Biorefinery of the green seaweed Ulva lactuca to produce animal feed, chemicals and biofuels

Journal of Applied Phycology

Volumn 28, Issue 6, 2016, Pages 3511-3525

  Bikker, Paul ^a   van Krimpen, Marinus M ^a   van Wikselaar, Piet ^a   Houweling Tan, Bwee ^a   Scaccia, Nazareno ^a   van Hal, Jaap W ^b   Huijgen, Wouter J J ^b   Cone, John W ^a   López Contreras, Ana M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b TNO   (Netherlands)

Author keywords

ABE fermentation; Animal feed; Biobutanol; Cascading biorefinery; In vitro digestibility; Seaweed; Ulva lactuca

Indexed keywords

EID: 84964297408     PISSN: 09218971     EISSN: 15735176     Source Type: Journal    
DOI: 10.1007/s10811-016-0842-3     Document Type: Article

References (79)

1. Abdel-Fattah AF, Edrees M (1973) Seasonal changes in the constituents of Ulva lactuca. Phytochemistry 12:481–485
2. Abreu MH, Pereira R, Yarish C, Buschmann AH, Sousa-Pinto I (2011) IMTA with Gracilaria vermiculophylla: productivity and nutrient removal performance of the seaweed in a land-based pilot scale system. Aquaculture 312:77–87
3. Abudabos AM, Okab AB, Aljumaah RS, Samara EM, Abdoun KA, Al-Haidary AA (2013) Nutritional value of green seaweed (Ulva lactuca) for broiler chickens. Ital J Anim Sci 12(2), e28
4. Angell AR, Mata L, de Nys R, Paul NA (2016) The protein content of seaweeds: a universal nitrogen-to-protein conversion factor of five. J Appl Phycol 28:511–524
5. Arieli A, Sklan D, Kissil G (1993) A note on the nutritive-value of Ulva lactuca for ruminants. Anim Prod 57:329–331
6. Bennett GN, San KY (2001) Microbial formation, biotechnological production and applications of 1,2-propanediol. Appl Microbiol Biotechnol 55:1–9
7. Bobin-Dubigeon C, Hoebler C, Lognone V, Dagorn-Scaviner C, Mabeau S, Barry JL, Lahaye M (1997) Chemical composition, physico-chemical properties, enzymatic inhibition and fermentative characteristics of dietary fibres from edible seaweeds. Sci Aliments 17:619–639
8. Boisen S, Fernandez JA (1997) Prediction of the total tract digestibility of energy in feedstuffs and pig diets by in vitro analyses. Anim Feed Sci Technol 68:277–286
9. Boland MJ, Rae AN, Vereijken JM, Meuwissen MPM, Fischer ARH, van Boekel M, Rutherfurd SM, Gruppen H, Moughan PJ, Hendriks WH (2013) The future supply of animal-derived protein for human consumption. Trends Food Sci Technol 29:62–73
10. Boubonari T, Malea P, Kevrekidis T (2008) The green seaweed Ulva rigida as a bioindicator of metals (Zn, Cu, Pb and Cd) in a low-salinity coastal environment. Bot Mar 51:472–484
11. Briand X, Morand P (1997) Anaerobic digestion of Ulva sp. 1. Relationship between Ulva composition and methanisation. J Appl Phycol 9:511–524
12. Choct M, Hughes RJ, Wang J, Bedford MR, Morgan AJ, Annison G (1996) Increased small intestinal fermentation is partly responsible for the anti-nutritive activity of non-starch polysaccharides in chickens. Bri Poultry Sci 37:609–621
13. Cole AJ, de Nys R, Paul NA (2014) Removing constraints on the biomass production of freshwater macroalgae by manipulating water exchange to manage nutrient flux. PLoS One 9(7), e101284
14. Cone JW, van Gelder AH (1999) Influence of protein fermentation on gas production profiles. Anim Feed Sci Technol 76:251–264
15. Cone JW, vanGelder AH, Visscher GJW, Oudshoorn L (1996) Influence of rumen fluid and substrate concentration on fermentation kinetics measured with a fully automated time related gas production apparatus. Anim Feed Sci Technol 61:113–128
16. CVB (2007) Veevoedertabel 2007, Centraal Veevoederbureau. Lelystad, The Netherlands
17. Dubois B, Tomkins NW, Kinley RD, Bai M, Seymour S, Paul NA (2013) Effect of tropical algae as additives on rumen in vitro gas production and fermentation characteristics. Am J Plant Sci 4:34–43
18. EC 159/2009 (2009) Commission Regulation of 27 January 2009 laying down the methods of sampling and analysis for the official control of feed
19. Edmonds MS, Parsons CM, Baker DH (1985) Limiting amino acids in low protein corn soybean meal diets fed to growing chicks. Poultry Sci 64:1519–1526
20. European Commission (2002) Directive 2002/32/EC of the European Parliament and of the Council of 7 May 2002 on undesirable substances in animal feed—Council statement. OJ L 140, 30.5.2002, 10–22
21. FAO (2006) World agriculture: towards 2030/2050. Interim Report. Food and Agriculture Organisation, Rome
22. Fleurence J (1999) Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends Food Sc. Technol 10(1):25-28 doi:10.1016/S0924-2244(99)00015-1
23. Fleurence J, LeCoeur C, Mabeau S, Maurice M, Landrein A (1995) Comparison of different extractive procedures for proteins from the edible seaweeds Ulva rigida and Ulva rotundata. J Appl Phycol 7:577–582
24. Flourie B, Vidon N, Florent C, Bernier JJ (1984) Effect of pectin on jejunal glucose-absorption and unstirred layer thickness in normal man. Gut 25:936–941
25. Forsberg CW, Donaldson L, Gibbins LN (1987) Metabolism of rhamnose and other sugars by strains of Clostridium acetobutylicum and other Clostridium species. Can J Microbiol 33:21–26
26. Francavilla M, Franchi M, Monteleone M, Caroppo C (2013) The red seaweed Gracilaria gracilis as a multi products source. Mar Drugs 11:3754–3776
27. Francavilla M, Pineda A, Romero AA, Colmenares JC, Vargas C, Monteleone M, Luque R (2014) Efficient and simple reactive milling preparation of photocatalytically active porous ZnO nanostructures using biomass derived polysaccharides. Green Chem 16:2876–2885
28. Gardiner GE, Campbell AJ, O’Doherty JV, Pierce E, Lynch PB, Leonard FC, Stanton C, Ross RP, Lawlor PG (2008) Effect of Ascophyllum nodosum extract on growth performance, digestibility, carcass characteristics and selected intestinal microflora populations of grower-finisher pigs. Anim Feed Sci Technol 141:259–273
29. Greenwood Y, Orpin CG, Paterson IW (1983) Digestibility of seaweeds in Orkney sheep. Proc Physiol Soc 120
30. Haritonidis S, Malea P (1999) Bioaccumulation of metals by the green alga Ulva rigida from Thermaikos Gulf, Greece. Environ Pollut 104:365–372
31. Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597
32. ISO 13903 (2005) Animal feeding stuffs—determination of amino acids content. International Organization for Standardization, Geneva
33. ISO 13904 (2005) Animal feeding stuffs—determination of tryptophan content. International Organization for Standardization, Geneva
34. ISO 13906 (2008) Animal feeding stuffs—determination of acid detergent fibre (ADF) and acid detergent lignin (ADL) contents. International Organization for Standardization, Geneva
35. ISO 15914 (2004) Animal feeding stuffs—enzymatic determination of total starch content. International Organization for Standardization, Geneva
36. ISO 5983 (2005) Animal feeding stuffs—determination of nitrogen content and calculation of crude protein content—Part 1: Kjeldahl method. International Organization for Standardization, Geneva
37. ISO 5984 (2002) Animal feeding stuffs—determination of crude ash. International Organization for Standardization, Geneva
38. ISO 6496 (1999) Animal feeding stuffs—determination of moisture and other volatile matter content. International Organization for Standardization, Geneva
39. Khotimchenko SV, Vaskovsky VE, Titlyanova TV (2002) Fatty acids of marine algae from the Pacific coast of north California. Bot Mar 45:17–22
40. Kraan S (2013) Mass-cultivation of carbohydrate rich macroalgae, a possible solution for sustainable biofuel production. Mitig Adapt Strateg Glob Chang 18:27–46
41. Lahaye M, Robic A (2007) Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 8:1765–1774
42. Lawton RJ, Mata L, de Nys R, Paul NA (2013) Algal bioremediation of waste waters from land-based aquaculture using Ulva: selecting target species and strains. PloS One 8(10), e77344
43. López-Contreras AM, Claassen PAM, Mooibroek H, De Vos WM (2000) Utilisation of saccharides in extruded domestic organic waste by Clostridium acetobutylicum ATCC 824 for production of acetone, butanol and ethanol. Appl Microbiol Biotechnol 54:162–167
44. Lourenço SO, Barbarino E, De-Paula JC, Pereira LODS, Lanfer Marquez UM (2002) Amino acid composition, protein content and calculation of nitrogen-to-protein conversion factors for 19 tropical seaweeds. Phycol Res 50:233–241
45. MacArtain P, Gill CIR, Brooks M, Campbell R, Rowland IR (2007) Nutritional value of edible seaweeds. Nutr Rev 65:535–543
46. Machado L, Kinley RD, Magnusson M, de Nys R, Tomkins NW (2015) The potential of macroalgae for beef production systems in Northern Australia. J Appl Phycol 27:2001–2005
47. Mai K, Mercer JP, Donlon J (1994) Comparative-studies on the nutrition of 2 species of abalone, Haliotis tuberculata L and Haliotis discus hannai Ino. 2. Amino-acid-composition of abalone and 6 species of macroalgae with an assessment of their nutritional-value. Aquaculture 128:115–130
48. Makkar HPS, Tran G, Heuze V, Giger-Reverdin S, Lessire M, Lebas F, Ankers P (2016) Seaweeds for livestock diets: a review. Anim Feed Sci Technol 212:1–17
49. Marinho G, Nunes C, Sousa-Pinto I, Pereira R, Rema P, Valente LP (2013) The IMTA-cultivated Chlorophyta Ulva spp. as a sustainable ingredient in Nile tilapia (Oreochromis niloticus) diets. J Appl Phycol 25:1359–1367
50. Mariotti F, Tome D, Mirand PP (2008) Converting nitrogen into protein—beyond 6.25 and Jones’ factors. Crit Rev Food Sci Nutr 48:177–184
51. Mercer JP, Mai KS, Donlon J (1993) Comparative studies on the nutrition of two species of abalone, Haliotis tuberculata Linnaeus and Haliotis discus hannai Ino I. Effects of algal diets on growth and biochemical composition. Invertebr Reprod Dev 23(2–3):75–88 doi:10.1080/07924259.1993.9672298
52. Moroney NC, O’Grady MN, O’Doherty JV, Kerry JP (2012) Addition of seaweed (Laminaria digitata) extracts containing laminarin and fucoidan to porcine diets: influence on the quality and shelf-life of fresh pork. Meat Sci 92:423–429
53. NEN-EN 14627 (2010) Foodstuffs—determination of trace elements—determination of total arsenic and selenium by hydride generation atomic absorption spectrometry (HGAAS) after pressure digestion. Stichting Nederlands Normalisatie-Instituut [NL] 1–14
54. NEN-EN 15510 (2007) Animal feeding stuffs—determination of calcium, sodium, phosphorus, magnesium, potassium, iron, zinc, copper, manganese, cobalt, molybdenum, arsenic, lead and cadmium by ICP-AES. Stichting Nederlands Normalisatie-Instituut [NL] 1–29
55. NEN-EN 15763 (2010) Foodstuffs—determination of trace elements—determination of arsenic, cadmium, mercury and lead in foodstuffs by inductively coupled plasma mass spectrometry (ICP-MS) after pressure digestion. Stichting Nederlands Normalisatie-Instituut [NL] 1–18
56. NPR-CEN-ISO/TS 17764–1 and 2 (2006) Animal feeding stuffs—determination of the content of fatty acids—Part 1: preparation of methyl esters and Part 2: gas chromatographic method. International Organization for Standardization, Geneva
57. NRC (2005) Mineral tolerance of animals. National Research Council of the National Academies, second revised edition. The National Academic Press (Eds), Washington DC
58. Ortiz J, Romero N, Robert P, Araya J, Lopez-Hernandez J, Bozzo C, Navarrete E, Osorio A, Rios A (2006) Dietary fiber, amino acid, fatty acid and tocopherol contents of the edible seaweeds Ulva lactuca and Durvillaea antarctica. Food Chem 99:98–104
59. Petit E, LaTouf WG, Coppi MV, Warnick TA, Currie D, Romashko I, Deshpande S, Haas K, Alvelo-Maurosa JG, Wardman C, Schnell DJ, Leschine SB, Blanchard JL (2013) Involvement of a bacterial microcompartment in the metabolism of fucose and rhamnose by Clostridium phytofermentans. PLoS One 8(1), e54337
60. Potts T, Du JJ, Paul M, May P, Beitle R, Hestekin J (2012) The production of butanol from Jamaica bay macro algae. Environ Prog Sustain Energy 31:29–36
61. Ray B, Lahaye M (1995) Cell-wall polysaccharides from the marine green-alga Ulva rigida (Ulvales, Chlorophyta)—chemical structure of ulvan. Carbohydr Res 274:313–318
62. Robertson-Andersson D, Potgieter M, Hansen J, Bolton J, Troell M, Anderson R, Halling C, Probyn T (2008) Integrated seaweed cultivation on an abalone farm in South Africa. J Appl Phycol 20:579–595
63. Robic A, Sassi J-F, Dion P, Lerat Y, Lahaye M (2009) Seasonal variability of physicochemical and rheological properties of ulvan in two Ulva species (Chlorophyta) from the Brittany coast. J Phycol 45:962–973
64. Saxena RK, Anand P, Saran S, Isar J, Agarwal L (2010) Microbial production and applications of 1,2-propanediol. Indian J Microbiol 50:2–11
65. Sorek N, Yeats T, Szemenyei H, Youngs H, Somerville C (2014) The implications of lignocellulosic biomass chemical composition for the production of advanced biofuels. Bio Sci. doi:10.1093/biosci/bit037
66. Sosulski FW, Imafidon GI (1990) Amino acid composition and nitrogen-to-protein conversion factors for animal and plant foods. J Agr Food Chem 38:1351–1356
67. Tabarsa M, Rezaei M, Ramezanpour Z, Waaland JR (2012) Chemical compositions of the marine algae Gracilaria salicornia (Rhodophyta) and Ulva lactuca (Chlorophyta) as a potential food source. J Sci Food Agric 92:2500–2506
68. van de Werken HJG, Verhaart MRA, VanFossen AL, Willquist K, Lewis DL, Nichols JD, Goorissen HP, Mongodin EF, Nelson KE, van Niel EWJ, Stams AJM, Ward DE, de Vos WM, van der Oost J, Kelly RM, Kengen SWM (2008) Hydrogenomics of the extremely thermophilic bacterium Caldicellulosiruptor saccharolyticus. Appl Environ Microbiol 74:6720–6729
69. Van den Burg S, Stuiver M, Veenstra F, Bikker P, López Contreras A, Palstra A, Broeze J, Jansen H, Jak R, Gerritsen A, Harmsen P, Kals J, Blanco A, Brandenburg W, Van Krimpen M, Van Duijn AP, Mulder W, Van Raamsdonk L (2013) A Triple P review of the feasibility of sustainable offshore seaweed production in the North Sea, Wageningen UR LEI Report 13–077, Wageningen, September 2013, pp 1–105
70. Van den Burg S, Van Duijn AP, Bartelings H, Van Krimpen MM, Poelman M (2016) The economic feasibility of seaweed production in the North Sea. Aquac Econ Manag. doi:10.1080/13657305.2016.1177859
71. van den Oever MJA, Bas N, van Soest LJM, Melis C, van Dam JEG (2003) Improved method for fibre content and quality analysis and their application to flax genetic diversity investigations. Ind Crops Prod 18:231–243
72. van der Wal H, Sperber BLHM, Houweling-Tan B, Bakker RRC, Brandenburg W, López-Contreras AM (2013) Production of acetone, butanol, and ethanol from biomass of the green seaweed Ulva lactuca. Bioresour Technol 128:431–437
73. van Hal JW, Huijgen WJJ, Lopez-Contreras AM (2014) Opportunities and challenges for seaweed in the biobased economy. Trends Biotechnol 32:231–233
74. Ventura MR, Castañón JIR (1998) The nutritive value of seaweed (Ulva lactuca) for goats. Small Ruminant Res 29:325–327
75. Ventura MR, Castanon JIR, McNab JM (1994) Nutritional-value of seaweed (Ulva rigida) for poultry. Anim Feed Sci Technol 49:87–92
76. Whittemore CT, Percival JK (1975) Seaweed residue unsuitable as a major source of energy or nitrogen for growing pigs. J Sci Food Agric 26:215–217
77. Wong KH, Cheung PCK (2000) Nutritional evaluation of some subtropical red and green seaweeds Part I: proximate composition, amino acid profiles and some physico-chemical properties. Food Chem 71:475–482
78. Wong KH, Cheung PCK (2001) Nutritional evaluation of some subtropical red and green seaweeds Part II. In vitro protein digestibility and amino acid profiles of protein concentrates. Food Chem 72:11–17
79. Yaich H, Garna H, Besbes S, Paquot M, Blecker C, Attia H (2011) Chemical composition and functional properties of Ulva lactuca seaweed collected in Tunisia. Food Chem 128:895–901