Abstract
This study evaluated the growth stimulatory effect of low-frequency ultrasound on an ecologically and economically important marine diatom, Skeletonema costatum. To investigate the effect of repeated ultrasonication and the optimum duration of ultrasonication, S. costatum cells were exposed to low-frequency ultrasound (40 kHz) for 0, 2, 30 or 90 s under two sonication conditions: a one-time sonication treatment or a 24-h interval treatment. The cell density and cellular carbohydrate content increased in the ultrasonicated cultures. Similarly, the photosynthetic efficiency, particularly in the exponential growth phase, was enhanced in ultrasonicated cultures, which might account for the enhanced cell growth. At the end of the experiment, compared with the corresponding one-time treatment groups, the cell density in the 30-s sonicated culture and the cellular carbohydrate concentration in the 2-s sonicated culture of the 24-h interval treatment group were increased by 34 ± 4% and 28 ± 3%, respectively. This indicates that, under the same ultrasonic treatment conditions, a higher cellular carbohydrate content can be achieved by repeating the ultrasonication. This study also revealed that, compared with control, the silica/nitrate ratio and silica/phosphate ratio required to produce the same number of S. costatum cells were lower in the sonicated cultures, particularly in the one-time sonicated cultures. This finding indicates that ultrasonic irradiation results in the light silicification of S. costatum cells. This study provides valuable information on the diatom response to low-frequency ultrasonic irradiation and is an important benchmark study for future biotechnological applications of the mass production of S. costatum and other microalgae.
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References
Balzano S, Sarno D, Kooistra WH (2010) Effects of salinity on the growth rate and morphology of ten Skeletonema strains. J Plankton Res 33:937–945
Bar R (1988) Ultrasound enhanced bioprocesses: cholesterol oxidation by Rhodococcus erythropolis. Biotechnol Bioeng 32:655–663
Brányiková I, Maršálková B, Doucha J, Brányik T, Bišová K, Zachleder V, Vítová M (2011) Microalgae—novel highly efficient starch producers. Biotechnol Bioeng 108:766–776
Castillo JA, Meave del Castillo M, Hernández-Becerril D (1995) Morphology and distribution of species of the diatom genus Skeletonema in a tropical coastal lagoon. Eur J Phycol 30:107–115
Chen D (2006) Ultrasonic control of ceramic membrane fouling caused by silica particles and dissolved organic matter. J Membr Sci 276:135–144
Cosgrove J, Borowitzka MA (2011) Chlorophyll fluorescence terminology: an introduction. In: Suggett DJ, Prásil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Dordrecht, pp 1–17
El Ghamrawy A, de Comtes F, Koruk H, Mohammed A, Jones JR, Choi JJ (2019) Acoustic streaming in a soft tissue microenvironment. Ultrasound Med Biol 45:208–217
Francko DA, Taylor SR, Thomas BJ, McIntosh D (1990) Effect of low-dose ultrasonic treatment on phystological variables in Anabaena flos-aquae and Selenastrum capricornutum. Biotechnol Lett 12:219–224
Golub N, Levtun I (2016) Impact of sound irradiation on Chlorella vulgaris cell metabolism. Eastern-Europ J Enterpr Technol 2:27–31
Gügi B, Le Costaouec T, Burel C, Lerouge P, Helbert W, Bardor M (2015) Diatom-specific oligosaccharide and polysaccharide structures help to unravel biosynthetic capabilities in diatoms. Mar Drugs 13:5993–6018
Guillard RR, Sieracki MS (2005) Counting cells in cultures with the light microscope. In: Andersen RA (ed) Algal culturing techniques. Academic Press, Amsterdam, pp 239–252
Guillard RRL, Ryther JH (1962) Studies of marine plankton diatoms: Cyclotella nana Husted, and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229–239
Hao H, Wu M, Chen Y, Tang J, Wu Q (2004) Cyanobacterial bloom control by ultrasonic irradiation at 20 kHz and 1.7 MHz. J Env Sci Health A 39:1435–1446
Harvey EN, Loomis AL (1928) High frequency sound waves of small intensity and their biological effects. Nature 121:622–624
Hassanien RHE, T-z H, Y-f L, B-m L (2014) Advances in effects of sound waves on plants. J Integr Ag 13:335–348
Hu Q (2004) Environmental effects on cell composition. In: Richmond A (ed) Handbook of microalgal culture: biotechnology and applied phycology. Blackwell, London, pp 83–94
Jiang T, Yu Z, Song X, Cao X, Yuan Y (2010) Long-term ecological interactions between nutrient and phytoplankton community in the Changjiang estuary. Chin J Oceanol Limnol 28:887–898
Jomdecha C, Prateepasen A (2011) Effects of pulse ultrasonic irradiation on the lag phase of Saccharomyces cerevisiae growth. Lett Appl Microbiol 52:62–69
Jones GE (1967) Growth of Escherichia coli in heat-and copper-treated synthetic seawater. Limnol Oceanogr 12:167–172
Joyce EM, King PM, Mason TJ (2014) The effect of ultrasound on the growth and viability of microalgae cells. J Appl Phycol 26:1741–1748
Joyce EM, Wu X, Mason TJ (2010) Effect of ultrasonic frequency and power on algae suspensions. J Environmenta Sci Health A 45:863–866
Khan S, Haque M, Arakawa O, Onoue Y (1998) Physiological observations on a diatom Skeletonema costatum (Greville) Cleve. Bangladesh J Fish Res 2:109–118
Kumar CS, Prabu VA (2015) Nutritional value of Skeletonema costatum (Cleve, 1873) from Parangipettai, southeast coast of India. Int J Pharmacuet Sci Res 6:3463–3466
Kurokawa M, King PM, Wu X, Joyce EM, Mason TJ, Yamamoto K (2016) Effect of sonication frequency on the disruption of algae. Ultrason Sonochem 31:157–162
Lestari DP, Ekawati AW, Maftuch M (2014) Dried Skeletonema costatum in feed formulation for the growth of Vaname shrimp (Litopenaeus vannamei). J Exp Life Sci 4:45–49
Li Y, Shi X, Zhang Z, Peng Y (2019) Enhanced coagulation by high-frequency ultrasound in Microcystis aeruginosa-laden water: strategies and mechanisms. Ultrason Sonochem 55:232–242
Liu C, Wang J, Cao Z, Chen W, Bi H (2016) Variation of dissolved organic nitrogen concentration during the ultrasonic pretreatment to Microcystis aeruginosa. Ultrason Sonochem 29:236–243
Ma B, Chen Y, Hao H, Wu M, Wang B, Lv H, Zhang G (2005) Influence of ultrasonic field on microcystins produced by bloom-forming algae. Colloids Surf B 41:197–201
Markou G, Chatzipavlidis I, Georgakakis D (2012) Carbohydrates production and bio-flocculation characteristics in cultures of Arthrospira (Spirulina) platensis: improvements through phosphorus limitation process. BioEnergy Res 5:915–925
Martin CJ, Gemmell HG, Watmough DJ (1978) A study of streaming in plant tissue induced by a Doppler fetal heart detector. Ultrasound Med Biol 4:131–138
Meng Q, Zhou Q, Zheng S, Gao Y (2012) Responses on photosynthesis and variable chlorophyll fluorescence of Fragaria ananassa under sound wave. Energy Procedia 16:346–352
Miller DL (1979) Cell death thresholds in Elodea for 0.45–10 MHz ultrasound compared to gas-body resonance theory. Ultrasound Med Biol 5:351–357
Miller DL (1986) Effects of a high-amplitude 1-MHz standing ultrasonic field on the algae Hydrodictyon. IEEE Trans Ultrason Ferroelect Freq Contr 33:165–170
Millie DF (1984) The effects of silica, nitrogen, and phosphorus limitation on the biochemical composition of Cyclotella meneghiniana Kütz: an experimental analysis. PhD Thesis, Iowa State University
Mooij PR, de Jongh LD, van Loosdrecht MCM, Kleerebezem R (2016) Influence of silicate on enrichment of highly productive microalgae from a mixed culture. J Appl Phycol 28:1453–1457
Myklestad S, Haug A, Larsen B (1972) Production of carbohydrates by the marine diatom Chaetoceros affinis var. willei (Gran) Hustedt. II. Preliminary investigation of the extracellular polysaccharide. J Exp Mar Biol Ecol 9:137–144
Nelson DM, Treguer P, Brzenzinski MA, Leynaert A, Queguiner B (1995) Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Glob Biogeochem Cycle 9:359–372
Nyborg W (1982) Ultrasonic microstreaming and related phenomena. Brit J Cancer Suppl 5:156
Paleg LG, Aspinall D (1981) The physiology and biochemistry of drought resistance in plants. Academic Press, Sydney
Park S, Park J-S, Lee H, Heo J, Yoon Y, Choi K, Her N (2011) Ultrasonic degradation of endocrine disrupting compounds in seawater and brackish water. Env Eng Res 16:137–148
Penna A, Berluti S, Penna N, Magnani M (1999) Influence of nutrient ratios on the in vitro extracellular polysaccharide production by marine diatoms from the Adriatic Sea. J Plankton Res 21:1681–1690
Pérez L, Salgueiro JL, González J, Parralejo AI, Maceiras R, Cancela Á (2017) Scaled up from indoor to outdoor cultures of Chaetoceros gracilis and Skeletonema costatum microalgae for biomass and oil production. Biochem Eng J 127:180–187
Reis Batista I, Garcia AB, Van Dalen P, Kamermans P, Verdegem M, Smaal AC (2015) Culturing Chaetoceros muelleri using simplified media with different N sources: effects on production and lipid content. Eur J Phycol 50:92–99
Rekha V, Gurusamy R, Santhanam P, Devi AS, Ananth S (2012) Culture and biofuel production efficiency of marine microalgae Chlorella marina and Skeletonema costatum. Indian J Geo-Mar Sci 41:152–158
Rokhina EV, Lens P, Virkutyte J (2009) Low-frequency ultrasound in biotechnology: state of the art. Trends Biotechnol 27:298–306
Sivaramakrishnan R, Incharoensakdi A (2019) Low power ultrasound treatment for the enhanced production of microalgae biomass and lipid content. Biocatal Ag Biotechnol 20:101230
Sivaramakrishnan R, Muthukumar K (2012) Production of methyl ester from Oedogonium sp. oil using immobilized isolated novel Bacillus sp. lipase. Energy Fuel 26:6387–6392
Tang JW, Wu QY, Hao HW, Chen Y, Wu M (2004) Effect of 1.7 MHz ultrasound on a gas-vacuolate cyanobacterium and a gas-vacuole negative cyanobacterium. Colloids Surfaces B 36:115–121
Taraldsvik M, Myklestad S (2000) The effect of pH on growth rate, biochemical composition and extracellular carbohydrate production of the marine diatom Skeletonema costatum. Eur J Phycol 35:189–194
Uddin SA, Zafar M (2007) Mass culture of marine diatom Skeletonema costatum (Greville) Cleve collected from the Bay of Bengal. Pakistan J Mar Sci 16:33–38
Wang C, Lin X, Li L, Lin S (2016) Differential growth responses of marine phytoplankton to herbicide glyphosate. PLoS One 11:e0151633
Warr SRC, Reed RH, Stewart WDP (1985) Carbohydrate accumulation in osmotically stressed cyanobacteria (blue-green algae): interactions of temperature and salinity. New Phytol 100:285–292
Yao J, Chen X, Zhang M, Zhang Y, Zhang Z, Xian X, Bao B, Bai J (2019) Inhibition of the photosynthetic activity of Synedra sp. by sonication: performance and mechanism. J Env Manage 233:54–62
Zhang G, Zhang P, Wang B, Liu H (2006) Ultrasonic frequency effects on the removal of Microcystis aeruginosa. Ultrason Sonochemi 13:446–450
Zhang S-F, Yuan C-J, Chen Y, Chen X-H, Li D-X, Liu J-L, Lin L, Wang D-Z (2016) Comparative transcriptomic analysis reveals novel insights into the adaptive response of Skeletonema costatum to changing ambient phosphorus. Front Microbiol 7:1476–1476
Acknowledgements
We would like to thank the following funding agencies for supporting this research: the National Key Research and Development Program of China (No. 2016YFA0601302), the China Postdoctoral Science Foundation (No. 2018M632580) and the National Natural Science Foundation of China (Nos. 41876146, 41476116).
Funding
This work was funded by the National Key Research and Development Program of China (No. 2016YFA0601302), the China Postdoctoral Science Foundation (No. 2018M632580) and the National Natural Science Foundation of China (Nos. 41876146, 41476116).
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Y.G., R.A. and B.H. conceived the project; V.P, L.S. and X.L. prepared samples and maintained the laboratory facilities; R.A. and S.S performed the experiment and data analysis; C.C. and J.L. contributed to the experimental design; and R.A., B.H. and Y.G. wrote and edited the manuscript.
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The effect of low-frequency ultrasonic irradiation on the extracellular carbohydrate concentration of S. costatum cell cultures sonicated for 0 (control), 2, 30 and 90 s in the one-time (a) and 24-h interval treatments (b). The data points represent triplicate analyses (±SE, n = 3) (DOCX 132 kb)
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Abate, R., Song, S., Patil, V. et al. Enhancing the production of a marine diatom (Skeletonema costatum) with low-frequency ultrasonic irradiation. J Appl Phycol 32, 3711–3722 (2020). https://doi.org/10.1007/s10811-020-02270-6
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DOI: https://doi.org/10.1007/s10811-020-02270-6