Wang A, Li X (2020a) Physiological characteristics and environment adaptability of reef-building corals at the Wuzhizhou island of south China Sea. Front Physiol 11:390. https://doi.org/10.3389/fphys.2020.00390
Xu S, Yu K, Zhang Z, Chen B, Qin Z, Huang X, Jiang W, Wang Y, Wang Y (2020) Intergeneric differences in trophic status of scleractinian corals from Weizhou Island, northern South China sea: implication for their different environmental stress tolerance. J Geophy Res-Biogeo. https://doi.org/10.1029/2019jg005451
Zaneveld J, McMinds R, Vega Thurber R (2017) Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat Microbiol 2:17121. https://doi.org/10.1038/nmicrobiol.2017.121
Zhang Y, Chen RW, Liu X, Zhu M, Li Z, Wang A, Li X (2022) Oxidative stress, apoptosis, and transcriptional responses in Acropora microphthalma under simulated diving activities. Mar Pollut Bull 183:114084. https://doi.org/10.1016/j.marpolbul.2022.114084
Zhu W, Xia J, Ren Y, Xie M, Yin H, Liu X, Huang J, Zhu M, Li X (2021) Coastal corals during heat stress and eutrophication: a case study in northwest Hainan coastal areas. Mar Pollut Bull 173(Pt B):113048. https://doi.org/10.1016/j.marpolbul.2021.113048
Zhu W, Liu X, Zhu M, Li X, Yin H, Huang J, Wang A, Li X (2022a) Responses of Symbiodiniaceae shuffling and microbial community assembly in thermally stressed Acropora hyacinthus. Front Microbiol 13:832081. https://doi.org/10.3389/fmicb.2022.832081
Zhu W, Zhu M, Liu X, Xia J, Wang H, Chen R, Li X (2022b) Adaptive changes of coral Galaxea fascicularis holobiont in response to nearshore stress. Front Microbiol 13:1052776. https://doi.org/10.3389/fmicb.2022.1052776
Ziegler M, Grupstra CG, Barreto MM, Eaton M, BaOmar J, Zubier K, Al-Sofyani A, Turki AJ, Ormond R, Voolstra CR (2019) Coral bacterial community structure responds to environmental change in a host-specific manner. Nat Commun 10:3092. https://doi.org/10.1038/s41467-019-10969-5
Acknowledgements
The authors were grateful for constructive suggestions and technical support from the instructors and all the laboratory members.
Funding
This work was financially supported by the National Natural Science Foundation of China (42206108, 42161144006 or 3511/21) and the Natural Science Foundation of Hainan Province (2021RC169, 423QN210).
Author information
Authors and Affiliations
Contributions
RWC and XL designed this study. ZL, XBL, and JH acquired the data. RWC, WZ, and YL performed the analyses and drew graphs. RWC drafted the manuscript. AW took part in supervision and funding acquisition. XL framed the research, supervision, and funding acquisition. All author reviewed the manuscript and made suggestions.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
338_2024_2475_MOESM1_ESM.eps
Fig. S1 Location of the study site at the WZZ Island. The sampling sites of the north side are the area of intensive tourism activities (N1–N5), and the south side is the area far from the influence of tourism activities (S1–S5)
Supplementary file1 (EPS 10340 KB)
Fig. S2. Bacterial metabolic enrichment in the KEGG function was predicted by PICRUSt
Supplementary file2 (EPS 3378 KB)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Chen, RW., Li, Z., Huang, J. et al. The community stability of Symbiodiniaceae and bacteria of different morphological corals and linkages to coral susceptibility to anthropogenic disturbance. Coral Reefs 43, 467–481 (2024). https://doi.org/10.1007/s00338-024-02475-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-024-02475-y