Abstract
Three red seaweeds from the Venice Lagoon: Gracilaria gracilis, Gracilaria vermiculophylla, Gracilariopsis longissima and the green seaweed Ulva rigida were investigated to determine the yields and the annual fluctuation of sulfated polysaccharides (SP) for biotechnological applications. The Gracilariaceae and U. rigida were investigated and evaluated taking into account various environmental parameters of the water column and surface sediments. The annual production of SP was the highest for G. longissima (13.2 tons dw ha−1 year−1), followed by G. vermiculophylla (11.4 tons dw ha−1 year−1) and G. gracilis (7.4 tons dw ha−1 year−1), whereas U. rigida showed the lowest production (2.7 tons dw ha−1 year−1). High nutrient availability, turbidity and phytoplankton blooms inhibited the production of SP in the red seaweeds especially in summer. The SP produced by Gracilariaceae in March and April, at water temperatures ranging between 13°C and 17°C, accounted for more than half of the total annual production. In contrast, U. rigida produced the highest quantity of SP (ulvan) in June with temperatures >25°C.
Article note:
This article belongs to the special issue Phycomorph: macroalgal development and morphogenesis, published in Botanica Marina 2017, vol. 60, issue 2.
About the authors

Andrea Augusto Sfriso, graduated from Ca’ Foscari University of Venice in 2013. He is a PhD student at Ca’ Foscari University of Venice researching biotechnological applications for seaweeds, seaweed ecology and biochemistry. Currently, he is researching algal polysaccharides, fluorophores and wild bacterial strains for biomass conversion to high value compounds. He is laying the groundwork for a scientific expertise in the sustainable use of algal biomasses in transition environments.

Michele Gallo graduated as a chemical-biological laboratory technician in 1989. Since then, he has worked at the Department of Molecular Sciences and Nanosystems, Ca’ Foscari University of Venice as a Technical Laboratory Assistant with expertise in microbiology: characterization of bacteria isolated from extreme environments and archeological sites; study of bacterial metal-resistance and exopolymeric-metal complexes production and characterization; study of bacterial biodegradation of hydrocarbons and paper manuscripts; extraction of polysaccharides from bacterial cultures and production of “green” nanoparticles for catalytic activities, antimicrobial and nutraceutical applications.

Franco Baldi, graduated from Siena University in 1975. In 1998, he joined Ca’ Foscari University as an Associated Professor and has been a full Professor in General Microbiology (BIO-19) at the same university since 2005. He has scientific expertise in Environmental Microbiology with a special interest in microbial interactions with metals in terrestrial and marine ecosystems with relative applications. He has published almost 100 publications, the majority of them in international journals (see also: http://www.unive.it/data/persone/5591470/pubb_anno). Prof. Baldi worked in several laboratories mostly in Europe and the USA.
Acknowledgments
The authors are grateful to Dr. Orietta Zucchetta and the journal editor for the English editing and to Prof. Adriano Sfriso for his taxonomical expertise and support.
References
Armisén, R., F. Galatas and S.A. Hispanagar. 2000. Agar. In: (G.O. and P.A. Williams, eds.) Handbook of hydrocolloids. Woodhead Publishing, Madrid. pp. 21–40.Search in Google Scholar
Arvizu-Higuera D.L., Y.E. Rodríguez-Montesinos, J.I. Murillo-Álvarez, M. Muñoz-Ochoa and G. Hernández-Carmona. 2008. Effect of alkali treatment time and extraction time on agar from Gracilaria vermiculophylla. J. Appl. Phycol. 20: 515–519.10.1007/978-1-4020-9619-8_9Search in Google Scholar
Briand, X. and P. Morand. 1997. Anaerobic digestion of Ulva sp. 1. Relationship between Ulva composition and methanisation. J. Appl. Phycol. 9: 511.Search in Google Scholar
Bunson, C. and A. Prathep. 2012. Effects of salinity, light intensity and sediment on growth, pigments, agar production and reproduction in Gracilaria tenuistipitata from Songkhla Lagoon in Thailand. Phycol. Res. 60: 169–178.10.1111/j.1440-1835.2012.00648.xSearch in Google Scholar
Buriyo, A.S. and A.K. Kivaisi. 2003. Standing stock, agar yield and properties of Gracilaria salicornia harvested along the Tanzanian coast. Western Indian Ocean J. Mar. Sci. 2: 171–178.10.4314/wiojms.v2i2.28433Search in Google Scholar
Chakraborty, S. and S.C. Santra. 2008. Biochemical composition of eight benthic algae collected from Sunderban. Indian J. Mar. Sci. 37: 329–332.Search in Google Scholar
Chiellini, F. and A. Morelli. 2011. Ulvan: a versatile platform of biomaterials from renewable resources. In: (R. Pignatello, ed.) Biomaterials – physics and chemistry. InTech. pp. 75–98.10.5772/24901Search in Google Scholar
Co, C., I.W. Araujo, E.S. Vanderlei, J.A. Rodrigues, A.L. Quindere, B.P. Fontes, I.N. Queiroz, D.B. Menezes, M.M. Bezera, A.A. Silva, H.V. Chaves, R.J. Jorge, J.S. Evangelista and N.M. Benevides. 2012. Antinociceptive and anti-inflammatory activities of sulphated polysaccharides from the red seaweed Gracilaria cornea. Basic Clin. Pharmacol. Toxicol. 110: 335–341.10.1111/j.1742-7843.2011.00811.xSearch in Google Scholar
DuBois, M., K.A. Gilles, J.K. Hamilton, P.A. Rebers and F. Smith. 1956. Colorimetric Method for Determination of Sugars and Related Substances. Anal. Chem. 28: 350–356.10.1021/ac60111a017Search in Google Scholar
Edding, M., J. Macchiavello and H. Black. 1987. Culture of Gracilaria sp. in outdoor tanks: productivity. Hydrobiologia 151/152: 369–373.10.1007/978-94-009-4057-4_55Search in Google Scholar
Engledow, H.R. and J.J. Bolton. 1992. Environmental tolerances in culture and agar content of Gracilaria verrucosa (Hudson) Paperfuss (Rhodophyta, Gigartinales) from Saldanha Bay. S Afr. J. Bot. J. 58: 263–267.10.1016/S0254-6299(16)30845-6Search in Google Scholar
Fan, Y., W. Wang, W. Song, H. Chen, H. Teng, A. Teng and A. Liu. 2012. Partial characterization and anti-tumor activity of an acidic polysaccharide from Gracilaria lemaneiformis. Carbohydr. Polym. 88: 1313–1318.10.1016/j.carbpol.2012.02.014Search in Google Scholar
Francavilla, M., P. Manara, P. Kamaterou, M. Monteleone and A. Zabaniotou. 2015. Cascade approach of red macroalgae Gracilaria gracilis sustainable valorization by extraction of phycobiliproteins and pyrolysis of residue. Bioresour. Technol. 184: 305–313.10.1016/j.biortech.2014.10.147Search in Google Scholar PubMed
Freile-Pelegrin, Y. and D. Robledo. 1997. Influence of alkali treatment on agar from Gracilaria cornea from Yucatan, México. J. Appl. Phycol. 9: 533–539.Search in Google Scholar
Gonzalez-Leija, J.A., E. Hernandez-Garibay, I. Pacheco-Ruiz, J. Guardado-Puentes, J. Espinoza-Avalos, J.M. Lopez-Vivas and J. Bautista-Alcantar. 2009. Optimization of the yield and quality of agar from Gracilariopsis lemaneiformis (Gracilariales) from the Gulf of California using an alkaline treatment. J. Appl. Phycol. 21: 321–326.10.1007/s10811-008-9370-0Search in Google Scholar
Jayasankar, R. and G. Kulandaivelu. 1999. Seasonal variation in the biochemical constituents of Gracilaria spp. with reference to growth. Indian J. Mar. Sci. 28: 464–466.Search in Google Scholar
Kumar, S., R. Gupta, G. Kumar, D. Sahoo and R.C. Kuhad. 2013. Bioethanol production from Gracilaria verrucosa, a red alga, in a biorefinery approach. Bioresour. Technol. 135: 150–156.10.1016/j.biortech.2012.10.120Search in Google Scholar
Lahaye, M. and A. Robic. 2007. Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 8: 1765–1774.10.1021/bm061185qSearch in Google Scholar
Lahaye, M. and C. Rochas. 1991. Chemical structure and physico-chemical properties of agar. Hydrobiologia 221: 137–148.10.1007/978-94-011-3610-5_13Search in Google Scholar
Marinho-Soriano, E. 2001. Agar polysaccharides from Gracilaria species (Rhodophyta, Gracilariaceae). J. Biotechnol. 89: 81–84.10.1016/S0168-1656(01)00255-3Search in Google Scholar
Marinho-Soriano, E. and E. Bourret. 2003. Effects of season on the yield and quality of agar from Gracilaria species (Gracilariaceae, Rhodophyta). Bioresour. Technol. 90: 329–333.10.1016/S0960-8524(03)00112-3Search in Google Scholar
Mclachlan, J. and C.J. Bird. 1986. Gracilaria (Gigartinales, Rohodophyta) and productivity. Aquat. Bot. 26: 27–49.10.1016/0304-3770(86)90004-5Search in Google Scholar
Meena, R., K. Prasad, M. Ganesan and A.K. Siddhanta. 2008. Superior quality agar from Gracilaria species (Gracilariales, Rhodophyta) collected from the Gulf of Mannar. India. J. Appl. Phycol. 20: 397–402.10.1007/s10811-007-9272-6Search in Google Scholar
Mollet, J.C., A. Rahaoui and Y. Lemoine. 1998. Yield, chemical composition and gel strenght of agarocolloids of Gracilaria gracilis, Gracilariopsis longissima and the newely reported Gracilaria cf. vermiculophylla from Roscoff (Brittany, France). J. Appl. Phycol. 10: 59–66.10.1023/A:1008051528443Search in Google Scholar
Nishinari K. and M. Watase. 1983. Effect of Alkali Pretreatment on the Rheological Properties of Concentrated Agar-Agar Gels. Carbohydr. Polym. 3: 39–52.10.1016/0144-8617(83)90011-5Search in Google Scholar
Praiboon, J., A. Chirapart, Y. Akakabe, O. Bhumibhamon, and T. Kajiwara. 2006. Physical and chemical characterization of agar polysaccharides extracted from the Thai and Japanese species of Gracilaria. Sci. Asia 32: 11–17.10.2306/scienceasia1513-1874.2006.32(s1).011Search in Google Scholar
Qi, H., T. Zhao, Q. Zhang, Z. Li, Z. Zhao and R. Xing. 2005a. Antioxidant activity of different molecular weight sulfated polysaccharides from Ulva pertusa Kjellm (Chlorophyta). J. Appl. Phycol. 17: 527–534.10.1007/s10811-005-9003-9Search in Google Scholar
Qi, H., Q. Zhang, T. Zhao, R. Chen, H. Zhang, X. Niu and Z. Li. 2005b. Antioxidant activity of different sulfate content derivatives of polysaccharides extracted from Ulva pertusa (Chlorophyta) in vitro. Int. J. Biol. Macromol. 37: 195–199.10.1016/j.ijbiomac.2005.10.008Search in Google Scholar
Ray, B. and M. Lahaye. 1995. Cell-wall polysaccharides from the marine green alga Ulva “rigida” (Ulvales, Chlorophyta). Extraction and chemical composition. Carbohydr. Res.274: 251–261.10.1016/0008-6215(95)00138-JSearch in Google Scholar
Rebello, J., M. Ohno, H. Ukeda and M. Sawamura. 1997. Agar quality of commercial agarophytes from different geographical origins: 1. Physical and rheological properties. J. Appl. Phycol. 8: 517–521.10.1007/BF02186330Search in Google Scholar
Robic, A., C. Gaiilard, J.F. Sassi, Y. Lerat and M. Lahaye. 2009. Ultrastructure of Ulvan: a polysaccharide from green seaweeds. Biopolymers 98: 652–664.10.1002/bip.21195Search in Google Scholar
Roleda, M.Y., N.E. Montano, E.T. Ganzon-Fortes and R.D. Villanueva. 1997. Acetic acid pretreatment in Agar extraction of Philippine Gelidiella acerosa (Forsskaal) Feldmann et Hamel (Rodophyta, Gelidiales). Bot. Mar. 40: 63–69.Search in Google Scholar
Sfriso, A.A. and A. Sfriso. 2017. In situ biomass production of Gracilariaceae and Ulva rigida: the Venice Lagoon as a study case. Bot. Mar 60: 271–283.10.1515/bot-2016-0061Search in Google Scholar
Sfriso, A., A. Marcomini and B. Pavoni. 1987. Relationship between macroalgal biomass and nutrient concentrations in a hypertrophic area of the Venice Lagoon. Mar. Environ. Res.22: 297–312.10.1016/0141-1136(87)90005-5Search in Google Scholar
Sfriso, A., A. Marcomini and B. Pavoni. 1994. Gracilaria distribution, production and composition in the Lagoon of Venice. Bioresour. Technol. 50: 165–173.10.1016/0960-8524(94)90069-8Search in Google Scholar
Sfriso, A., C. Facca, A. Bonometto and R. Boscolo. 2014a. Compliance of the Macrophyte Quality index (MaQI) with the WFD (2000/60/EC) and ecological status assessment in transitional areas: the Venice lagoon as study case. Ecol. Indic.46: 536–547.10.1016/j.ecolind.2014.07.012Search in Google Scholar
Sfriso, A., C. Facca, D. Bon, F. Giovannone and A. Buosi. 2014b. Using phytoplankton and macrophytes to assess the trophic and ecological status of some Italian transitional systems. Cont. Shelf. Res.81: 88–98.10.1016/j.csr.2014.03.013Search in Google Scholar
Shefer, S., A. Israel, A. Golberg and A. Chudnovsky. 2017. Carbohydrate-based phenotyping of the green macroalga Ulva fasciata using near-infrared spectrometry: potential implications for marine biorefinery. Bot. Mar. 60: 219–228.10.1515/bot-2016-0039Search in Google Scholar
Soedjak, H.S. 1994. Colorimetric determination of carragenans and other anionic hydrocolloids with methylene blue. Anal. Chem. 66: 4514–4518.10.1021/ac00096a018Search in Google Scholar
Sousa, A.M.M., V.D. Alves, S. Morais, C. Delerue-Matos and M.P. Goncalves. 2010. Agar extraction from integrated multitrophic aquacultured Gracilaria vermiculophylla: evaluation of a microwave-assisted process using response surface methodology. Bioresour. Technol. 101: 3258–3267.10.1016/j.biortech.2009.12.061Search in Google Scholar PubMed
Sousa, A.M.M., S. Morais, M.H. Abreu, R. Pereira, I.S. Pinto, E.J. Cabrita, C.D. Matos and M.P. Goncalves. 2012. Structural, physical and chemical modifications induced by microwave heating on native agar-like galactans. J. Agric. Food Chem.60: 4977–4985.10.1021/jf2053542Search in Google Scholar PubMed
TerBraak, C.J.F. and P. Šmilauer. 2012. Canoco reference manual and user’s guide: software for ordination, version 5.0. Microcomputer Power, Ithaca, USA. pp. 496.Search in Google Scholar
Thomsen, M.S. and K.J. McGlathery. 2006. Stress tolerance of the invasive macroalgae Codium fragile and Gracilaria vermiculophylla in a soft-bottom turbid lagoon. Biol. Invasions 9: 499–513.10.1007/s10530-006-9043-3Search in Google Scholar
Vergara-Rodarte, M.A., G. Hernandez-Carmona, Y.E. Rodriguez-Montesinos, D.L. Arvizu-Higuera, R. Riosmena-Rodriguez and J.I. Murillo-Alvarez. 2010. Seasonal variation of agar from Gracilaria vermiculophylla, effect of alkali treatment time, and stability of its Colagar. J. Appl. Phycol. 22: 753–759.10.1007/s10811-010-9516-8Search in Google Scholar
Vilar, V.J.P., C.M.S. Botelho and R.A.R. Boaventura. 2008. Copper removal by algae Gelidium, agar extraction algal waste and granulated algal waste: kinetics and equilibrium. Bioresour. Technol. 99: 750–762.10.1016/j.biortech.2007.01.042Search in Google Scholar PubMed
Villanueva R.D., A.M.M. Sousa, M.P. Gonçalves, M. Nilsson and L. Hilliou. 2010. Production and properties of agar from the invasive marine alga, Gracilaria vermiculophylla (Gracilariales, Rhodophyta). J. Appl. Phycol. 22: 211–220.10.1007/s10811-009-9444-7Search in Google Scholar
Wakibia, J.G., R.J. Anderson and D.W. Keats. 2001. Growth rates and agar properties of three gracilarioids in suspended open-water cultivation in St. Helena Bay, South Africa. J. Appl. Phycol. 13: 195–207.10.1023/A:1011148411897Search in Google Scholar
Wang, X., X. Liu and G. Wang. 2011. Two-stage Hydrolysis of invasive algal feedstock for ethanol fermentation. J. Integr. Plant Biol. 53: 246–252.10.1111/j.1744-7909.2010.01024.xSearch in Google Scholar PubMed
Wei, N., J. Quarterman and Y.S. Jin. 2013. Marine macroalgae: an untapped resource for producing fuels and chemicals. Trends Biotechnol. 31: 70–77.10.1016/j.tibtech.2012.10.009Search in Google Scholar PubMed
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