Changes of microbial community composition in Porites lutea during health-bleaching recovery under high temperature stress

LIU Ziyi; LIU Yongchun; ZHU Ming; CHEN Bogui; ZHENG Huina; XIAO Baohua

Article Contents

Article Navigation > Haiyang Xuebao > 2025 > Accepted Manuscript

LIU Ziyi，LIU Yongchun，ZHU Ming, et al. Changes of microbial community composition in Porites lutea during health-bleaching recovery under high temperature stress[J]. Haiyang Xuebao，2025, 47(x)：1–16

Citation:

PDF( 3467 KB)

Changes of microbial community composition in Porites lutea during health-bleaching recovery under high temperature stress

LIU Ziyi^1
,,
LIU Yongchun²,
ZHU Ming²,
CHEN Bogui^{2, 3},
ZHENG Huina^{2, 4},
XIAO Baohua^{1, 2
,
,}

1.
College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, China
2.
Shenzhen Research Institute, Guangdong Ocean University, Shenzhen 518108, China
3.
Shenzhen Bihai Blue Sky Marine Technology Co., LTD., Shenzhen 518108, China
4.
College of Food Science and Technology, Guangdong Ocean University, Zhanjiang 524088, China

Received Date: 2024-06-13
Rev Recd Date: 2025-02-19

Available Online: 2025-04-16

Abstract

Abstract

Global coral bleaching under heat stress has been identified as a major driver of coral reef degradation. The composition, metabolism and functional characteristics of microbial communities in coral holosomes under heat stress has been reported. However, the changes in microbial structure and composition throughout the entire process of coral health - bleaching - recovery have not been studied so far. In this study, Porites lutea in Shenzhen Sea area was selected as the research object. The process of coral health - bleaching - recovery under heat stress was simulated in the laboratory. High-throughput sequencing and macro-genome sequencing technologies were used to analyse the differences in coral microbial communities and functional gene changes during five characteristic phases of coral bleaching and restoration: healthy, beginning of bleaching, continued bleaching, beginning of recover, and recovered. With the increase of temperature, Proteobacteria increased significantly during the bleaching process and decreased during recovery; Bacteroidota etc. decreased during bleaching and increased during recovery. During the coral bleaching process, the abundance of bacteria associated with stress tolerance, biofilm formation, mobile elements, and potential pathogenicity significantly increases. Conversely, the abundance of bacteria involved in quorum sensing decreases. Notably,four kinds of microbes play a crucial role in coral bleaching: Acinetobacter, Rhodobacter, and Burkholderia are key differential taxa in warming-induced coral bleaching, while Delftia may modulate other bacterial assemblages via quorum sensing mechanisms to maintain the stability of coral microbial communities.This study revealed the changes of microbes and their functions in coral tissues under high temperature stress, which provided molecular basis for elucidating the interaction mechanism between microbes and hosts during coral bleaching.
- Coral Bleaching,
- Pure Bacteria,
- High-Throughput Sequencing,
- Metagenome

FullText(HTML)

References(53)

References

[1]	Polidoro B, Carpenter K. Dynamics of coral reef recovery[J]. Science, 2013, 340(6128): 34−35. doi: 10.1126/science.1236833
[2]	Doney S C, Ruckelshaus M, Emmett Duffy J, et al. Climate change impacts on marine ecosystems[J]. Annual Review of Marine Science, 2012, 4(1): 11−37. doi: 10.1146/annurev-marine-041911-111611
[3]	Manikandan B, Ravindran J, Shrinivaasu S, et al. Community structure and coral status across reef fishing intensity gradients in Palk Bay reef, southeast coast of India[J]. Environmental Monitoring and Assessment, 2014, 186(10): 5989−6002. doi: 10.1007/s10661-014-3835-1
[4]	Hughes T P, Kerry J T, Álvarez-Noriega M, et al. Global warming and recurrent mass bleaching of corals[J]. Nature, 2017, 543(7645): 373−377. doi: 10.1038/nature21707
[5]	Frölicher T L, Fischer E M, Gruber N. Marine heatwaves under global warming[J]. Nature, 2018, 560(7718): 360−364. doi: 10.1038/s41586-018-0383-9
[6]	Chen Tianrun, Yu Kefu, Shi Qi, 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[J]. Chinese Science Bulletin, 2009, 54(12): 2107−2117. doi: 10.1007/s11434-009-0007-8
[7]	Yu Kefu. Coral reefs in the South China Sea: their response to and records on past environmental changes[J]. Science China Earth Sciences, 2012, 55(8): 1217−1229. doi: 10.1007/s11430-012-4449-5
[8]	Charpy L, Casareto B E, Langlade M J, et al. Cyanobacteria in coral reef ecosystems: a review[J]. Journal of Marine Sciences, 2012, 2012(1): 259571.
[9]	Tout J, Jeffries T C, Webster N S, et al. Variability in microbial community composition and function between different niches within a coral reef[J]. Microbial Ecology, 2014, 67(3): 540−552. doi: 10.1007/s00248-013-0362-5
[10]	Glasl B, Webster N S, Bourne D G. Microbial indicators as a diagnostic tool for assessing water quality and climate stress in coral reef ecosystems[J]. Marine Biology, 2017, 164(4): 91. doi: 10.1007/s00227-017-3097-x
[11]	Shade A, Peter H, Allison S D, et al. Fundamentals of microbial community resistance and resilience[J]. Frontiers in Microbiology, 2012, 3: 417.
[12]	Liu Zhuhong, Chen Chang, Gao Lei, et al. Differences in microbial communities between healthy and bleached coral Acropora solitaryensis from Xisha Islands, South China Sea[J]. Marine Biology Research, 2016, 12(10): 1101−1108. doi: 10.1080/17451000.2016.1236201
[13]	周进, 晋慧, 蔡中华. 微生物在珊瑚礁生态系统中的作用与功能[J]. 应用生态学报, 2014, 25(3): 919−930. Zhou Jin, Jin Hui, Cai Zhonghua. A review of the role and function of microbes in coral reef ecosystem[J]. Chinese Journal of Applied Ecology, 2014, 25(3): 919−930.
[14]	Ziegler M, Seneca F O, Yum L K, et al. Bacterial community dynamics are linked to patterns of coral heat tolerance[J]. Nature Communications, 2017, 8(1): 14213. doi: 10.1038/ncomms14213
[15]	Qin Zhenjun, Yu Kefu, Liang Jiayuan, et al. Significant changes in microbial communities associated with reef corals in the southern South China Sea during the 2015/2016 global‐scale coral bleaching event[J]. Journal of Geophysical Research: Oceans, 2020, 125(7): e2019JC015579. doi: 10.1029/2019JC015579
[16]	Xie J Y, Yeung Y H, Kwok C K, et al. Localized bleaching and quick recovery in Hong Kong's coral communities[J]. Marine Pollution Bulletin, 2020, 153: 110950. doi: 10.1016/j.marpolbul.2020.110950
[17]	Bourne D, Iida Y, Uthicke S, et al. Changes in coral-associated microbial communities during a bleaching event[J]. The ISME Journal, 2008, 2(4): 350−363. doi: 10.1038/ismej.2007.112
[18]	Littman R, Willis B L, Bourne D G. Metagenomic analysis of the coral holobiont during a natural bleaching event on the Great Barrier Reef[J]. Environmental Microbiology Reports, 2011, 3(6): 651−660. doi: 10.1111/j.1758-2229.2010.00234.x
[19]	Ben-Haim Y, Rosenberg E. A novel Vibrio sp. pathogen of the coral Pocillopora damicornis[J]. Marine Biology, 2002, 141(1): 47−55. doi: 10.1007/s00227-002-0797-6
[20]	Oladi M, Shokri M R, Rajabi-Maham H. Application of the coral health chart to determine bleaching status of Acropora downingi in a subtropical coral reef[J]. Ocean Science Journal, 2017, 52(2): 267−275. doi: 10.1007/s12601-017-0025-4
[21]	黄晖, 杨泽民, 张俊彬, 等. 柳珊瑚4种不同DNA提取方法的比较研究[J]. 海洋通报, 2007, 26(2): 100−104. doi: 10.3969/j.issn.1001-6392.2007.02.015 Huang Hui, Yang Zemin, Zhang Junbin, et al. Comparison of 4 different gorgonian DNA extraction methods[J]. Marine Science Bulletin, 2007, 26(2): 100−104. doi: 10.3969/j.issn.1001-6392.2007.02.015
[22]	Walters W, Hyde E R, Berg-Lyons D, et al. Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys[J]. Msystems, 2016, 1(1): 10. 1128.
[23]	Li Dinghua, Liu Chiman, Luo Ruibang, et al. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph[J]. Bioinformatics, 2015, 31(10): 1674−1676. doi: 10.1093/bioinformatics/btv033
[24]	Fu Limin, Niu Beifang, Zhu Zhengwei, et al. CD-HIT: accelerated for clustering the next-generation sequencing data[J]. Bioinformatics, 2012, 28(23): 3150−3152. doi: 10.1093/bioinformatics/bts565
[25]	Li Ruiqiang, Yu Chang, Li Yingrui, et al. SOAP2: an improved ultrafast tool for short read alignment[J]. Bioinformatics, 2009, 25(15): 1966−1967. doi: 10.1093/bioinformatics/btp336
[26]	Wyatt A S J, Leichter J J, Toth L T, et al. Heat accumulation on coral reefs mitigated by internal waves[J]. Nature Geoscience, 2019, 13(1): 28−34.
[27]	Gardner S G, Camp E F, Smith D J, et al. Coral microbiome diversity reflects mass coral bleaching susceptibility during the 2016 El Niño heat wave[J]. Ecology and Evolution, 2019, 9(3): 938−956. doi: 10.1002/ece3.4662
[28]	Ziegler M, Grupstra C G B, Barreto M M, et al. Coral bacterial community structure responds to environmental change in a host-specific manner[J]. Nature Communications, 2019, 10(1): 3092. doi: 10.1038/s41467-019-10969-5
[29]	Glasl B, Herndl G J, Frade P R. The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance[J]. The ISME Journal, 2016, 10(9): 2280−2292. doi: 10.1038/ismej.2016.9
[30]	Suggett D J, Smith D J. Coral bleaching patterns are the outcome of complex biological and environmental networking[J]. Global Change Biology, 2020, 26(1): 68−79. doi: 10.1111/gcb.14871
[31]	林姿君, 蔡中华, 林光辉, 等. 健康与白化状态下珊瑚共生菌的群落组成与功能差异[J]. 海洋学报, 2018, 40(2): 104−116. Lin Zijun, Cai Zhonghua, Lin Guanghui, et al. Community composition and functional differences of symbiotic bacteria in healthy and blenching coral[J]. Haiyang Xuebao, 2018, 40(2): 104−116.
[32]	Zaneveld J R, McMinds R, Vega Thurber R. Stress and stability: applying the Anna Karenina principle to animal microbiomes[J]. Nature Microbiology, 2017, 2(9): 17121. doi: 10.1038/nmicrobiol.2017.121
[33]	徐帅良. 滨珊瑚共附生细菌多样性及其纯培养研究[D]. 南宁: 广西大学, 2020. Xu Shuailiang. Diversity of Porites. associated bacteria and its pure culture study[D]. Nanning: Guangxi University, 2020.
[34]	Van De Water J A J M, Allemand D, Ferrier-Pagès C. Host-microbe interactions in octocoral holobionts - recent advances and perspectives[J]. Microbiome, 2018, 6(1): 64. doi: 10.1186/s40168-018-0431-6
[35]	Chapelle E, Mendes R, Bakker P A H M, et al. Fungal invasion of the rhizosphere microbiome[J]. The ISME Journal, 2016, 10(1): 265−268. doi: 10.1038/ismej.2015.82
[36]	Sharp K H, Distel D, Paul V J. Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides[J]. The ISME Journal, 2012, 6(4): 790−801. doi: 10.1038/ismej.2011.144
[37]	Kusdianto H, Kullapanich C, Palasuk M, et al. Microbiomes of healthy and bleached corals during a 2016 thermal bleaching event in the upper Gulf of Thailand[J]. Frontiers in Marine Science, 2021, 8: 643962. doi: 10.3389/fmars.2021.643962
[38]	Du Jikun, Xiao Kai, Huang Yali, et al. Seasonal and spatial diversity of microbial communities in marine sediments of the South China Sea[J]. Antonie Van Leeuwenhoek, 2011, 100(3): 317−331. doi: 10.1007/s10482-011-9587-9
[39]	Alexandre A, Laranjo M, Young J P W, et al. DnaJ is a useful phylogenetic marker for alphaproteobacteria[J]. International Journal of Systematic and Evolutionary Microbiology, 2008, 58(12): 2839−2849. doi: 10.1099/ijs.0.2008/001636-0
[40]	Brettar I, Christen R, Höfle M G. Rheinheimera perlucida sp. nov. , a marine bacterium of the Gammaproteobacteria isolated from surface water of the central Baltic Sea[J]. International Journal of Systematic and Evolutionary Microbiology, 2006, 56(9): 2177-2183.
[41]	Sun Fulin, Wang Youshao, Wu Meilin, et al. Spatial and vertical distribution of bacteria in the Pearl River estuary sediment[J]. African Journal of Biotechnology, 2012, 11(9): 2256−2266.
[42]	Miura N, Motone K, Takagi T, et al. Ruegeria sp. strains isolated from the reef-building coral Galaxea fascicularis inhibit growth of the temperature-dependent pathogen Vibrio coralliilyticus[J]. Marine Biotechnology, 2019, 21(1): 1−8. doi: 10.1007/s10126-018-9853-1
[43]	Kitamura R, Miura N, Ito M, et al. Specific detection of coral-associated Ruegeria, a potential probiotic bacterium, in corals and subtropical seawater[J]. Marine Biotechnology, 2021, 23(4): 576−589. doi: 10.1007/s10126-021-10047-2
[44]	Jones P R, Cottrell M T, Kirchman D L, et al. Bacterial community structure of biofilms on artificial surfaces in an estuary[J]. Microbial Ecology, 2007, 53(1): 153−162. doi: 10.1007/s00248-006-9154-5
[45]	Cárdenas A, Rodriguez-R L M, Pizarro V, et al. Shifts in bacterial communities of two Caribbean reef-building coral species affected by white plague disease[J]. The ISME Journal, 2012, 6(3): 502−512. doi: 10.1038/ismej.2011.123
[46]	Yellowlees D, Rees T A V, Leggat W. Metabolic interactions between algal symbionts and invertebrate hosts[J]. Plant, Cell & Environment, 2008, 31(5): 679-694.
[47]	Hördt A, López M G, Meier-Kolthoff J P, et al. Analysis of 1, 000+ type-strain genomes substantially improves taxonomic classification of Alphaproteobacteria[J]. Frontiers in Microbiology, 2020, 11: 468. doi: 10.3389/fmicb.2020.00468
[48]	McDevitt-Irwin J M, Baum J K, Garren M, et al. Responses of coral-associated bacterial communities to local and global stressors[J]. Frontiers in Marine Science, 2017, 4: 262. doi: 10.3389/fmars.2017.00262
[49]	O'Brien P A, Morrow K M, Willis B L, et al. Implications of ocean acidification for marine microorganisms from the free-living to the host-associated[J]. Frontiers in Marine Science, 2016, 3: 47.
[50]	Hayashi K, Senuma W, Kai K, et al. Major exopolysaccharide, EPS I, is associated with the feedback loop in the quorum sensing of Ralstonia solanacearum strain OE1-1[J]. Molecular Plant Pathology, 2019, 20(12): 1740−1747. doi: 10.1111/mpp.12870
[51]	Ainsworth T D, Krause L, Bridge T, et al. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts[J]. The ISME Journal, 2015, 9(10): 2261−2274. doi: 10.1038/ismej.2015.39
[52]	Zhou Jin, Lin Zijun, Cai Zhonghua, et al. Opportunistic bacteria use quorum sensing to disturb coral symbiotic communities and mediate the occurrence of coral bleaching[J]. Environmental Microbiology, 2020, 22(5): 1944−1962. doi: 10.1111/1462-2920.15009
[53]	Teplitski M, Warriner K, Bartz J, et al. Untangling metabolic and communication networks: interactions of enterics with phytobacteria and their implications in produce safety[J]. Trends in Microbiology, 2011, 19(3): 121−127. doi: 10.1016/j.tim.2010.11.007