水质变化对豆荚软珊瑚(Lobophytum sp.)共生藻(Symbiodiniaceae)、菌群落结构的影响

doi:10.11978/2024138

摘要/Abstract

摘要： 本研究对豆荚软珊瑚(Lobophytum sp.)个体在不同水质条件下饲养1个月, 通过高通量测序技术比较分析水质变化下珊瑚共生藻、水体细菌和珊瑚共生细菌的群落结构变化特征。结果显示: 1)环境营养盐在硝态氮0~80.64μmol·L^-1、磷酸盐0~ 1.05μmol·L^-1时, 珊瑚共生藻丰富度大幅降低, 三组珊瑚共生藻均以Cladocopium属为主导优势种群(相对丰度70.25%~ 98.13%), 且该属共生藻对低营养盐耐受性较佳, 对高营养盐耐受性较差; 2)水体细菌和珊瑚共生细菌主导优势种群均为变形菌门(Proteobacteria)(相对丰度45.63%~86.55%), 在属水平上水体细菌多样性(Shannon指数4.60~4.97)高于珊瑚共生细菌多样性(Shannon指数2.58~3.81), 且两者优势菌群种类具有相对独立性; 3)共生细菌Cohaesibacter表现出较强的低营养盐耐受性, 环境营养盐降低, 其丰度显著升高, 由<3%升高至40.27%, 且该属珊瑚对共生细菌弧菌(Vibrio)具有较强的适应性(Vibrio属丰度占比23.71%时珊瑚共生体未表现出明显异常)。研究表明, 水质变化(营养盐)能够影响豆荚软珊瑚共生藻和共生细菌的种群结构, 其中珊瑚共生细菌群落结构的改变更为显著, 且相较于环境水体细菌, 环境营养盐的变动对该珊瑚共生细菌群落结构的影响更为明显。本实验旨在补充水质变化对珊瑚共生体的影响研究, 为珊瑚共生系统的稳态研究提供实验依据, 同时为制定珊瑚保育方案提供一定借鉴。

关键词: 豆荚软珊瑚, 共生藻, 共生细菌, 营养盐, 群落结构

Abstract:

In this study, Lobophytum sp. was cultured under different water qualities for one month, and the community structure of Symbiodiniaceae, ambient water bacteria, and symbiotic bacteria were analyzed using high-throughput sequencing technology. The findings indicated the following. 1) Symbiodiniaceae richness decreased significantly under nutrients conditions ranging from 0 to 80.64 μmol·L^-1nitrate and 0 to 1.05 μmol·L^-1phosphate. Cladocopium sp. dominated the Symbiodiniaceae in all three coral groups, with a relative abundance ranging from 70.25% to 98.13%, exhibiting higher tolerance to low nutrients concentration but greater sensitivity to high nutrients concentration. 2) At the phylum level, water-associated bacteria and coral symbiotic bacteria differed in relative abundance, with all dominant bacterial populations belonging to Proteobacteria, ranging from 45.63% to 86.55% in relative abundance. However, the environmental bacterial diversity at the genus level (Shannon index 4.60~4.97) was higher than that of coral symbiotic bacteria (Shannon index 2.58~3.81), with distinct taxonomic separation between the two communities at the genus level. 3) The coral symbiotic bacterium Cohaesibacter exhibited high tolerance to low nutrient levels, with its relative abundance increasing significantly from < 3% to 40.27% as nutrient levels decreased. Additionally, this genus of soft corals demonstrated strong adaptability to symbiotic bacteria Vibrio, with no significant anomalies observed even at a high Vibrio abundance of 23.71%. These results suggest that the abundance of Symbiodiniaceae and symbiotic bacteria in corals is influenced by ambient water quality, leading to changes in dominant bacteria and alterations in community structure of symbiotic bacteria from corals. Moreover, nutrient fluctuations preferentially shaped the community structure of coral-associated bacteria over environmental bacteria, with more pronounced effects on the former. This study contributes to the growing body of research on soft corals by providing a foundation for understanding how different water quality parameters dynamically affect the structure of symbiotic microorganisms in soft corals. It also offers insights into the effect of water quality fluctuations on soft coral Symbiodiniaceae and bacterial community structure in artificial environments, thereby supporting the development of coral conservation programs.

Key words: Lobophytum, Symbiodiniaceae, symbiotic bacteria, nutrients, community structure

中图分类号:

李达, 王云忠, 齐继光, 杨翠华. 水质变化对豆荚软珊瑚(Lobophytum sp.)共生藻(Symbiodiniaceae)、菌群落结构的影响[J]. 热带海洋学报, 2025, 44(4): 136-144.

LI Da, WANG Yunzhong, QI Jiguang, YANG Cuihua. Effects of water quality changes on community structures of Symbiodiniaceae and symbiotic bacteria in soft coral Lobophytum sp.[J]. Journal of Tropical Oceanography, 2025, 44(4): 136-144.

图/表 13

表1

表2

表3

表4

表5

图1

图2

表6

表7

表8

图3

图4

图5

参考文献 49

[1]	BAKER D M, ANDRAS J P, JORDÁN-GARZA A G, et al, 2013. Nitrate competition in a coral symbiosis varies with temperature among Symbiodinium clades[J]. The ISME Journal, 7(6): 1248-1251.
[2]	BANIN E, KHARE S K, NAIDER F, et al, 2001. Proline-rich peptide from the coral pathogen Vibrio shiloi that inhibits photosynthesis of Zooxanthellae[J]. Applied and Environmental Microbiology, 67(4): 1536-1541.
[3]	BAROTT K L, RODRIGUEZ-BRITO B, JANOUŠKOVEC J, et al, 2011. Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis[J]. Environmental Microbiology, 13(5): 1192-1204.
[4]	BAWAKID N O, ALORFI H S, ALQARNI N M, et al, 2023. Cembranoids from the Red Sea soft coral Sarcophyton glaucum protect against indomethacin-induced gastric injury[J]. Naunyn-Schmiedeberg’s Archives of Pharmacology, 396(2): 289-300.
[5]	BEN-HAIM Y, THOMPSON F L, THOMPSON C C, et al, 2003. Vibrio coralliilyticus sp. nov., a temperature-dependent pathogen of the coral Pocillopora damicornis[J]. International Journal of Systematic and Evolutionary Microbiology, 53(Pt 1): 309-315.
[6]	BERKELMANS R, VAN OPPEN M J H, 2006. The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change[J]. Proceedings of the Royal Society B-Biological Sciences, 273(1599): 2305-2312.
[7]	CHENG S Y, WANG S K, DUH C Y, 2014. Secocrassumol, a seco-cembranoid from the Dongsha Atoll soft coral Lobophytum crassum[J]. Marine Drugs, 12(12): 6028-6037.
[8]	COLEMAN A W, SUAREZ A, GOFF L J, 1994. Molecular delineation of species and syngens in volvocacean green algae (Chlorophyta)[J]. Journal of Phycology, 30(1): 80-90.
[9]	ENRÍQUEZ S, MÉNDEZ E R, HOEGH-GULDBERG O, et al, 2017. Key functional role of the optical properties of coral skeletons in coral ecology and evolution[J]. Proceedings of the Royal Society B-Biological Sciences, 284(1853): 20161667.
[10]	FARMER J J, HICKMAN-BRENNER F W, 2021. The genera Vibrio and Photobacterium[M]// DWORKIN M, FALKOW S, ROSENBERG E, et al. The Prokaryotes. New York: Springer: 508-563.
[11]	FRANYOTO Y D, MASDUQI A F, MUCHLISIN S, et al, 2019. Bacterial symbionts of soft coral Lobophytum sp. from Panjang island, Jepara, Indonesia with antimicrobial MDR TB potency[J]. Journal of Tropical Pharmacy and Chemistry, 4(5): 194-202.
[12]	GLASL B, HERNDL G J, FRADE P R, 2016. The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance[J]. The ISME Journal, 10(9): 2280-2292.
[13]	KAMADA T, ZANIL I I, PHAN C S, et al, 2018. A new cembrane, from soft coral genus Sarcophyton in Borneo[J]. Natural Product Communications, 13(2): 123-124.
[14]	KANIEWSKA P, MAGNUSSON S H, ANTHONY K R N, et al, 2011. Importance of macro-versus microstructure in modulating light levels inside coral colonies[J]. Journal of Phycology, 47(4): 846-860.
[15]	KELLY L W, WILLIAMS G J, BAROTT K L, et al, 2014. Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors[J]. Proceedings of the National Academy of Sciences of the United States of America, 111(28): 10227-10232.
[16]	LA RIVIÈRE M, ROUMAGNAC M, GARRABOU J, et al, 2013. Transient shifts in bacterial communities associated with the temperate gorgonian Paramuricea clavata in the Northwestern Mediterranean Sea[J]. PLoS ONE, 8(2): e57385.
[17]	LAI K H, YOU WANJING, LIN CHICHEN, et al, 2017. Anti-inflammatory cembranoids from the soft coral Lobophytum crassum[J]. Marine Drugs, 15(10): 327.
[18]	LAJEUNESSE T, 2002. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs[J]. Marine Biology, 141(2): 387-400.
[19]	LAJEUNESSE T C, PARKINSON J E, GABRIELSON P W, et al, 2018. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts[J]. Current Biology, 28(16): 2570-2580. e6.
[20]	LAJEUNESSE T C, TRENCH R K, 2000. Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea Anemone Anthopleura elegantissima (Brandt)[J]. The Biological Bulletin, 199(2): 126-134.
[21]	LEE O O, YANG JIANGKE, BOUGOUFFA S, et al, 2012. Spatial and species variations in bacterial communities associated with corals from the Red Sea as revealed by pyrosequencing[J]. Applied and Environmental Microbiology, 78(20): 7173-7184.
[22]	LI SHU, YU KEFU, SHI QI, et al, 2008. Interspecies and spatial diversity in the symbiotic zooxanthellae density in corals from northern South China Sea and its relationship to coral reef bleaching[J]. Chinese Science Bulletin, 53(2): 295-303.
[23]	LITTLE A F, VAN OPPEN M J H, WILLIS B L, 2004. Flexibility in algal endosymbioses shapes growth in reef corals[J]. Science, 304(5676): 1492-1494.
[24]	MACKNIGHT N J, COBLEIGH K, LASSEIGNE D, et al, 2021. Microbial dysbiosis reflects disease resistance in diverse coral species[J]. Communications Biology, 4(1): 679.
[25]	MATTHÉE G F, KÖNIG G M, WRIGHT A D, 1998. Three new diterpenes from the marine soft coral Lobophytum crassum[J]. Journal of Natural Products, 61(2): 237-240.
[26]	MCCAULEY E P, HALTLI B, CORREA H, et al, 2016. Spatial and temporal investigation of the microbiome of the Caribbean octocoral Erythropodium caribaeorum[J]. FEMS Microbiology Ecology, 92(9): fiw147.
[27]	MOHAMED T A, ABDELMAWGOUD S M, HAMDY A A, et al, 2024. A new cembranoid from the Red Sea soft coral Sarcophyton acutum[J]. Natural Product Research, 38(3): 512-522.
[28]	MOHAMED T A, ELSHAMY A I, ABD EL-RAZEK M H, et al, 2022. Sarcoconvolutums F and G: polyoxygenated cembrane-type diterpenoids from Sarcophyton convolutum, a red sea soft coral[J]. Molecules, 27(18): 5835.
[29]	MOHAMMED-GEBA K, ELSHAARAWY R S, ALIAN A, et al, 2024. Unraveling the Red Sea soft coral Sarcophyton convolutum potentials against oxidative and inflammatory stresses in zebrafish[J]. Fish & Shellfish Immunology, 147: 109442.
[30]	MORENO C, ROMERO J, ESPEJO R T, 2002. Polymorphism in repeated 16S rRNA genes is a common property of type strains and environmental isolates of the genus Vibrio[J]. Microbiology, 148(Pt 4): 1233-1239.
[31]	NGOC N T, HANH T T H, QUANG T H, et al, 2021. Polyhydroxylated steroids from the Vietnamese soft coral Sarcophyton ehrenbergi[J]. Steroids, 176: 108932.
[32]	PHAN C S, YEE C S, VAIRAPPAN C S, et al, 2019. Sinulaflexiolide P, a cembrane-type diterpenoid from Bornean soft coral Sinularia flexibilis[J]. Chemistry of Natural Compounds, 55(2): 285-288.
[33]	QIN ZHENJUN, YU KEFU, WANG YINGHUI, et al, 2019. Spatial and intergeneric variation in physiological indicators of corals in the South China Sea: insights into their current state and their adaptability to environmental stress[J]. Journal of Geophysical Research: Oceans, 124(5): 3317-3332.
[34]	RESHEF L, KOREN O, LOYA Y, et al, 2006. The coral probiotic hypothesis[J]. Environmental Microbiology, 8(12): 2068-2073.
[35]	RODRIGUES I G, MIGUEL M G, MNIF W, 2019. A brief review on new naturally occurring cembranoid diterpene derivatives from the soft corals of the genera Sarcophyton, Sinularia, and Lobophytum since 2016[J]. Molecules, 24(4): 781.
[36]	ROHWER F, SEGURITAN V, AZAM F, et al, 2002. Diversity and distribution of coral-associated bacteria[J]. Marine Ecology Progress Series, 243: 1-10.
[37]	ROSENBERG E, KOREN O, RESHEF L, et al, 2007. The role of microorganisms in coral health, disease and evolution[J]. Nature Reviews Microbiology, 5(5): 355-362.
[38]	ROWAN R, KNOWLTON N, BAKER A, et al, 1997. Landscape ecology of algal symbionts creates variation in episodes of coral bleaching[J]. Nature, 388(6639): 265-269.
[39]	ROY P K, ROY S, UEDA K, 2019. New cytotoxic cembranolides from an Okinawan soft coral, Lobophytum sp.[J]. Fitoterapia, 136: 104162.
[40]	SANTOS S R, TAYLOR D J, COFFROTH M A, 2001. Genetic comparisons of freshly isolated versus cultured symbiotic dinoflagellates: implications for extrapolating to the intact symbiosis[J]. Journal of Phycology, 37(5): 900-912.
[41]	SATO K, ISHIGAMI S, KOIKE M, et al, 2023. New marine diterpenoid from the Okinawan soft coral, Lobophytum sp.[J]. Natural Product Communications, 18(1): 1934578X221075978.
[42]	VAN DE WATER J A J M, VOOLSTRA C R, ROTTIER C, et al, 2018. Seasonal stability in the microbiomes of temperate gorgonians and the red coral Corallium rubrum across the Mediterranean Sea[J]. Microbial Ecology, 75(1): 274-288.
[43]	WANGPRASEURT D, HOLM J B, LARKUM A W D, et al, 2017. In vivo microscale measurements of light and photosynthesis during coral bleaching: evidence for the optical feedback loop?[J]. Frontiers in Microbiology, 8: 59.
[44]	WESSELS W, SPRUNGALA S, WATSON S A, et al, 2017. The microbiome of the octocoral Lobophytum pauciflorum: minor differences between sexes and resilience to short-term stress[J]. FEMS Microbiology Ecology, 93(5): fix013.
[45]	YU XIAOPENG, YU KEFU, HUANG WEN, et al, 2020. Thermal acclimation increases heat tolerance of the scleractinian coral Acropora pruinosa[J]. Science of The Total Environment, 733: 139319.
[46]	ZHU WENTAO, LIU XIANGBO, ZHU MING, et al, 2022. Responses of Symbiodiniaceae shuffling and microbial community assembly in thermally stressed Acropora hyacinthus[J]. Frontiers in Microbiology, 13: 832081.
[47]	ZIEGLER M, ARIF C, BURT J A, et al, 2017. Biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the Arabian Peninsula[J]. Journal of Biogeography, 44(3): 674-686.
[48]	ZIEGLER M, EGUÍLUZ V M, DUARTE C M, et al, 2018. Rare symbionts may contribute to the resilience of coral-algal assemblages[J]. The ISME Journal, 12(1): 161-172.
[49]	ZIEGLER M, ROIK A, PORTER A, et al, 2016. Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea[J]. Marine Pollution Bulletin, 105(2): 629-640.

珊瑚缸	红皮藻科	刺尾鱼科	雀鲷科	天竺鲷科	软珊瑚科	海葵科
1	Y	Y	N	N	Y	Y
2	N	N	Y	Y	N	Y
3	N	N	N	N	N	Y

珊瑚缸	水温/℃	盐度/‰	pH	亚硝态氮 /(μmol·L^-1)	氨氮 /(μmol·L^-1)	硝态氮 /(μmol·L^-1)	磷酸盐 /(μmol·L^-1)	KH/dKH	钙离子 /(μmol·L^-1)	镁离子 /(μmol·L^-1)
1	25	32	8.1~8.4	0~0.43	0~2.77	80.64~161.28	1.05~2.11	8~9	9.48~9.98	46.49~52.58
2	25	32	8.1~8.4	0~0.43	0~2.77	403.20~806.39	2.11~5.26	8~9	9.48~9.98	46.49~52.58
3	25	32	8.1~8.4	0~0.43	0~2.77	32.26~80.64	0~1.05	8~9	9.48~9.98	46.49~52.58

样本组名	效序列条数	平均长度/bp	最短序列长度/bp	最长序列长度/bp
C1	106234	289.89	240	369
C2	92647	305.81	201	369
C3	95787	283.77	237	385

样本组名	Cladocopium 相对丰度/%	Symbiodinium 相对丰度/%	未鉴定类相对丰度/%	其他类相对丰度/%
C1	90.69	1.01	8.18	0.12
C2	70.25	0.75	28.85	0.15
C3	98.13	1.14	0.13	0.60

样本组名	序列数	分类单元	Shannon 指数	Simpson 指数	Chao 指数	Ace 指数	覆盖率
C1	105818	20	0.42	0.82	21.00	22.82	1.00
C2	92363	22	0.74	0.56	22.00	22.00	1.00
C3	95698	14	0.15	0.95	14.00	14.00	1.00