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Glycerol outflow in Symbiodinium under osmotic and nitrogen stress

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Abstract

In marine nutrient-poor environments, the success of Symbiodinium–cnidarian symbioses depends on the translocation of photosynthetically fixed carbon to the host. However, the mechanisms involved in this translocation are not well understood. Glycerol has been identified in the literature as one of the main photosynthates translocated from symbiont to host. Considering that glycerol is a preferred regulatory osmolyte in many unicellular eukaryotes and exposure of isolated symbionts to host homogenate results in the liberation of glycerol, we investigated the potential role of glycerol and its release in Symbiodinium. We studied the response to high osmolarity in two cultured species of Symbiodinium, examining glycerol production, specific activity of the enzyme glycerol 3-phosphate dehydrogenase and expression of the coding gene. We also assessed the production of glycerol and glucose under osmotic stress and nitrogen depletion. Results showed that cells exposed to high osmolarity conditions induced the synthesis of glycerol, although it was not retained effectively inside cells. In addition, nitrogen depletion also induced the synthesis of glycerol, although values were an order of magnitude lower. Interestingly, a significant decrease in glucose levels was detected in osmotically stressed cultures and under low nitrogen, possibly associated with the storage of carbon. While glycerol is a metabolite induced by osmotic stress, our results do not support its role as osmolyte. We conclude that glycerol may have a role as a sink for reducing power to prevent feedback inhibition of photosynthesis, particularly under low nitrogen, conditions that may be prevalent in the symbiosis.

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References

  • Andersen CL, Jensen JL, Orntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64:5245–5250. doi:10.1158/0008-5472.CAN-04-0496

    Article  CAS  Google Scholar 

  • André L, Hemming A, Adler L (1991) Osmoregulation in Saccharomyces cerevisiae. Studies on the osmotic induction of glycerol production and glycerol 3-phosphate dehydrogenase (NAD+). FEBS Lett 286:13–17. doi:10.1016/0014-5793(91)80930-2

    Article  Google Scholar 

  • Bayer T, Aranda M, Sunagawa S, Yum LK, DeSalvo MK et al (2012) Symbiodinium transcriptomes: genome insights into the dinoflagellate symbionts of reef-building corals. PLoS One 7(4):e35269. doi:10.1371/journal.pone.0035269

    Article  CAS  Google Scholar 

  • Ben-Amotz A, Avron M (1983) Accumulation of metabolites by halotolerant algae and its industrial potential. Annu Rev Microbiol 37:95–119. doi:10.1146/annurev.mi.37.100183.000523

    Article  CAS  Google Scholar 

  • Bergmeyer J, Graβl M (1987) Methods of enzymatic analysis. Vol III. Enzymes I. Oxydorreductases, transferases. VCH Publishers, New York. ISSN: 3527260439

  • Blank RJ (1987) Cell architecture of the dinoflagellate Symbiodinium sp. inhabiting the Hawaiian stony coral Montastrea verrucosa. Mar Biol 94:143–155. doi:10.1007/BF00392906

    Article  Google Scholar 

  • Burch TA, Adams WW III, Degrenne BLS, Englert CH, Mines BR et al (2015) Environmental manipulation of growth and energy carrier release from freshwater and marine Chlamydomonas species. J Appl Phycol 27:1127–1136. doi:10.1007/s10811-014-0433-0

    Article  CAS  Google Scholar 

  • Burriesci MS, Raab TK, Pringle JR (2012) Evidence that glucose is the major transferred metabolite in dinoflagellate–cnidarian symbiosis. J Exp Biol 215:3467–3477. doi:10.1242/jeb.070946

    Article  CAS  Google Scholar 

  • Chapin FS (1991) Integrated responses of plants to stress. Bioscience 41:29–36. doi:10.2307/1311538

    Article  Google Scholar 

  • Chen H, Jiang J-G (2009) Osmotic responses of Dunaliella to the changes of salinity. J Cell Physiol 219:251–258. doi:10.1002/jcp.21715

    Article  CAS  Google Scholar 

  • Colombo-Pallota MF, Rodríguez-Román A, Iglesias-Prieto R (2010) Calcification in bleached and unbleached Montastraea faveolata: evaluating the role of oxygen and glycerol. Coral Reefs 29:899–907. doi:10.1007/s00338-010-0638-x

    Article  Google Scholar 

  • Cook CB, D’Elia CF (1987) Are natural populations of zooxanthellae ever nutrient limited? Symbiosis 4:199–211

    Google Scholar 

  • Cook CB, D’Elia CF, Muller-Parker G (1988) Host feeding and nutrient sufficiency for zooxanthellae in the sea anemone Aiptasia pallida. Mar Biol 98:253–262. doi:10.1007/BF00391203

    Article  CAS  Google Scholar 

  • Cook CB, Muller-Parker G, Orlandini CD (1994) Ammonium enhancement of dark carbon fixation and nitrogen limitation in zooxanthellae symbiotic with the reef corals Madracis mirabilis and Montastrea annularis. Mar Biol 118:157–165. doi:10.1007/BF00699230

    Article  CAS  Google Scholar 

  • Dagenais BS, Dorion S, Rivoal J, Morse D (2014) The dinoflagellate Lingulodinium polyedrum responds to N depletion by a polarized deposition of starch and lipid bodies. PLoS One 9(11):e111067. doi:10.1371/journal.pone.0111067

    Article  Google Scholar 

  • Davy SK, Cook CB (2001a) The relationship between nutritional status and carbon flux in the zooxanthellate sea anemone Aiptasia pallida. Mar Biol 139:999–1005. doi:10.1007/s002270100640

    Article  CAS  Google Scholar 

  • Davy SK, Cook CB (2001b) The influence of ‘host release factor’ on carbon release by zooxanthellae isolated from fed and starved Aipatsia pallida (Verril). Comp Biochem Physiol Part A 129:487–494. doi:10.1016/S1095-6433(01)00285-9

    Article  CAS  Google Scholar 

  • Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Rev 76:229–261. doi:10.1128/MMBR.05014-11

    Article  CAS  Google Scholar 

  • Dubinsky Z, Jokiel PL (1994) Ratios of energy and nutrient fluxes regulates symbiosis between zooxanthellae and corals. Pac Sci 48:313–324

    Google Scholar 

  • Ezzat L, Magger JF, Grover R, Ferrier-Pagès C (2015) New insights into carbon acquisition and exchanges within the coral-dinoflagellate symbiosis under NH4 + and NO3 – supply. Proc R Soc B 282:20150610. doi:10.1098/rspb.2015.0610

    Article  Google Scholar 

  • Falkowski PG, Dubinzky Z, Muscatine L, McCloskey LR (1993) Population control in symbiotic corals. Bioscience 43:606–611. doi:10.2307/1312147

    Article  Google Scholar 

  • Ferrier-Pagès C, Gattuso JP, Dallot S, Jaubert J (2000) Effect of nutrient enrichment on growth and photosynthesis of the zooxanthellate coral Stylophora pistillata. Coral Reefs 19:103–113. doi:10.1007/s003380000078

    Article  Google Scholar 

  • Gancedo C, Gancedo JM, Sols A (1968) Glycerol metabolism in yeasts. Pathways of utilization and production. Eur J Biochem 5:165–172. doi:10.1111/j.1432-1033.1968.tb00353.x

    Article  CAS  Google Scholar 

  • Goiran C, Allemand D, Galgani I (1997) Transient Na+ stress in symbiotic dinoflagellates after isolation from coral-host cells and subsequent immersion in seawater. Mar Biol 129:581–589. doi:10.1007/s002270050199

    Article  CAS  Google Scholar 

  • Goyal A (2007) Osmoregulation in Dunaliella, part II: photosynthesis and starch contribute carbon for glycerol synthesis during a salt stress in Dunaliella tertiolecta. Plant Physiol Biochem 45:705–710. doi:10.1016/j.plaphy.2007.05.009

    Article  CAS  Google Scholar 

  • Grant AJ, Rémond M, People J, Hinde R (1997) Effects of host tissue homogenate of the scleractinian coral Plesiastrea versipora on glycerol metabolism in isolated symbiotic dinoflagellates. Mar Biol 128:665–670. doi:10.1007/s002270050133

    Article  CAS  Google Scholar 

  • Grant AJ, Rémond M, Hinde R (1998) Low molecular-weight factor from Plesiastrea versipora (Scleractinia) that modifies release and glicerol metabolism of isolated symbiotic algae. Mar Biol 130:553–557. doi:10.1007/s002270050276

    Article  CAS  Google Scholar 

  • Grant A, People J, Rémond M, Frankland S, Hinde R (2013) How a host cell signaling molecule modifies carbon metabolism in symbionts of the coral Plesiastrea versipora. FEBS J 280:2085–2096. doi:10.1111/febs.12233

    Article  CAS  Google Scholar 

  • Grover R, Maguer JF, Reynaud-Vaganay S, Ferrier-Pagès C (2002) Uptake of ammonium by the scleractinian coral Stylophora pistillata: effect of feeding, light, and ammonium concentrations. Limnol Oceanogr 47:782–790. doi:10.4319/lo.2002.47.3.0782

    Article  Google Scholar 

  • He Y, Meng X, Fan Q, Sun X, Xu Z et al (2009) Cloning and characterization of two novel chloroplastic glycerol 3-phosphate dehydrogenases from Dunaliella viridis. Plant Mol Biol 71:193–205. doi:10.1007/s11103-009-9517-7

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O, Hinde R (1986) Studies on a nudibranch that contains zooxanthellae I. Photosynthesis, respiration and the translocation of newly fixed carbon by zooxanthellae in Pteraeolidia ianthina. Proc R Soc Lond B 228:493–509. doi:10.1098/rspb.1986.0066

    Article  Google Scholar 

  • Holocomb M, Tambutté E, Allemand D, Tambutté S (2014) Light enhanced calcification in Stylophora pistillata: effects of glucose, glycerol and oxygen. PeerJ 2:e375. doi:10.7717/peerj.375

    Article  Google Scholar 

  • Islas-Flores T, Guillén G, Alvarado-Affantranger X, Lara-Flores M, Sánchez F, Villanueva MA (2011) PvRACK1 loss-of-function impairs cell expansion and morphogenesis in Phaseolus vulgaris L. root nodules. Mol Plant Microbe Interact 24:819–826. doi:10.1094/MPMI-11-10-0261

    Article  CAS  Google Scholar 

  • Jiang P-L, Pasaribu B, Chen C-S (2014) Nitrogen-deprivation elevates lipid levels in Symbiodinium spp. by lipid droplet accumulation: morphological and compositional analyses. PLoS One 9(1):e87416. doi:10.1371/journal.pone.0087416

    Article  Google Scholar 

  • Kremer BR (1980) Taxonomic implications of algal photoassimilate patterns. Br Phycol J 15:399–409

    Article  Google Scholar 

  • Kremer BP, Schmaljohann R, Röttger R (1980) Features and nutritional significance of photosynthates produced by unicellular algae symbiotic with larger foraminifera. Mar Ecol Prog Ser 2:225–228

    Article  CAS  Google Scholar 

  • LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol 37:866–880. doi:10.1046/j.1529-8817.2001.01031.x

    Article  CAS  Google Scholar 

  • LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400. doi:10.1007/s00227-002-0829-2

    Article  Google Scholar 

  • Leggat W, Yellowlees D, Medina M (2011) Recent progress in Symbiodinium transcriptomics. J Exp Mar Biol Ecol 408:120–125. doi:10.1016/j.jembe.2011.07.032

    Article  CAS  Google Scholar 

  • León R, Galván F (1994) Halotolerance studies in Chlamydomonas reinhardtii: glycerol excretion by free and immobilized cells. J Appl Phycol 6:13–20. doi:10.1007/BF02185898

    Article  Google Scholar 

  • Lipschultz F, Cook C (2002) Uptake and assimilation of 15N-ammonium by the symbiotic sea anemones Bartholomea annulata and Aiptasia pallida: conservation versus recycling of nitrogen. Mar Biol 140:489–502. doi:10.1007/s00227-001-0717-1

    Article  CAS  Google Scholar 

  • Liska AJ, Shevchenko A, Pick U, Katz A (2004) Enhanced photosynthesis and redox energy production contribute to salinity tolerance in Dunaliella as revealed by homology-based proteomics. Plant Physiol 136:2806–2817. doi:10.1104/pp.104

    Article  CAS  Google Scholar 

  • Luo YJ, Wang LH, Chen WNU, Peng SE et al (2009) Ratiometric imaging of gastrodermal lipid bodies in coral-dinoflagellate endosymbiosis. Coral Reefs 28:289–301. doi:10.1007/s00338-008-0462-8

    Article  Google Scholar 

  • McGuire MP, Szmant AM (1997) Time course of physiological responses to NH4 enrichment by a coral-zooxanthellae symbiosis.In: Proc 8th Int Coral Reef Symp, vol 1. pp 909–914

  • Muller-Parker G, Lee K, Cook CB (1996) Changes in the ultrastructure of symbiotic zooxanthellae (Symbiodinium sp., Dinophyceae) in fed and starved sea anemones maintained under high light and low light. J Phycol 32:987–994. doi:10.1111/j.0022-3646.1996.00987.x

    Article  Google Scholar 

  • Muscatine L (1967) Glycerol excretion by symbiotic algae from corals and Tridacna and its control by the host. Science 156:516–519. doi:10.1126/science.156.3774.516

    Article  CAS  Google Scholar 

  • Muscatine L, Hand C (1958) Direct evidence for the transfer of materials from symbiotic algae to the tissues of a coelenterate. Proc Natl Acad Sci USA 44:1259–1263

    Article  CAS  Google Scholar 

  • Muscatine L, Porter JW (1977) Reefs corals: mutualistic symbioses adapted to nutrient poor environments. Bioscience 27:454–460. doi:10.2307/1297526

    Article  Google Scholar 

  • Muscatine L, Falkowski PG, Porter JW, Dubinski Z (1984) Fate of photosynthetic fixed carbon in light-adapted and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc R Soc Lond B 222:181–202. doi:10.1098/rspb.1984.0058

    Article  CAS  Google Scholar 

  • Muscatine L, Falkowski PG, Dubinzky Z, Cook PA, McCloskey LR (1989) The effect of external nutrient resources on the population dynamics of zooxanthellae in a reef coral. Proc R Soc Lond B 236:311–324

    Article  Google Scholar 

  • Oren A (2005) A hundred years of Dunaliella research: 1905–2005. Saline Syst 1:1–14. doi:10.1186/1746-1448-1-2

    Article  Google Scholar 

  • Patton JS, Burris JE (1983) Lipid synthesis and extrusion by freshly isolated zooxanthellae (symbiotic algae). Mar Biol 75:131–136. doi:10.1007/BF00405995

    Article  CAS  Google Scholar 

  • Peng S-E, Chen C-S, Song Y-F, Huang H-T, Jiang P-L et al (2012) Assessment of metabolic modulation in free-living versus endosymbiotic Symbiodinium using synchrotron radiation-based infrared microspectroscopy. Biol Lett 8:434–437. doi:10.1098/rsbl.2011.0893

    Article  Google Scholar 

  • Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper–Excel-based tool using pair-wise correlations. Biotechnol Lett 26:509–515. doi:10.1023/B:BILE.0000019559.84305.47

    Article  CAS  Google Scholar 

  • Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139:1069–1078. doi:10.1007/s002270100674

    Article  Google Scholar 

  • Ritchie RJ, Grant AJ, Eltringham K, Hinde R (1997) Clotrimazole, a model compound for the host release factor of the coral Plesiastrea versipora. Funct Plant Biol 24:283–290. doi:10.1071/PP96106

    CAS  Google Scholar 

  • Robledo D, Hernández-Urcera J, Cal RM, Pardo BG, Sánchez L, Martínez P, Viñas A (2014) Analysis of qPCR reference gene stability determination methods and a practical approach for efficiency calculation on a turbot (Scopthalmus maximus) gonad dataset. BMC Genom 15:648. doi:10.1186/1471-2164-15-648

    Article  Google Scholar 

  • Rodríguez-Román A, Iglesias-Prieto R (2005) Regulation of photochemical activity in cultured symbiotic dinoflagellates under nitrate limitation and deprivation. Mar Biol 146:1063–1073. doi:10.1007/s00227-004-1529-x

    Article  Google Scholar 

  • Rosic NN, Hoegh-Guldberg O (2010) A method for extracting high-quality RNA from Symbiodinium sp. J Appl Phycol 22:139–146. doi:10.1007/s10811-009-9433-x

    Article  CAS  Google Scholar 

  • Rosic NN, Pernice M, Dove S, Dunn S, Hoegh-Guldberg O (2011) Gene expression profiles of cytosolic heat shock proteins Hsp70 and Hsp90 from symbiotic dinoflagellates in response to thermal stress: possible implications for coral bleaching. Cell Stress Chaperones 16:69–80. doi:10.1007/s12192-010-0222-x

    Article  CAS  Google Scholar 

  • Rowan R (1998) Review—diversity and ecology of zooxanthellae on coral reefs. J Phyol 34:407–417. doi:10.1046/j.1529-8817.1998.340407.x

    Article  Google Scholar 

  • Schmitz K, Kremer BP (1977) Carbon fixation and analysis of assimilates in a coral-dinoflagellate symbiosis. Mar Biol 42:305–313. doi:10.1007/BF00402192

    Article  CAS  Google Scholar 

  • Seibt C, Schlichter D (2001) Compatible intracellular ion composition of the host improves carbon assimilation by zooxanthellae in mutualistic symbioses. Naturwissenschaften 88:382–386. doi:10.1007/s001140100240

    Article  CAS  Google Scholar 

  • Silver N, Best S, Jiang J, Thein SL (2006) Selection of housekeeping genes for gene expression studies in human reticulocytes using real-time PCR. BMC Mol Biol 7:33. doi:10.1186/1471-2199-7-33

    Article  Google Scholar 

  • Sols A, Gancedo C, de la Fuente G (1971) Energy-yielding metabolism in yeasts. In: Rose AH (ed) The yeasts. Academic Press, London, pp 271–307

    Google Scholar 

  • Suescún-Bolívar LP, Thomé PE (2015) Osmosensing and osmoregulation in unicellular eukaryotes. World J Microbiol Biotechnol 31:435–443. doi:10.1007/s11274-015-1811-8

    Article  Google Scholar 

  • Suescún-Bolívar LP, Iglesias-Prieto R, Thomé PE (2012) Induction of glycerol synthesis and release in cultured Symbiodinium. PLoS One 7(10):e47182. doi:10.1371/journal.pone.0047182

    Article  Google Scholar 

  • Sutton DC, Hoegh-Guldberg O (1990) Host-zooxanthellae interactions in four temperate marine invertebrate symbioses: assessment of effect of host extracts on symbionts. Biol Bull 178:175–186

    Article  Google Scholar 

  • Swanson R, Hoegh-Guldberg O (1998) Amino acid synthesis in the symbiotic sea anemone Aiptasia pulchella. Mar Biol 131:83–93. doi:10.1007/s002270050299

    Article  CAS  Google Scholar 

  • Takeuchi T, Endo K (2006) Biphasic and dual coordinated expression of the genes encoding major shell matrix proteins in the pearl oyster Pinctada fucata. Mar Biotechnol 8:52–61. doi:10.1007/s10126-005-5037-x

    Article  CAS  Google Scholar 

  • Tanaka Y, Miyajima T, Koike I, Hayashibara T, Ogawa H (2006) Translocation and conservation of organic nitrogen within the coral-zooxanthella symbiotic system of Acropora pulchra, as demonstrated by dual isotope-labeling techniques. J Exp Mar Biol Ecol 336:110–119. doi:10.1016/j.jembe.2006.04.011

    Article  CAS  Google Scholar 

  • Tremblay P, Grover R, Maguer JF, Legendre L, Ferrier-Pagès C (2012) Autotrophic carbon budget in coral tissue: a new 13C-based model of photosynthate translocation. J Exp Biol 215:1384–1393. doi:10.1242/jeb.065201

    Article  CAS  Google Scholar 

  • Trench RK (1971) The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. II. Liberation of fixed 14C by zooxanthellae in vitro. Proc R Soc Lond B 177:237–250. doi:10.1098/rspb.1971.0025

    Article  CAS  Google Scholar 

  • Trench RK (1979) The cell biology of plant-animal symbiosis. Annu Rev Plant Physiol 30:485–531. doi:10.1146/annurev.pp.30.060179.002413

    Article  CAS  Google Scholar 

  • Valdesompele J, De Peter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:research0034.1. doi:10.1186/gb-2002-3-7-research0034

    Google Scholar 

  • Wang JT, Douglas AE (1997) Nutrients, signals, and photosynthate release by symbiotic algae (the impact of taurine on the dinoflagellate alga Symbiodinium from the sea anemone Aiptasia pulchella). Plant Physiol 114:631–636. doi:10.1104/pp.114.2.631

    Article  CAS  Google Scholar 

  • Whitehead LF, Douglas AE (2003) Metabolite comparisons and the identity of nutrients translocated from symbiotic algae to an animal host. J Exp Biol 206:3149–3157. doi:10.1242/jeb.00539

    Article  CAS  Google Scholar 

  • Yancey PH, Heppenstall M, Ly S, Andrell RM, Gates RD et al (2010) Betaines and dimethylsulfoniopropionate as major osmolytes in cnidaria with endosymbiotic dinoflagellates. Physiol Biochem Zool 83:167–173. doi:10.1086/644625

    Article  CAS  Google Scholar 

  • Yellowlees D, Rees TA, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694. doi:10.1111/j.1365-3040.2008.01802

    Article  CAS  Google Scholar 

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Acknowledgments

LPS-B and GMIT acknowledge a graduate fellowship from the Consejo Nacional de Ciencia y Tecnología, México. We thank Dr. Iglesias-Prieto and three anonymous reviewers for improving the manuscript, Luis F. Ortiz-Matamoros for the cloning of the GPD fragment, and Elisa López for retyping the Symbiodinium cultures employed in this work. This work was partially financed by UNAM-DGAPA-PAPIIT Grant Number IN205714 to PET.

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  1. Unidad Académica de Sistemas Arrecifales Puerto Morelos, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Apartado Postal 13, 77500, Cancún, Quintana Roo, Mexico

    Luis P. Suescún-Bolívar, Gerad M. I. Traverse & Patricia E. Thomé

  2. Posgrado en Ciencias del Mar y Limnología, UNAM, UNAM-CDMX, Mexico

    Luis P. Suescún-Bolívar & Gerad M. I. Traverse

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  1. Luis P. Suescún-Bolívar
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Suescún-Bolívar, L.P., Traverse, G.M.I. & Thomé, P.E. Glycerol outflow in Symbiodinium under osmotic and nitrogen stress. Mar Biol 163, 128 (2016). https://doi.org/10.1007/s00227-016-2899-6

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