Academic Journal
Προβολή σε EDS

Dual urea utilization enzyme systems in Symbiodiniaceae coral symbionts under warming.

Λεπτομέρειες βιβλιογραφικής εγγραφής
Τίτλος: Dual urea utilization enzyme systems in Symbiodiniaceae coral symbionts under warming.
Συγγραφείς: Li T; Guangdong Provincial Key Laboratory of Marine Disaster Prediction and Prevention, Shantou University, Shantou, 515063, China. tchli@stu.edu.cn.; Institute of Marine Sciences and Guangdong Provincial Key Laboratory of Marine Biotechnology, Shantou University, Shantou , 515063, China. tchli@stu.edu.cn., Zhang B; Guangdong Provincial Key Laboratory of Marine Disaster Prediction and Prevention, Shantou University, Shantou, 515063, China., Liang H; Guangdong Provincial Key Laboratory of Marine Disaster Prediction and Prevention, Shantou University, Shantou, 515063, China., Huang J; Guangdong Provincial Key Laboratory of Marine Disaster Prediction and Prevention, Shantou University, Shantou, 515063, China., Sun Y; State Key Laboratory of Tropical Oceanography; Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Chinese Academy of Sciences, Guangzhou, 510301, China.; CAS-HKUST Sanya Joint Laboratory of Marine Science Research and Key Laboratory of Tropical Marine Biotechnology of Hainan Province, Tropical Marine Biological Research Station in Hainan, Chinese Academy of Sciences, Sanya, 572000, China., Wei Z; State Key Laboratory of Tropical Oceanography; Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Chinese Academy of Sciences, Guangzhou, 510301, China., Manullang C; Guangdong Provincial Key Laboratory of Marine Disaster Prediction and Prevention, Shantou University, Shantou, 515063, China., Huang H; State Key Laboratory of Tropical Oceanography; Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Chinese Academy of Sciences, Guangzhou, 510301, China.; CAS-HKUST Sanya Joint Laboratory of Marine Science Research and Key Laboratory of Tropical Marine Biotechnology of Hainan Province, Tropical Marine Biological Research Station in Hainan, Chinese Academy of Sciences, Sanya, 572000, China., Lin S; Department of Marine Sciences, University of Connecticut, Groton, CT 06340, USA. senjie.lin@uconn.edu.
Πηγή: BMC biology [BMC Biol] 2026 Apr 27; Vol. 24 (1). Date of Electronic Publication: 2026 Apr 27.
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: BioMed Central Country of Publication: England NLM ID: 101190720 Publication Model: Electronic Cited Medium: Internet ISSN: 1741-7007 (Electronic) Linking ISSN: 17417007 NLM ISO Abbreviation: BMC Biol Subsets: MEDLINE
Imprint Name(s): Original Publication: [London] : BioMed Central, c2003-
Ιατρικοί όροι (MeSH): Urea*/metabolism , Dinoflagellida*/enzymology , Dinoflagellida*/genetics , Dinoflagellida*/physiology , Anthozoa*/physiology , Urease*/metabolism , Urease*/genetics , Symbiosis*, Animals ; Phylogeny
Περίληψη: Background: Urea has been shown to be important as a nitrogen (N) nutrient for coral holobionts, but the mechanism underpinning urea utilization by symbiotic algae is not fully understood. In this study, we investigated the molecular pathways underlying urea utilization in the Symbiodiniaceae family and the responses of these pathways to different N-nutrient conditions and heat stress through comprehensive genomic screening, multi-omics analysis and stable isotope pulse-chase experiments.
Results: Genome screening revealed that two urea hydrolysis systems, urease (URE) and urea amidolyase (UAL), were present in Symbiodiniaceae, positioning this lineage as one of the few non-green algae that possess UAL. Furthermore, our data reveal an interesting evolutionary trajectory of UAL. While subunit DUR2 occurs in most symbiodiniacean genomes sequenced to date, only two species (Cladocopium goreaui and Cladopium c92) possess the complete UAL system (DUR1 with DUR2). In the phylogenetic tree of UAL sequences, Symbiodiniaceae clustered more closely with coral symbiotic bacteria than with other eukaryotes, but show clear distinct genetic features such as GC content and codon usage, suggesting evolutionary horizontal gene transfer from bacteria. Furthermore, ex-hospite C. goreaui exhibited better growth and achieved higher maximum specific growth rates when urea was provided as the sole nitrogen source, compared to ammonium. Notably, when experimenting on the Cladocopium-dominating Pocillopora damicornis holobiont using 15N isotope tracer, we found that under heat stress (HS) conditions, the in-hospite Symbiodiniaceae significantly increased urea uptake but decreased NO3- and NH4+ uptake. Omics analyses suggest that responses to different nitrogen, light, and temperature conditions were more likely mediated by UAL.
Conclusions: This study reveals two distinct urea utilization systems in the coral ecosystem and their differential responses to warming, highlighting the importance of urea as N-nutrient when facing global warming.
(© 2026. The Author(s).)
Competing Interests: Declarations. Ethics approval and consent to participate: Not applicable. Consent for publication: All authors have read and approved the final version of the submitted manuscript, and all co-authors consent to the publication of this work in BMC Biology, including all associated supplementary materials. Competing interests: The authors declare no competing interests.
References: Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Jackson JBC, et al. Global trajectories of the long-term decline of coral reef ecosystems. Science. 2003;301:955–8. (PMID: 1292029610.1126/science.1085706)
Hughes TP, Barnes ML, Bellwood DR, Cinner JE, Cumming GS, Jackson JB, et al. Coral reefs in the Anthropocene. Nature. 2017;546:82–90. (PMID: 2856980110.1038/nature22901)
Rädecker N, Pogoreutz C, Voolstra CR, Wiedenmann J, Wild C. Nitrogen cycling in corals: the key to understanding holobiont functioning? Trends Microbiol. 2015;23:490–7. (PMID: 2586868410.1016/j.tim.2015.03.008)
Cui G, Liew YJ, Konciute MK, Zhang Y, Hung S, Thistle H. Nutritional control regulates symbiont proliferation and life history in coral-dinoflagellate symbiosis. BMC Biol. 2022;20:103. (PMID: 35549698910292010.1186/s12915-022-01306-2)
Lema KA, Clouard V, Warner ME, Pettay DT, Van Oppen MJH. Coral mass spawning predicted by rapid seasonal rise in ocean temperature. Proc R Soc B Biol Sci. 2016;281:20160011.
Bourne DG, Morrow KM, Webster NS. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu Rev Microbiol. 2016;70:317–40. (PMID: 2748274110.1146/annurev-micro-102215-095440)
Muscatine L, Porter JW. Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience. 1977;27:454–60. (PMID: 10.2307/1297526)
LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol. 2018;28:2570–80. (PMID: 3010034110.1016/j.cub.2018.07.008)
Wham DC, Carmichael M, LaJeunesse TC. Microsatellite loci for Symbiodinium goreaui and other Clade C Symbiodinium. Conserv Genet Resour. 2014;6:127–9. (PMID: 10.1007/s12686-013-0023-5)
Yang Y, Zhou H, Yao X, Yao X, Qiao L, Geng T, et al. Molecular diversity and biogeography of symbiotic algae in dominant scleractinian corals around Hainan Island. Reg Stud Mar Sci. 2024;73:103487.
Baker AC, Starger CJ, McClanahan TR, Glynn PW. Corals’ adaptive response to climate change. Nature. 2004;430:741. (PMID: 1530679910.1038/430741a)
Wall CB, Kalunhiokalani M, Popp BN, Donahue MJ, Gates RD. Divergent symbiont communities determine the physiology and nutrition of a reef coral across a light-availability gradient. ISME J. 2020;14:945–58. (PMID: 31900444708233610.1038/s41396-019-0570-1)
McIlroy SE, Wong JCY, Baker DM. Competitive traits of coral symbionts may alter the structure and function of the microbiome. ISME J. 2020;14:2424–32. (PMID: 32518247749036910.1038/s41396-020-0697-0)
Morgans CA, Hung JY, Bourne DG, Quigley KM. Symbiodiniaceae probiotics for use in bleaching recovery. Restor Ecol. 2020;28:282–8. (PMID: 10.1111/rec.13069)
Quigley KM, Alvarez Roa C, Beltran VH, Leggat B, Willis BL. Experimental evolution of the coral algal endosymbiont, Cladocopium goreaui: Lessons learnt across a decade of stress experiments to enhance coral heat tolerance. Restor Ecol. 2021;29:e13342. (PMID: 10.1111/rec.13342)
Li T, Huang J, Du H, Liu X, Zhong C, Lin S. Coral bleaching from a nutrient perspective is understudied: A bibliometric survey. Front Mar Sci. 2022;9:926783. (PMID: 10.3389/fmars.2022.926783)
Xiang T, Lehnert E, Jinkerson RE, Clowez S, Kim R, DeNofrio JC, et al. Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-Cnidarian associations. Nat Commun. 2020;11:108. (PMID: 31913264694930610.1038/s41467-019-13963-z)
Oliveira CYB, Brandão B, Jannuzzi LGS, Oliveira DW, Yogui GT. New insights on the role of nitrogen in the resistance to environmental stress in an endosymbiotic dinoflagellate. Environ Sci Pollut Res. 2023;30:82142–51. (PMID: 10.1007/s11356-023-28228-y)
Crehan O, Davy SK, Grover R, Ferrier-Pagès C. Nutrient depletion and heat stress impair the assimilation of nitrogen compounds in a scleractinian coral. J Exp Biol. 2024;227:jeb246466. (PMID: 3856329210.1242/jeb.246466)
Li T, Chen X, Lin S. Physiological and transcriptomic responses to N-deficiency and ammonium: nitrate shift in Fugacium kawagutii (Symbiodiniaceae). Sci Total Environ. 2021;753:141906. (PMID: 3289087310.1016/j.scitotenv.2020.141906)
Li T, Yu L, Chen X, Lin X, Li L, Guo C, et al. Remarkable metabolic reconfiguration due to N deficiency and an ammonium-to-nitrate shift in the free-living Effrenium voratum (Symbiodiniaceae). J Geophys Res Biogeosci. 2021;126:e2020JG006172. (PMID: 10.1029/2020JG006172)
Babbin AR, Tamasi T, Dumit D, Weber L, Rodríguez MVI, Schwartz SL, et al. Discovery and quantification of anaerobic nitrogen metabolisms among oxygenated tropical Cuban stony corals. ISME J. 2021;15:1222–35. (PMID: 3334299910.1038/s41396-020-00845-2)
McCarthy JJ. The uptake of urea by natural populations of marine phytoplankton. Limnol Oceanogr. 1972;17:738–48. (PMID: 10.4319/lo.1972.17.5.0738)
Cornell SE, Jickells TD, Cape JN, Rowland AP, Duce RA. Organic nitrogen deposition on land and coastal environments: a review of methods and data. Atmos Environ. 2003;37:2173–91. (PMID: 10.1016/S1352-2310(03)00133-X)
Grover R, Maguer JF, Allemand D, Ferrier-Pagès C. Urea uptake by the scleractinian coral Stylophora pistillata. J Exp Mar Biol Ecol. 2006;332:216–25. (PMID: 10.1016/j.jembe.2005.11.020)
Glibert PM, Harrison J, Heil C, Seitzinger S. Escalating worldwide use of urea-a global change contributing to coastal eutrophication. Biogeochemistry. 2006;77:441–63. (PMID: 10.1007/s10533-005-3070-5)
Solomon CM, Collier JL, Berg GM, Glibert PM. Role of urea in microbial metabolism in aquatic systems: a biochemical and molecular review. Aquat Microb Ecol. 2010;59:67–88. (PMID: 10.3354/ame01390)
Barnes DJ, Crossland CJ. Urease activity in the staghorn coral, Acropora acuminata. Comp Biochem Physiol B Biochem Mol Biol. 1976;55:371–6.
Crandall JB, Teece MA. Urea is a dynamic pool of bioavailable nitrogen in coral reefs. Coral Reefs. 2012;31:207–14. (PMID: 10.1007/s00338-011-0836-1)
Biscéré T, Ferrier-Pages C, Grover R, Glibert A, Rottier C, Wright A, et al. Enhancement of coral calcification via the interplay of nickel and urease. Aquat Toxicol. 2018;200:247–56. (PMID: 2980316510.1016/j.aquatox.2018.05.013)
Strope PK, Nickerson KW, Harris SD, Moriyama EN. Molecular evolution of urea amidolyase and urea carboxylase in fungi. BMC Evol Biol. 2011;11:80. (PMID: 21447149307391210.1186/1471-2148-11-80)
Liang H, Li T, Chen Y, Wang J, Aslam M, Qin H, et al. Urea amidolyase as the enzyme for urea utilization in algae: functional display in Chlamydomonas reinhardtii and evolution in algae. Mol Ecol. 2025;34:e17734. (PMID: 4011070110.1111/mec.17734)
Qin Y, Cabral JMS. Review properties and applications of urease. Biocatal Biotransform. 2002;20:1–14. (PMID: 10.1080/10242420210154)
Navarathna DHMLP, Harris SD, Roberts DD, Nickerson KW. Evolutionary aspects of urea utilization by fungi. FEMS Yeast Res. 2010;10:209–13. (PMID: 20100286282288010.1111/j.1567-1364.2009.00602.x)
Sumner JB. The isolation and crystallization of the enzyme urease: preliminary paper. In: Source Book in Chemistry, 1900–1950. Harvard University Press; 1926. p. 322–7.
Dixon NE, Gazzola C, Blakeley RL, Zerner B. Jack bean urease (EC 3.5.1.5). Metalloenzyme. Simple biological role for nickel. J Am Chem Soc. 1975;97:4131–3. (PMID: 115921610.1021/ja00847a045)
Ip YK, Teng GCY, Boo MV, Poo JST, Hiong KC, Kim H, et al. Symbiodiniaceae dinoflagellates express urease in three subcellular compartments and upregulate its expression levels in situ in three organs of a giant clam (Tridacna squamosa) during illumination. J Phycol. 2020;56:1696–711. (PMID: 3272578410.1111/jpy.13053)
Hodson RC, Williams SK, Davidson WR Jr. Metabolic control of urea catabolism in Chlamydomonas reinhardi and Chlorella pyrenoidosa. J Bacteriol. 1975;121:1022–35. (PMID: 111699424603210.1128/jb.121.3.1022-1035.1975)
Roon RJ, Hampshire J, Levenberg B. Urea amidolyase. J Biol Chem. 1972;247:7539–45. (PMID: 456456610.1016/S0021-9258(19)44559-6)
Lin Y, Boese CJ, St MM. The urea carboxylase and allophanate hydrolase activities of urea amidolyase are functionally independent. Protein Sci. 2016;25:1812–24. (PMID: 27452902502953110.1002/pro.2990)
Leftley JW, Syrett PJ. Urease and ATP: urea amidolyase activity in unicellular algae. J Gen Microbiol. 1973;77:109–15. (PMID: 10.1099/00221287-77-1-109)
Al-Houty FAA, Syrett PJ. The occurrence of urease/urea amidolyase and glycollate oxidase/dehydrogenase in Klebsormidium spp. and members of the Ulotrichales. Br Phycol J. 1984;19:1–10. (PMID: 10.1080/00071618400650011)
Manullang C, Huang J, Lin W, Liang H, Du H, Li T. Physiological and molecular responses to urea environment in Cladocopium goreaui (Symbiodiniaceae). Environ Res. 2025;273:121239. (PMID: 4002085810.1016/j.envres.2025.121239)
Trench RK, Blank RJ. Symbiodinium microadriaticum Freudenthal, S. goreauii sp. nov., S. kawagutii sp. nov. and S. pilosum sp. nov.: gymnodinioid dinoflagellate symbionts of marine invertebrates. J Phycol. 1987;23:469–81. (PMID: 10.1111/j.1529-8817.1987.tb02534.x)
Liu H, Stephens TG, Gonzalez-Pech RA, Beltran VH, Lapeyre B, Bongaerts P, et al. Symbiodinium genomes reveal adaptive evolution of functions related to symbiosis. Commun Biol. 2018;1:95. (PMID: 30271976612363310.1038/s42003-018-0098-3)
Chen Y, Shah S, Dougan KE, Van Oppen MJ, Bhattacharya D, Chan CX. Improved Cladocopium goreaui genome assembly reveals features of a facultative coral symbiont and the complex evolutionary history of dinoflagellate genes. Microorganisms. 2022;10:1662. (PMID: 36014080941297610.3390/microorganisms10081662)
Thornhill DJ, Xiang Y, Pettay DT, Zhong M, Santos SR. Population genetic data of a model symbiotic cnidarian system reveal remarkable symbiotic specificity and vectored introductions across ocean basins. Mol Ecol. 2013;22:4499–515. (PMID: 2398076410.1111/mec.12416)
Saad OS, Lin X, Ng TY, Li L, Ang P, Lin S. Species richness and generalists-specialists mosaicism of symbiodiniacean symbionts in corals from Hong Kong revealed by high-throughput ITS sequencing. Coral Reefs. 2022;41:1–12. (PMID: 10.1007/s00338-021-02196-6)
Su Y, Zhang K, Zhou Z, Wang J, Yang X, Tang J, et al. Microplastic exposure represses the growth of endosymbiotic dinoflagellate Cladocopium goreaui in culture through affecting its apoptosis and metabolism. Chemosphere. 2020;244:125485. (PMID: 3180992910.1016/j.chemosphere.2019.125485)
Lin S. Genomic understanding of dinoflagellates. Res Microbiol. 2011;162:551–69. (PMID: 2151437910.1016/j.resmic.2011.04.006)
Lin S. A decade of dinoflagellate genomics illuminating an enigmatic eukaryote cell. BMC Genomics. 2024;25:932. (PMID: 393673461145309110.1186/s12864-024-10847-5)
Morse D, Salois P, Markovic P, Hastings JW. A nuclear-encoded form II RuBisCo in dinoflagellates. Science. 1995;268:1622–4. (PMID: 777786110.1126/science.7777861)
Lin S, Zhang H, Zhuang Y, Tran B, Gill J. Spliced leader-based metatranscriptomic analyses lead to recognition of hidden genomic features in dinoflagellates. Proc Natl Acad Sci U S A. 2010;107:20033–8. (PMID: 21041634299334310.1073/pnas.1007246107)
Santos EO, Alves NJ, Dias GM, Mazotoo AM, Vermelho A, Vora GJ, et al. Genomic and proteomic analyses of the coral pathogen Vibrio coralliilyticus reveal a diverse virulence repertoire. ISME J. 2011;5:1471–83. (PMID: 21451583316067710.1038/ismej.2011.19)
González-Pech RA, Stephens TG, Chen Y, Mohamed AR, Cheng Y, Shah S, et al. Comparison of 15 dinoflagellate genomes reveals extensive sequence and structural divergence in family Symbiodiniaceae and genus Symbiodinium. BMC Biol. 2021;19:73. (PMID: 33849527804528110.1186/s12915-021-00994-6)
He J, Huang Y, Li L, Lin S, Ma M, Wang Y. Novel plastid genome characteristics in Fugacium kawagutii and the trend of accelerated evolution of plastid proteins in dinoflagellates. Genome Biol Evol. 2024;16:evad237. (PMID: 3815559610.1093/gbe/evad237)
Solomon CM, Glibert PM. Urease activity in five phytoplankton species. Aquat Microb Ecol. 2008;52:149–57. (PMID: 10.3354/ame01213)
Xu J, Zhang Q, Chen M, Ge X, Ren J, Qin D. Chemical composition, sources, and processes of urban aerosols during summertime in Northwest China: insights from high-resolution aerosol mass spectrometry. Atmos Chem Phys. 2014;14:12593–611. (PMID: 10.5194/acp-14-12593-2014)
Huang K, Feng Q, Zhang Y, Ou L, Cen J, Lu S, et al. Comparative uptake and assimilation of nitrate, ammonium, and urea by dinoflagellate Karenia mikimotoi and diatom Skeletonema costatum s.l. in the coastal waters of the East China Sea. Mar Pollut Bull. 2020;155:111200.
Glibert PM, Wilkerson FP, Dugdale RC, Raven JA, Dupont CL, Leavitt PR, et al. Pluses and minuses of ammonium and nitrate uptake and assimilation by phytoplankton and implications for productivity and community composition, with emphasis on nitrogen-enriched conditions. Limnol Oceanogr. 2016;61:165–97. (PMID: 10.1002/lno.10203)
Lin S, Litaker RW, Sunda WG. Phosphorus physiological ecology and molecular mechanisms in marine phytoplankton. J Phycol. 2016;52:10–36. (PMID: 2698708510.1111/jpy.12365)
Allen AE, Dupont CL, Oborník M, Horák A, Nunes-Nesi A, McCrow JP, et al. Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature. 2011;473:203–7. (PMID: 2156256010.1038/nature10074)
Ludwig M, Bryant DA. Acclimation of the global transcriptome of the CyanobacteriumSynechococcus sp. strain PCC 7002 to nutrient limitations and different nitrogen sources. Front Microbiol. 2012;3:145. (PMID: 22514553332387210.3389/fmicb.2012.00145)
Veaudor T, Cassier-Chauvat C, Chauvat F. Genomics of urea transport and catabolism in cyanobacteria: biotechnological implications. Front Microbiol. 2019;10:2502. (PMID: 10.3389/fmicb.2019.02052)
Huang Y, He J, Wang Y, Li L, Lin S. Nitrogen source type modulates heat stress response in coral symbiont (Cladocopium goreaui). Appl Environ Microbiol. 2024;91:e00591-24. (PMID: 10.1128/aem.00591-24)
Xiang T, Jinkerson RE, Clowez S, Tran C, Krediet CJ, Onishi M, et al. Glucose-induced trophic shift in an endosymbiont dinoflagellate with physiological and molecular consequences. Plant Physiol. 2018;176:1793–807. (PMID: 2921759410.1104/pp.17.01572)
Ezzat L, Fine M, Maguer JF, Grover R, Ferrier-Pagès C. Carbon and nitrogen acquisition in shallow and deep holobionts of the scleractinian coral S. pistillata. Front Mar Sci. 2017;4:1–12. (PMID: 10.3389/fmars.2017.00102)
Rädecker N, Pogoreutz C, Gegner HM, Cárdenas A, Roth F, Bougoure J, et al. Heat stress destabilizes symbiotic nutrient cycling in corals. Proc Natl Acad Sci U S A. 2021;118:e2022653118. (PMID: 33500354786514710.1073/pnas.2022653118)
Fan C, Glibert PM, Alexander J, Lomas MW. Characterization of urease activity in three marine phytoplankton species, Aureococcus anophagefferens, Prorocentrum minimum, and Thalassiosira weissflogii. Mar Biol. 2003;142:949–58. (PMID: 10.1007/s00227-003-1017-8)
Peers SG, Milligan AJ, Harrison PJ. Assay optimization and regulation of urease activity in two marine diatoms. J Phycol. 2000;36:523–8. (PMID: 2954401310.1046/j.1529-8817.2000.99037.x)
Shah S, Chan,CX. Eff renium voratum genomes and genes. The University of Queensland. Data Collection. 2023. https://doi.org/10.48610/1f0377a .
Yu L, Li T, Li L, Lin X, Li H, Liu C, et al. SAGER: a database of Symbiodiniaceae and algal genomic resource. Database. 2020;2020:baaa051. (PMID: 32621601733488910.1093/database/baaa051)
Lai F, Li C, Zhang Y, Li Y, Wang Y, Zhou Q, et al. DinoSource: a comprehensive database of dinoflagellate genomic resources. Plant Biotechnol J. 2025;23:2648–50. (PMID: 4021497110.1111/pbi.70054)
Li K, Lin W, Song D, Liu C, Syaifudin M, Huang J, et al. Complete genome sequencing of 18 urea-utilizing Vibrio strains isolated from coral. Sci Data. 2025;12:1718. (PMID: 411682471257570510.1038/s41597-025-06001-9)
Guillard RRL, Hargraves PE. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia. 1993;32:234–6. (PMID: 10.2216/i0031-8884-32-3-234.1)
Hu Z, Duan S, Xu N, Mulholland MR. Growth and nitrogen uptake kinetics in cultured Prorocentrum donghaiense. PLoS One. 2014;9:e94030. (PMID: 24710151397798710.1371/journal.pone.0094030)
Monod J. Recherches sur la croissance des cultures bactériennes. Actual Sci Ind. 1942;911:1–215.
Sheng HX, Wan XS, Zou B, Sun Y, Hanoch B, Zou W, et al. An efficient diazotroph-derived nitrogen transfer pathway in coral reef system. Limnol Oceanogr. 2023;68:963–81. (PMID: 10.1002/lno.12324)
Tanaka Y, Suzuki A, Sakai K. The stoichiometry of coral-dinoflagellate symbiosis: carbon and nitrogen cycles are balanced in the recycling and double translocation system. ISME J. 2018;12:860–8. (PMID: 29330535586421410.1038/s41396-017-0019-3)
Li T, Liu G, Yuan H, Chen J, Lin X, Li H, et al. Eukaryotic plankton community assembly and influencing factors between continental shelf and slope sites in the northern South China Sea. Environ Res. 2023;216:114584. (PMID: 3627053210.1016/j.envres.2022.114584)
Quigley KM, Davies SW, Kenkel CD, Willis BL, Matz MV, Bay LK. Deep-sequencing method for quantifying background abundances of Symbiodinium types: exploring the rare Symbiodinium biosphere in reef-building corals. PLoS One. 2014;9:e94297. (PMID: 24728373398413410.1371/journal.pone.0094297)
Magoc T, Salzberg S. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011;27:2957–63. (PMID: 21903629319857310.1093/bioinformatics/btr507)
Shi T, Niu G, Kvitt H, Zheng X, Qin Q, Sun D, et al. Untangling ITS2 genotypes of algal symbionts in zooxanthellate corals. Mol Ecol Resour. 2021;21:137–52. (PMID: 3287638010.1111/1755-0998.13250)
Li T, Yu L, Song B, Song Y, Li L, Lin X, et al. Genome improvement and core gene set refinement of Fugacium kawagutii. Microorganisms. 2020;8:102. (PMID: 31940756702307910.3390/microorganisms8010102)
Aranda M, Li Y, Liew YJ, Baumgarten S, Simakov O, Wilson MC, et al. Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Sci Rep. 2016;6:39734. (PMID: 28004835517791810.1038/srep39734)
Cunning R, Bay RA, Gillette P, Baker AC, Traylor-Knowles N. Comparative analysis of the Pocillopora damicornis genome highlights role of immune system in coral evolution. Sci Rep. 2018;8:16134. (PMID: 30382153620841410.1038/s41598-018-34459-8)
Grabherr MG, Haas BJ, Yassour M, Levin ZZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29:644–52. (PMID: 21572440357171210.1038/nbt.1883)
Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011;12:323. (PMID: 21816040316356510.1186/1471-2105-12-323)
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550. (PMID: 25516281430204910.1186/s13059-014-0550-8)
Grant Information: 42206116 Natural Science Foundation of China grants; 2024A1515011467 Natural Science Foundation of Guangdong Province; LTMB202302 Key Laboratory of Tropical Marine Biotechnology of Hainan Province open fund; MELRS2325 MEL Visiting Fellowship of the State Key Laboratory of Marine Environmental Science; FJHY-YYKJ-2024-1-18-6 Fujian Province Marine Service and Fishery High-Quality Development Special Fund Project
Contributed Indexing: Keywords: Climate change; Nitrogen; Symbiodiniaceae; Urea; Urea amidolyase; Urease
Molecular Sequence: BioProject PRJNA1163438; PRJNA1198500
Substance Nomenclature: 8W8T17847W (Urea)
EC 3.5.1.5 (Urease)
Entry Date(s): Date Created: 20260428 Date Completed: 20260613 Latest Revision: 20260805
Update Code: 20260805
PubMed Central ID: PMC13255410
DOI: 10.1186/s12915-026-02610-x
PMID: 42046096
Βάση Δεδομένων: MEDLINE
Περιγραφή
ISSN:1741-7007
DOI:10.1186/s12915-026-02610-x