Isolated culture and physiological characteristics of four symbiotic Symbiodiniaceae strains from South China Sea

BU Hailu; WANG Jun; ZHOU Zhi

doi:10.15886/j.cnki.rdswxb.20230117

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Volume 15 Issue 4

Jul. 2024

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Article Navigation > Journal of Tropical Biology > 2024 > 15(4): 460-470

BU Hailu, WANG Jun, ZHOU Zhi. Isolated culture and physiological characteristics of four symbiotic Symbiodiniaceae strains from South China Sea[J]. Journal of Tropical Biology, 2024, 15(4): 460-470. doi: 10.15886/j.cnki.rdswxb.20230117

Citation:

BU Hailu, WANG Jun, ZHOU Zhi. Isolated culture and physiological characteristics of four symbiotic Symbiodiniaceae strains from South China Sea[J]. Journal of Tropical Biology, 2024, 15(4): 460-470. doi: 10.15886/j.cnki.rdswxb.20230117

Isolated culture and physiological characteristics of four symbiotic Symbiodiniaceae strains from South China Sea

doi: 10.15886/j.cnki.rdswxb.20230117

College of Marine Science and Engineering, Hainan University, Haikou, Hainan 570228, China

Received Date: 2023-10-16
Rev Recd Date: 2023-11-19
Publish Date: 2024-07-25

Abstract

In recent years, coral bleaching events induced by marine heat waves have occurred frequently, and Symbiodiniaceae, as algal symbionts of coral hosts, has been proved to play an important role in controlling coral environmental tolerance. In order to explore the differences among different species of Symbiodiniaceae and their physiological characteristics, four monoclonal strains of Symbiodiniaceae were isolated and obtained from different cnidaria organisms in the South China Sea, and a series of investigations were conducted on their phylogenetic, morphological and various physiological characteristics. The results exhibited that the four strains of Symbiodiniaceae were Symbiodinium（type A3, HNUA3-1）, Breviolum（type B1, HNUB1-1）, Cladocopium（type C1, HNUC1-1） and Durusdinium（type D1, HNUD1-1）, respectively. Observations by light microscopy and transmission electron microscopy revealed that the four strains had higher similarity in morphological characteristics but there were significant differences in specific growth rates, reflecting the species-specific growth characteristics. The specific growth rate of Breviolum sp. HNUB1-1 was the highest, and the cell density of Breviolum sp. HNUB1-1 was significantly higher than that of the other three strains on the 3rd, 5th and 7th day（P ＜ 0.05）, the specific growth rate of Symbiodinium sp. HNUA3-1 was second highest, the specific growth rate of Cladocopium sp. HNUC1-1 and Durusdinium sp. HNUD1-1 was the lowest, and there was no significant difference in cell density within 7 days of culture. Furthermore, different strains waere also specie-specific in maximum quantum efficiency of Photosystem II（Fv/Fm）. Under the same conditions, the Fv/Fm of the Durusdinium sp. HNUD1-1 was significantly lower than that of the other three strains, reflecting the photosynthetic and physiological characteristics of its potential heat resistance. This study provided theoretical basis for enriching the resources of Symbiodiniaceae in the South China Sea, and clarifying the differences and characteristics of the Symbiodiniaceae, which can be used to provide basic data support for the conservation and restoration of the coral reef ecosystem in the South China Sea.
- Symbiodiniaceae,
- Symbiodinium,
- Breviolum,
- Cladocopium,
- Durusdinium

References

[1]	MUSCATINE L, PORTER J W. Reef corals:mutualistic symbioses adapted to nutrient-poor environments[J]. BioScience, 1977, 27(7):454-460.
[2]	POCHON X, GATES R D. A new Symbiodinium clade(Dinophyceae)from soritid foraminifera in Hawai’i[J].Molecular Phylogenetics and Evolution, 2010, 56:492-497.
[3]	LAJEUNESSE T C, PARKINSON J E, GABRIELSON P W, et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts[J]. Current Biology, 2018, 28(16):2570-2580.
[4]	NITSCHKE M R, CRAVEIRO S C, BRANDÃO C, et al.Description of freudenthalidium gen. nov. and halluxium gen. nov. to formally recognize clades Fr3 and H as Genera in the family Symbiodiniaceae(Dinophyceae)[J]. Journal of Phycology, 2020, 56(4):923-940.
[5]	POCHON X, LAJEUNESSE T C. Miliolidium n. gen, a new symbiodiniacean genus whose members associate with soritid foraminifera or are free-living[J]. The Journal of Eukaryotic Microbiology, 2021:e12856.
[6]	FISHER P L, MALME M K, DOVE S. The effect of temperature stress on coral-Symbiodinium associations containing distinct symbiont types[J]. Coral Reefs, 2012,31(2):473-485.
[7]	MULLER-PARKER G, D’ELIA C F, COOK C B. Interactions between corals and their symbiotic algae[J]. Coral reefs in the Anthropocene, 2015:99-116.
[8]	FALKOWSKI P G, DUBINSKY Z, MUSCATINE L, et al.Light and the bioenergetics of a symbiotic coral[J]. BioScience, 1984, 34(11):705-709.
[9]	GONZÁLEZ-PECH R A, BHATTACHARYA D, RAGAN M A, et al. Genome evolution of coral reef symbionts as intracellular residents[J]. Trends in Ecology&Evolution,2019, 34(9):799-806.
[10]	ROBISON J D, WARNER M E. Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium(Pyrrhophyta)[J]. Journal of Phycology, 2006, 42(3):568-579.
[11]	SUGGETT D J, WARNER M E, SMITH D J, et al. Photosynthesis and production of hydrogen peroxide by Symbiodinium(Pyrrhophyta)phylotypes with different thermal tolerances[J]. Journal of Phycology, 2008, 44(4):948-956.
[12]	MCBRIDE B B, MULLER-PARKER G, JAKOBSEN H H. Low thermal limit of growth rate of Symbiodinium californium(Dinophyta)in culture may restrict the symbiont to southern populations of its host anemones(Anthopleura spp.; Anthozoa, Cnidaria)[J]. Journal of Phycology, 2009, 45(4):855-863.
[13]	MCGINTY E S, PIECZONKA J, MYDLARZ L D. Variations in reactive oxygen release and antioxidant activity in multiple Symbiodinium types in response to elevated temperature[J]. Microbial Ecology, 2012, 64(4):1000-1007.
[14]	GILBERT C, SCHAACK S, PACE II J K, et al. A role for host-parasite interactions in the horizontal transfer of transposons across phyla[J]. Nature, 2010, 464:1347-1350.
[15]	BAKER A C, STARGER C J, MCCLANAHAN T R,et al. Corals’ adaptive response to climate change[J].Nature, 2004, 430:741.
[16]	THORNHILL D J, KEMP D W, BRUNS B U, et al. Correspondence between cold tolerance and temperate biogeography in a western Atlantic Symbiodinium(dinophyta)lineage[J]. Journal of Phycology, 2008, 44(5):1126-1135.
[17]	VOOLSTRA C R, VALENZUELA J J, TURKARSLAN S,et al. Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance[J]. Molecular Ecology, 2021,30(18):4466-4480.
[18]	ISHIKURA M, HAGIWARA K, TAKISHITA K, et al.Isolation of new Symbiodinium strains from tridacnid giant clam(Tridacna crocea)and sea slug(Pteraeolidia ianthina)using culture medium containing giant clam tissue homogenate[J]. Marine Biotechnology, 2004, 6(4):378-385.
[19]	FITT W K. Chemosensory responses of the symbiotic dinoflagellate Symbiodinium microadriaticum(Dinophyceae)[J]. Journal of Phycology, 1985, 21(1):62-67.
[20]	KRUEGER T, GATES R D. Cultivating endosymbionts-host environmental mimics support the survival of Symbiodinium C15 ex hospite[J]. Journal of Experimental Marine Biology and Ecology, 2012, 413:169-176.
[21]	BUERGER P, ALVAREZ-ROA C, COPPIN C W, et al.Heat-evolved microalgal symbionts increase coral bleaching tolerance[J]. Science Advances, 2020, 6(20):eaba2498.
[22]	张乔民,余克服,施祺,等.中国珊瑚礁分布和资源特点[C] //第二届全国海洋高新技术产业化论坛论文集.北京:中国高科技产业化研究会, 2015:176-178.
[23]	余克服.南海珊瑚礁及其对全新世环境变化的记录与响应[J].中国科学:地球科学, 2012, 42(8):1160-1172.
[24]	LIAO Z, YU K, CHEN B, et al. Spatial distribution of benthic algae in the South China Sea:responses to gradually changing environmental factors and ecological impacts on coral communities[J]. Diversity and Distributions, 2021, 27(5):929-943.
[25]	TONG H, CAI L, ZHOU G, et al. Temperature shapes coral-algal symbiosis in the South China Sea[J]. Scientific Reports, 2017, 7:40118.
[26]	XIANG T, HAMBLETON E A, DENOFRIO J C, et al.Isolation of clonal axenic strains of the symbiotic dinoflagellate Symbiodinium and their growth and host specificity[J]. Journal of Phycology, 2013, 49(3):447-458.
[27]	XIE J, CHEN Y, CAI G, et al. Tree Visualization By One Table(tvBOT):a web application for visualizing, modifying and annotating phylogenetic trees[J]. Nucleic Acids Research, 2023, 51(W1):W587-W592.
[28]	SAMPAYO E M, RIDGWAY T, BONGAERTS P, et al.Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type[J]. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(30):10444-10449.
[29]	GLYNN V M, VOLLMER S V, KLINE D I, et al. Environmental and geographical factors structure cauliflower coral's algal symbioses across the Indo-Pacific[J]. Journal of Biogeography, 2023, 50(4):669-684.
[30]	KLEPAC C N, EATON K R, PETRIK C G, et al. Symbiont composition and coral genotype determines massive coral species performance under end-of-century climate scenarios[J]. Frontiers in Marine Science, 2023, 10:1026426.
[31]	TURNHAM K E, WHAM D C, SAMPAYO E, et al.Mutualistic microalgae co-diversify with reef corals that acquire symbionts during egg development[J]. The ISME Journal, 2021, 15:3271-3285.
[32]	覃良云,许勇前,陈金妮,等.造礁石珊瑚共生虫黄藻离体培养方法的优化[J].微生物学报, 2023, 63(4):1658-1671.
[33]	WANG J, CHEN J, WANG S, et al. Monoclonal culture and characterization of Symbiodiniaceae C1 strain from the scleractinian coral Galaxea fascicularis[J]. Frontiers in Physiology, 2021, 11:1879.
[34]	ZHOU G, CAI L, LI Y, et al. Temperature-driven local acclimatization of Symbiodnium hosted by the coral Galaxea fascicularis at Hainan Island, China[J]. Frontiers in Microbiology, 2017, 8:2487.
[35]	JEONG H J, LEE S Y, KANG N S, et al. Genetics and morphology characterize the dinoflagellate Symbiodinium voratum, n. sp.,(Dinophyceae)as the sole representative of Symbiodinium Clade E[J]. The Journal of Eukaryotic Microbiology, 2014, 61(1):75-94.
[36]	BLANK R J, TRENCH R K. Speciation and symbiotic dinoflagellates[J]. Science, 1985, 229(4714):656-658.
[37]	SUGGETT D J, GOYEN S, EVENHUIS C, et al. Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation[J]. The New Phytologist, 2015, 208(2):370-381.
[38]	SUGGETT D J, MOORE C M, HICKMAN A E, et al.Interpretation of fast repetition rate(FRR)fluorescence:signatures of phytoplankton community structure versus physiological state[J]. Marine Ecology Progress Series,2009, 376:1-19.
[39]	WU Y, CAMPBELL D A, IRWIN A J, et al. Ocean acidification enhances the growth rate of larger diatoms[J].Limnology and Oceanography, 2014, 59(3):1027-1034.
[40]	LEE R E. Phycology[M]. Cambridge:Cambridge university press, 2018.
[41]	傅维洁.关于微生物比生长速率和指数生长期的讨论[J].微生物学通报, 1992, 19(2):114-115.
[42]	LITTLE A F, VAN OPPEN M J H, WILLIS B L. Flexibility in algal endosymbioses shapes growth in reef corals[J]. Science, 2004, 304(5676):1492-1494.
[43]	JONES A, BERKELMANS R. Potential costs of acclimatization to a warmer climate:growth of a reef coral with heat tolerant vs. sensitive symbiont types[J]. PLoS One,2010, 5(5):e10437.
[44]	WANG C, ZHENG X, KVITT H, et al. Lineage-specific symbionts mediate differential coral responses to thermal stress[J]. Microbiome, 2023, 11(1):211.
[45]	汪亚俊,孙明哲,李爱芬,等.不同氮素水平对产油尖状栅藻生长及光合生理的影响[J].中国生物工程杂志, 2014, 34(12):51-58.
[46]	KROMKAMP J C, FORSTER R M. The use of variable fluorescence measurements in aquatic ecosystems:differences between multiple and single turnover measuring protocols and suggested terminology[J]. European Journal of Phycology, 2003, 38(2):103-112.
[47]	ROWAN R. Thermal adaptation in reef coral symbionts[J].Nature, 2004, 430:742.

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通讯作者: 陈斌, bchen63@163.com

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沈阳化工大学材料科学与工程学院沈阳 110142

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Isolated culture and physiological characteristics of four symbiotic Symbiodiniaceae strains from South China Sea

College of Marine Science and Engineering, Hainan University, Haikou, Hainan 570228, China

Received Date: 2023-10-16

Rev Recd Date: 2023-11-19

Publish Date: 2024-07-25

Key words:

Abstract: In recent years, coral bleaching events induced by marine heat waves have occurred frequently, and Symbiodiniaceae, as algal symbionts of coral hosts, has been proved to play an important role in controlling coral environmental tolerance. In order to explore the differences among different species of Symbiodiniaceae and their physiological characteristics, four monoclonal strains of Symbiodiniaceae were isolated and obtained from different cnidaria organisms in the South China Sea, and a series of investigations were conducted on their phylogenetic, morphological and various physiological characteristics. The results exhibited that the four strains of Symbiodiniaceae were Symbiodinium（type A3, HNUA3-1）, Breviolum（type B1, HNUB1-1）, Cladocopium（type C1, HNUC1-1） and Durusdinium（type D1, HNUD1-1）, respectively. Observations by light microscopy and transmission electron microscopy revealed that the four strains had higher similarity in morphological characteristics but there were significant differences in specific growth rates, reflecting the species-specific growth characteristics. The specific growth rate of Breviolum sp. HNUB1-1 was the highest, and the cell density of Breviolum sp. HNUB1-1 was significantly higher than that of the other three strains on the 3rd, 5th and 7th day（P ＜ 0.05）, the specific growth rate of Symbiodinium sp. HNUA3-1 was second highest, the specific growth rate of Cladocopium sp. HNUC1-1 and Durusdinium sp. HNUD1-1 was the lowest, and there was no significant difference in cell density within 7 days of culture. Furthermore, different strains waere also specie-specific in maximum quantum efficiency of Photosystem II（Fv/Fm）. Under the same conditions, the Fv/Fm of the Durusdinium sp. HNUD1-1 was significantly lower than that of the other three strains, reflecting the photosynthetic and physiological characteristics of its potential heat resistance. This study provided theoretical basis for enriching the resources of Symbiodiniaceae in the South China Sea, and clarifying the differences and characteristics of the Symbiodiniaceae, which can be used to provide basic data support for the conservation and restoration of the coral reef ecosystem in the South China Sea.

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Reference (47)

[1]	MUSCATINE L, PORTER J W. Reef corals:mutualistic symbioses adapted to nutrient-poor environments[J]. BioScience, 1977, 27(7):454-460.
[2]	POCHON X, GATES R D. A new Symbiodinium clade(Dinophyceae)from soritid foraminifera in Hawai’i[J].Molecular Phylogenetics and Evolution, 2010, 56:492-497.
[3]	LAJEUNESSE T C, PARKINSON J E, GABRIELSON P W, et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts[J]. Current Biology, 2018, 28(16):2570-2580.
[4]	NITSCHKE M R, CRAVEIRO S C, BRANDÃO C, et al.Description of freudenthalidium gen. nov. and halluxium gen. nov. to formally recognize clades Fr3 and H as Genera in the family Symbiodiniaceae(Dinophyceae)[J]. Journal of Phycology, 2020, 56(4):923-940.
[5]	POCHON X, LAJEUNESSE T C. Miliolidium n. gen, a new symbiodiniacean genus whose members associate with soritid foraminifera or are free-living[J]. The Journal of Eukaryotic Microbiology, 2021:e12856.
[6]	FISHER P L, MALME M K, DOVE S. The effect of temperature stress on coral-Symbiodinium associations containing distinct symbiont types[J]. Coral Reefs, 2012,31(2):473-485.
[7]	MULLER-PARKER G, D’ELIA C F, COOK C B. Interactions between corals and their symbiotic algae[J]. Coral reefs in the Anthropocene, 2015:99-116.
[8]	FALKOWSKI P G, DUBINSKY Z, MUSCATINE L, et al.Light and the bioenergetics of a symbiotic coral[J]. BioScience, 1984, 34(11):705-709.
[9]	GONZÁLEZ-PECH R A, BHATTACHARYA D, RAGAN M A, et al. Genome evolution of coral reef symbionts as intracellular residents[J]. Trends in Ecology&Evolution,2019, 34(9):799-806.
[10]	ROBISON J D, WARNER M E. Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium(Pyrrhophyta)[J]. Journal of Phycology, 2006, 42(3):568-579.
[11]	SUGGETT D J, WARNER M E, SMITH D J, et al. Photosynthesis and production of hydrogen peroxide by Symbiodinium(Pyrrhophyta)phylotypes with different thermal tolerances[J]. Journal of Phycology, 2008, 44(4):948-956.
[12]	MCBRIDE B B, MULLER-PARKER G, JAKOBSEN H H. Low thermal limit of growth rate of Symbiodinium californium(Dinophyta)in culture may restrict the symbiont to southern populations of its host anemones(Anthopleura spp.; Anthozoa, Cnidaria)[J]. Journal of Phycology, 2009, 45(4):855-863.
[13]	MCGINTY E S, PIECZONKA J, MYDLARZ L D. Variations in reactive oxygen release and antioxidant activity in multiple Symbiodinium types in response to elevated temperature[J]. Microbial Ecology, 2012, 64(4):1000-1007.
[14]	GILBERT C, SCHAACK S, PACE II J K, et al. A role for host-parasite interactions in the horizontal transfer of transposons across phyla[J]. Nature, 2010, 464:1347-1350.
[15]	BAKER A C, STARGER C J, MCCLANAHAN T R,et al. Corals’ adaptive response to climate change[J].Nature, 2004, 430:741.
[16]	THORNHILL D J, KEMP D W, BRUNS B U, et al. Correspondence between cold tolerance and temperate biogeography in a western Atlantic Symbiodinium(dinophyta)lineage[J]. Journal of Phycology, 2008, 44(5):1126-1135.
[17]	VOOLSTRA C R, VALENZUELA J J, TURKARSLAN S,et al. Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance[J]. Molecular Ecology, 2021,30(18):4466-4480.
[18]	ISHIKURA M, HAGIWARA K, TAKISHITA K, et al.Isolation of new Symbiodinium strains from tridacnid giant clam(Tridacna crocea)and sea slug(Pteraeolidia ianthina)using culture medium containing giant clam tissue homogenate[J]. Marine Biotechnology, 2004, 6(4):378-385.
[19]	FITT W K. Chemosensory responses of the symbiotic dinoflagellate Symbiodinium microadriaticum(Dinophyceae)[J]. Journal of Phycology, 1985, 21(1):62-67.
[20]	KRUEGER T, GATES R D. Cultivating endosymbionts-host environmental mimics support the survival of Symbiodinium C15 ex hospite[J]. Journal of Experimental Marine Biology and Ecology, 2012, 413:169-176.
[21]	BUERGER P, ALVAREZ-ROA C, COPPIN C W, et al.Heat-evolved microalgal symbionts increase coral bleaching tolerance[J]. Science Advances, 2020, 6(20):eaba2498.
[22]	张乔民,余克服,施祺,等.中国珊瑚礁分布和资源特点[C] //第二届全国海洋高新技术产业化论坛论文集.北京:中国高科技产业化研究会, 2015:176-178.
[23]	余克服.南海珊瑚礁及其对全新世环境变化的记录与响应[J].中国科学:地球科学, 2012, 42(8):1160-1172.
[24]	LIAO Z, YU K, CHEN B, et al. Spatial distribution of benthic algae in the South China Sea:responses to gradually changing environmental factors and ecological impacts on coral communities[J]. Diversity and Distributions, 2021, 27(5):929-943.
[25]	TONG H, CAI L, ZHOU G, et al. Temperature shapes coral-algal symbiosis in the South China Sea[J]. Scientific Reports, 2017, 7:40118.
[26]	XIANG T, HAMBLETON E A, DENOFRIO J C, et al.Isolation of clonal axenic strains of the symbiotic dinoflagellate Symbiodinium and their growth and host specificity[J]. Journal of Phycology, 2013, 49(3):447-458.
[27]	XIE J, CHEN Y, CAI G, et al. Tree Visualization By One Table(tvBOT):a web application for visualizing, modifying and annotating phylogenetic trees[J]. Nucleic Acids Research, 2023, 51(W1):W587-W592.
[28]	SAMPAYO E M, RIDGWAY T, BONGAERTS P, et al.Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type[J]. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(30):10444-10449.
[29]	GLYNN V M, VOLLMER S V, KLINE D I, et al. Environmental and geographical factors structure cauliflower coral's algal symbioses across the Indo-Pacific[J]. Journal of Biogeography, 2023, 50(4):669-684.
[30]	KLEPAC C N, EATON K R, PETRIK C G, et al. Symbiont composition and coral genotype determines massive coral species performance under end-of-century climate scenarios[J]. Frontiers in Marine Science, 2023, 10:1026426.
[31]	TURNHAM K E, WHAM D C, SAMPAYO E, et al.Mutualistic microalgae co-diversify with reef corals that acquire symbionts during egg development[J]. The ISME Journal, 2021, 15:3271-3285.
[32]	覃良云,许勇前,陈金妮,等.造礁石珊瑚共生虫黄藻离体培养方法的优化[J].微生物学报, 2023, 63(4):1658-1671.
[33]	WANG J, CHEN J, WANG S, et al. Monoclonal culture and characterization of Symbiodiniaceae C1 strain from the scleractinian coral Galaxea fascicularis[J]. Frontiers in Physiology, 2021, 11:1879.
[34]	ZHOU G, CAI L, LI Y, et al. Temperature-driven local acclimatization of Symbiodnium hosted by the coral Galaxea fascicularis at Hainan Island, China[J]. Frontiers in Microbiology, 2017, 8:2487.
[35]	JEONG H J, LEE S Y, KANG N S, et al. Genetics and morphology characterize the dinoflagellate Symbiodinium voratum, n. sp.,(Dinophyceae)as the sole representative of Symbiodinium Clade E[J]. The Journal of Eukaryotic Microbiology, 2014, 61(1):75-94.
[36]	BLANK R J, TRENCH R K. Speciation and symbiotic dinoflagellates[J]. Science, 1985, 229(4714):656-658.
[37]	SUGGETT D J, GOYEN S, EVENHUIS C, et al. Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation[J]. The New Phytologist, 2015, 208(2):370-381.
[38]	SUGGETT D J, MOORE C M, HICKMAN A E, et al.Interpretation of fast repetition rate(FRR)fluorescence:signatures of phytoplankton community structure versus physiological state[J]. Marine Ecology Progress Series,2009, 376:1-19.
[39]	WU Y, CAMPBELL D A, IRWIN A J, et al. Ocean acidification enhances the growth rate of larger diatoms[J].Limnology and Oceanography, 2014, 59(3):1027-1034.
[40]	LEE R E. Phycology[M]. Cambridge:Cambridge university press, 2018.
[41]	傅维洁.关于微生物比生长速率和指数生长期的讨论[J].微生物学通报, 1992, 19(2):114-115.
[42]	LITTLE A F, VAN OPPEN M J H, WILLIS B L. Flexibility in algal endosymbioses shapes growth in reef corals[J]. Science, 2004, 304(5676):1492-1494.
[43]	JONES A, BERKELMANS R. Potential costs of acclimatization to a warmer climate:growth of a reef coral with heat tolerant vs. sensitive symbiont types[J]. PLoS One,2010, 5(5):e10437.
[44]	WANG C, ZHENG X, KVITT H, et al. Lineage-specific symbionts mediate differential coral responses to thermal stress[J]. Microbiome, 2023, 11(1):211.
[45]	汪亚俊,孙明哲,李爱芬,等.不同氮素水平对产油尖状栅藻生长及光合生理的影响[J].中国生物工程杂志, 2014, 34(12):51-58.
[46]	KROMKAMP J C, FORSTER R M. The use of variable fluorescence measurements in aquatic ecosystems:differences between multiple and single turnover measuring protocols and suggested terminology[J]. European Journal of Phycology, 2003, 38(2):103-112.
[47]	ROWAN R. Thermal adaptation in reef coral symbionts[J].Nature, 2004, 430:742.

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Isolated culture and physiological characteristics of four symbiotic Symbiodiniaceae strains from South China Sea

doi: 10.15886/j.cnki.rdswxb.20230117

Abstract

References

Proportional views

通讯作者: 陈斌, bchen63@163.com

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