Journal of Applied Phycology

, Volume 31, Issue 1, pp 779–786 | Cite as

The inhibition of anaerobic digestion by model phenolic compounds representative of those from Sargassum muticum

  • John J. MilledgeEmail author
  • Birthe V. Nielsen
  • Patricia J. Harvey


Practical yields of biogas from the anaerobic digestion of macroalgae and, Sargassum muticum in particular, are substantially below the theoretical maximum. There is considerable conjecture about the reasons for the relatively low practical methane yields from seaweed, and polyphenols are suggested as one of the elements in the low yield of methane from brown seaweeds. However, there appears to be little information on the effect of specific phenolics on defined substrates. This paper examines the effect of some simple phenolic compounds, representative of those reported in S. muticum on methane production from a range of model substrates. Three simple phenolics were selected, gallic acid, epicatechin and phloroglucinol; at four addition levels, 0, 0.5, 3.5 and 7.5% w/w of substrate; for four substrates, a readily digested simple organic substance, glycerol, and three polymers found in seaweed, cellulose, alginic acid and the sodium salt of alginic acid. Alginic acid and its sodium salt were found to be recalcitrant with average methane yields of equivalent to only 23–28% of their theoretical methane potential. Methane yield was further reduced by the presence of high concentrations (7% of substrate equivalent to 17.5 mg L−1) of phloroglucinol and epicatechin. None of the phenolic compounds studied appeared to inhibit the breakdown of the simple and readily digested compound, glycerol. Low methane yield in seaweed may be due to the recalcitrance of complex hydrocolloids and phenolic inhibition of the breakdown of more complex molecules in the initial hydrolysis stage of anaerobic digestion, but further research is required.


Anaerobic digestion Polyphenols Gallic acid Phloroglucinol Epicatechin Algae Sargassum muticum Phaeophyta Japanese wireweed 



The authors would like to thank the assistance of colleagues at the University of Greenwich, and Smurfit Kappa Townsend Hook Paper Makers for provision of the inoculum.

Funding information

This work was supported by the EPSRC project number EP/K014900/1 (MacroBioCrude: Developing an Integrated Supply and Processing Pipeline for the Sustained Production of Ensiled Macroalgae-derived Hydrocarbon Fuels) and the University of Greenwich.


  1. Alvarado-Morales M, Boldrin A, Karakashev DB, Holdt SL, Angelidaki I, Astrup T (2013) Life cycle assessment of biofuel production from brown seaweed in Nordic conditions. Bioresour Technol 129:92–99PubMedCrossRefGoogle Scholar
  2. Astals S, Musenze RS, Bai X, Tannock S, Tait S, Pratt S, Jensen PD (2015) Anaerobic co-digestion of pig manure and algae: impact of intracellular algal products recovery on co-digestion performance. Bioresour Technol 181:97–104PubMedCrossRefGoogle Scholar
  3. Balboa E, Moure A, Domínguez H (2015) Valorization of Sargassum muticum biomass according to the biorefinery concept. Mar Drugs 13:3745–3760PubMedPubMedCentralCrossRefGoogle Scholar
  4. Banks C, Zhang Y (2010) Optimising inputs and outputs from anaerobic digestion processes—technical report. DEFRA, SouthamptonGoogle Scholar
  5. Barbot Y, Thomsen C, Thomsen L, Benz R (2015) Anaerobic digestion of Laminaria japonica waste from industrial production residues in laboratory- and pilot-scale. Mar Drugs 13:5947–5975PubMedPubMedCentralCrossRefGoogle Scholar
  6. Barbot Y, Al-Ghaili H, Benz R (2016) A review on the valorization of macroalgal wastes for biomethane production. Mar Drugs 14:120PubMedCentralCrossRefGoogle Scholar
  7. Battista F, Fino D, Ruggeri B (2014) Polyphenols concentration’s effect on the biogas production by wastes derived from olive oil production. Chem Eng Trans 38:373–377Google Scholar
  8. Biomara (2014) A short history of seaweed exploitation in the western British Isles Searched 27 January 2014
  9. Bruton T, Lyons H, Lerat Y, Stanley M, Rasmussen MB (2009) A review of the potential of marine algae as a source of biofuel in Ireland. Sustainable Energy Ireland, DublinGoogle Scholar
  10. Buswell AM, Mueller HF (1952) Mechanism of methane fermentation. Ind Eng Chem 44:550–552CrossRefGoogle Scholar
  11. Cave S (2013) Anaerobic digestion across the UK and Europe. Northern Ireland Assembly, BelfastGoogle Scholar
  12. Centre for Process Innovation (CPI) (2016) The SeaGas project. CPI http://seagascouk/ Searched 7 July 2016
  13. Chen H, Zhou D, Luo G, Zhang S, Chen J (2015) Macroalgae for biofuels production: progress and perspectives. Renew Sust Energy Rev 47:427–437CrossRefGoogle Scholar
  14. Connan S, Delisle F, Deslandes E, Gall EA (2006) Intra-thallus phlorotannin content and antioxidant activity in Phaeophyceae of temperate waters. Bot Mar 49:39–46CrossRefGoogle Scholar
  15. Critchley AT, Farnham WF, Morrell SL (1986) An account of the attempted control of an introduced marine alga, Sargassum muticum, in southern England. Biol Conserv 35:313–332CrossRefGoogle Scholar
  16. Daglia M (2012) Polyphenols as antimicrobial agents. Curr Opin Biotechnol 23:174–181PubMedCrossRefGoogle Scholar
  17. Dijk WV, Schoot JRVD (2015) An economic model for offshore cultivation of macroalgae. EnAlgae project, SwanseaGoogle Scholar
  18. Discover Tiree (2014) Brown gold. http://wwwisleoftireecom/about-tiree/the-land/ Searched 27 January 2014
  19. Farvin KHS, Jacobsen C (2013) Phenolic compounds and antioxidant activities of selected species of seaweeds from Danish coast. Food Chem 138:1670–1681CrossRefGoogle Scholar
  20. Fernando IP, Kim M, Son KT, Jeong Y, Jeon YJ (2016) Antioxidant activity of marine algal polyphenolic compounds: a mechanistic approach. J Med Food 19:615–628PubMedCrossRefGoogle Scholar
  21. Glombitza KW, Forster M, Farnham WF (1982) Antibiotics from algae .25. Polyhydroxyphenyl ethers from the brown alga Sargassum muticum (Yendo) Fensholt Part II. Bot Mar 25:449–453CrossRefGoogle Scholar
  22. Golueke CG, Oswald WJ, Gotaas HB (1957) Anaerobic digestion of algae. Appl Microbiol 5:47–55PubMedPubMedCentralGoogle Scholar
  23. Gonzalez-Lopez N, Moure A, Dominguez H (2012) Hydrothermal fractionation of Sargassum muticum biomass. J Appl Phycol 24:1569–1578CrossRefGoogle Scholar
  24. Gorham J, Lewey SA (1984) Seasonal changes in the chemical composition of Sargassum muticum. Mar Biol 80:103–107CrossRefGoogle Scholar
  25. Heaven S, Milledge JJ, Zhang Y (2011) Comments on ‘anaerobic digestion of microalgae as a necessary step to make microalgal biodiesel sustainable’. Biotechnol Adv 29:164–167PubMedCrossRefGoogle Scholar
  26. Hierholtzer A, Chatellard L, Kierans M, Akunna JC, Collier PJ (2013) The impact and mode of action of phenolic compounds extracted from brown seaweed on mixed anaerobic microbial cultures. J Appl Microbiol 114:964–973PubMedCrossRefGoogle Scholar
  27. Holdt S, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597CrossRefGoogle Scholar
  28. Jard G, Marfaing H, Carrere H, Delgenes JP, Steyer JP, Dumas C (2013) French Brittany macroalgae screening: composition and methane potential for potential alternative sources of energy and products. Bioresour Technol 144:492–498PubMedCrossRefGoogle Scholar
  29. Josefsson M, Jansson K (2011) NOBANIS—invasive alien species fact sheet—Sargassum muticum. http://wwwnobanisorg/files/factsheets/Sargassum_muticumpdf Searched 4 April 2014
  30. Jung KA, Lim SR, Kim Y, Park JM (2013) Potentials of macroalgae as feedstocks for biorefinery. Bioresour Technol 135:182–190PubMedCrossRefGoogle Scholar
  31. Kang N, Lee JH, Lee W, Ko JY, Kim EA, Kim JS, Heu MS, Kim GH, Jeon YJ (2015) Gallic acid isolated from Spirogyra sp. improves cardiovascular disease through a vasorelaxant and antihypertensive effect. Environ Toxicol Pharmacol 39:764–772PubMedCrossRefGoogle Scholar
  32. Kaplan D (1998) Biopolymers from renewable resources. Springer-Verlag, BerlinCrossRefGoogle Scholar
  33. Klejdus B, Plaza M, Šnóblová M, Lojková L (2017) Development of new efficient method for isolation of phenolics from sea algae prior to their rapid resolution liquid chromatographic–tandem mass spectrometric determination. J Pharm Biomed Anal 135:87–96PubMedCrossRefGoogle Scholar
  34. Kraan S (2012) Algal polysaccharides, novel applications and outlook. In: Chang C-F (ed) Carbohydrates—comprehensive studies on glycobiology and glycotechnology. InTech, Rijeka, pp 489–532Google Scholar
  35. Langlois J, Sassi JF, Jard G, Steyer JP, Delgenes JP, Helias A (2012) Life cycle assessment of biomethane from offshore-cultivated seaweed. Biofuels Bioprod Biorefin 6:387–404CrossRefGoogle Scholar
  36. Le Lann K, Surget G, Couteau C, Coiffard L, Cérantola S, Gaillard F, Larnicol M, Zubia M, Guérard F, Poupart N, Stiger-Pouvreau V (2016) Sunscreen, antioxidant, and bactericide capacities of phlorotannins from the brown macroalga Halidrys siliquosa. J Appl Phycol 28:3547–3559CrossRefGoogle Scholar
  37. Lewis J, Salam F, Slack N, Winton M, Hobson L (2011) Product options for the processing of marine macro-algae—summary report. The Crown Estates, RedcarGoogle Scholar
  38. Linville JL, Shen Y, Wu MM, Urgun-Demirtas M (2015) Current state of anaerobic digestion of organic wastes in North America. Curr Sust/Renew Energy Rep 2:136–144CrossRefGoogle Scholar
  39. Liu F, Pang SJ, Gao SQ, Shan TF (2013) Intraspecific genetic analysis, gamete release performance, and growth of Sargassum muticum (Fucales, Phaeophyta) from China. Chin J Ocean Limnol 31:1268–1275CrossRefGoogle Scholar
  40. López A, Rico M, Rivero A, Suárez de Tangil M (2011) The effects of solvents on the phenolic contents and antioxidant activity of Stypocaulon scoparium algae extracts. Food Chem 125:1104–1109CrossRefGoogle Scholar
  41. Lou XF, Nair J, Ho G (2013) Potential for energy generation from anaerobic digestion of food waste in Australia. Waste Manage Res 31:283–294CrossRefGoogle Scholar
  42. Mayfield SP (2015) Consortium for Algal Biofuel Commercialization (CAB-COMM) Final Report. Cal-CAB San DiegoGoogle Scholar
  43. Menetrez M (2012) An overview of algae biofuel production and potential environmental impact. Environ Sci Technol 46:7073–7085PubMedCrossRefGoogle Scholar
  44. Milledge JJ, Harvey PJ (2016a) Ensilage and anaerobic digestion of Sargassum muticum. J Appl Phycol 28:3021–3030CrossRefGoogle Scholar
  45. Milledge JJ, Harvey PJ (2016b) Potential process ‘hurdles’ in the use of macroalgae as feedstock for biofuel production in the British Isles. J Chem Technol Biotechnol 91:2221–2234PubMedPubMedCentralCrossRefGoogle Scholar
  46. Milledge JJ, Heaven S (2014) Methods of energy extraction from microalgal biomass: a review. Rev Environ Sci Biotechnol 13:301–320CrossRefGoogle Scholar
  47. Milledge JJ, Smith B, Dyer P, Harvey P (2014) Macroalgae-derived biofuel: a review of methods of energy extraction from seaweed biomass. Energies 7:7194–7222CrossRefGoogle Scholar
  48. Milledge JJ, Nielsen BV, Bailey D (2015a) High-value products from macroalgae: the potential uses of the invasive brown seaweed, Sargassum muticum. Rev Environ Sci Biotechnol 15:67–88CrossRefGoogle Scholar
  49. Milledge JJ, Staple A, Harvey P (2015b) Slow pyrolysis as a method for the destruction of Japanese Wireweed, Sargassum muticum. Environ Nat Resour Res 5:28–36Google Scholar
  50. Moen E, Horn S, Østgaard K (1997) Biological degradation of Ascophyllum nodosum. J Appl Phycol 9:347–357CrossRefGoogle Scholar
  51. Monlau F, Sambusiti C, Barakat A, Quéméneur M, Trably E, Steyer JP, Carrère H (2014) Do furanic and phenolic compounds of lignocellulosic and algae biomass hydrolyzate inhibit anaerobic mixed cultures? A comprehensive review. Biotechnol Adv 32:934–951PubMedCrossRefGoogle Scholar
  52. Montero L, Sánchez-Camargo AP, García-Cañas V, Tanniou A, Stiger-Pouvreau V, Russo M, Rastrelli L, Cifuentes A, Herrero M, Ibáñez E (2016) Anti-proliferative activity and chemical characterization by comprehensive two-dimensional liquid chromatography coupled to mass spectrometry of phlorotannins from the brown macroalga Sargassum muticum collected on North-Atlantic coasts. J Chromatogr A 1428:115–125PubMedCrossRefGoogle Scholar
  53. Moorthi PV, Balasubramanian C (2015) Antimicrobial properties of marine seaweed, Sargassum muticum against human pathogens. J Coast Life Med 3:122–125Google Scholar
  54. Mousa L, Forster CF (1999) The use of trace organics in anaerobic digestion. Process Saf Environ Prot 77:37–42CrossRefGoogle Scholar
  55. Nallathambi Gunaseelan V (1997) Anaerobic digestion of biomass for methane production: a review. Biomass Bioenergy 13:83–114CrossRefGoogle Scholar
  56. Nguyen H, Heaven S, Banks C (2014) Energy potential from the anaerobic digestion of food waste in municipal solid waste stream of urban areas in Vietnam. Int J Energy Environ Eng 5:365–374CrossRefGoogle Scholar
  57. Oliveira JV, Alves MM, Costa JC (2015) Optimization of biogas production from Sargassum sp. using a design of experiments to assess the co-digestion with glycerol and waste frying oil. Bioresour Technol 175:480–485PubMedCrossRefGoogle Scholar
  58. Østgaard K, Indergaard M, Markussen S, Knutsen SH, Jensen A (1993) Carbohydrate degradation and methane production during fermentation of Laminaria saccharina (Laminariales, Phaeophyceae). J Appl Phycol 5:333–342CrossRefGoogle Scholar
  59. Pérez MJ, Falqué E, Domínguez H (2016) Antimicrobial action of compounds from marine seaweed. Mar Drugs 14:52PubMedCentralCrossRefGoogle Scholar
  60. Rattaya S, Benjakul S, Prodpran T (2015) Extraction, antioxidative, and antimicrobial activities of brown seaweed extracts, Turbinaria ornata and Sargassum polycystum, grown in Thailand. Int Aquat Res 7:1–16CrossRefGoogle Scholar
  61. Rehm BHA (ed) (2009) Alginates: biology and applications. Microbiology Monographs, vol 13. Springer, HeidelbergGoogle Scholar
  62. Rodrigues D, Freitas AC, Pereira L, Rocha-Santos TAP, Vasconcelos MW, Roriz M, Rodríguez-Alcalá LM, Gomes AMP, Duarte AC (2015) Chemical composition of red, brown and green macroalgae from Buarcos Bay in Central West Coast of Portugal. Food Chem 183:197–207PubMedCrossRefGoogle Scholar
  63. Rodríguez-Bernaldo de Quirós A, Lage-Yusty MA, López-Hernández J (2010) Determination of phenolic compounds in macroalgae for human consumption. Food Chem 121:634–638CrossRefGoogle Scholar
  64. Salmeán AA, Duffieux D, Harholt J, Qin F, Michel G, Czjzek M, Willats WGT, Hervé C (2017) Insoluble (1 → 3), (1 → 4)-β-D-glucan is a component of cell walls in brown algae (Phaeophyceae) and is masked by alginates in tissues. Sci Rep 7:2880PubMedPubMedCentralCrossRefGoogle Scholar
  65. Sanchez-Camargo AD, Montero L, Stiger-Pouvreau V, Tanniou A, Cifuentes A, Herrero M, Ibanez E (2016) Considerations on the use of enzyme-assisted extraction in combination with pressurized liquids to recover bioactive compounds from algae. Food Chem 192:67–74CrossRefGoogle Scholar
  66. Savithramma N, Linga Rao M, Venkateswarlu P (2014) Isolation and identification of phenolic compounds from Boswellia ovalifoliolata Bal. & Henry and their free radical scavenger activity. Int J Drug Deliv Technol 4:14–21Google Scholar
  67. Shannon E, Abu-Ghannam N (2016) Antibacterial derivatives of marine algae: an overview of pharmacological mechanisms and applications. Mar Drugs 14:81–104PubMedCentralCrossRefGoogle Scholar
  68. Soto M, Falqué E, Domínguez H (2015a) Relevance of natural phenolics from grape and derivative products in the formulation of cosmetics. Cosmetics 2:259–276CrossRefGoogle Scholar
  69. Soto M, Vazquez MA, de Vega A, Vilarino JM, Fernandez G, de Vicente ME (2015b) Methane potential and anaerobic treatment feasibility of Sargassum muticum. Bioresour Technol 189:53–61PubMedCrossRefGoogle Scholar
  70. Sutherland A, Varela J (2014) Comparison of various microbial inocula for the efficient anaerobic digestion of Laminaria hyperborea. BMC Biotechnol 14:7PubMedPubMedCentralCrossRefGoogle Scholar
  71. Symons GE, Buswell AM (1933) The methane fermentation of carbohydrates. J Am Chem Soc 55:2028–2036CrossRefGoogle Scholar
  72. Tabassum MR, Xia A, Murphy JD (2016) Seasonal variation of chemical composition and biomethane production from the brown seaweed Ascophyllum nodosum. Bioresour Technol 216:219–226PubMedCrossRefGoogle Scholar
  73. Tanniou A, Esteban SL, Vandajon L, Ibnez E, mendiola JA, Cerantola S, Kervarec N, La Barre S, Marchal L, Stiger-Pouvreau V (2013) Green improved processes to extract bioactive phenolic compounds from brown macroalgae using Sargassum muticum as model. Talanta 104:44–52CrossRefGoogle Scholar
  74. Tanniou A, Vandanjon L, Incera M, Serrano Leon E, Husa V, Le Grand J, Nicolas J-L, Poupart N, Kervarec N, Engelen A, Walsh R, Guerard F, Bourgougnon N, Stiger-Pouvreau V (2014) Assessment of the spatial variability of phenolic contents and associated bioactivities in the invasive alga Sargassum muticum sampled along its European range from Norway to Portugal. J Appl Phycol 26:1215–1230Google Scholar
  75. Tedesco S, Stokes J (2017) Valorisation to biogas of macroalgal waste streams: a circular approach to bioproducts and bioenergy in Ireland. Chem Zvesti 71:721–728PubMedGoogle Scholar
  76. Tiwari B, Troy D (eds) (2015) Seaweed sustainability: food and non-food applications, 1st edn. Academic Press, AmsterdamGoogle Scholar
  77. Viana MB, Freitas AV, Leitão RC, Pinto GAS, Santaella ST (2012) Anaerobic digestion of crude glycerol: a review. Environ Technol Rev 1:81–92CrossRefGoogle Scholar
  78. Ward AJ, Lewis DM, Green B (2014) Anaerobic digestion of algae biomass: a review. Algal Res 5:204–214CrossRefGoogle Scholar
  79. Weiland P (2010) Biogas production: current state and perspectives. Appl Microbiol Biotechnol 85:849–860PubMedCrossRefGoogle Scholar
  80. Wikandari R, Sari NK, A'Yun Q, Millati R, Cahyanto MN, Niklasson C, Taherzadeh MJ (2015) Effects of lactone, ketone, and phenolic compounds on methane production and metabolic intermediates during anaerobic digestion. Appl Biochem Biotechnol 175:1651–1663PubMedCrossRefGoogle Scholar
  81. Yoshie Y, Wang W, Petillo D, Suzuki T (2000) Distribution of catechins in Japanese seaweeds. Fish Sci 66:998–1000CrossRefGoogle Scholar
  82. Zhao FJ, Liu FL, Liu JD, Ang PO, Duan DL (2008) Genetic structure analysis of natural Sargassum muticum (Fucales, Phaeophyta) populations using RAPD and ISSR markers. J Appl Phycol 20:191–198CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • John J. Milledge
    • 1
    Email author
  • Birthe V. Nielsen
    • 1
  • Patricia J. Harvey
    • 1
  1. 1.Algae Biotechnology Research Group, Faculty of Engineering and ScienceUniversity of GreenwichKentUK

Personalised recommendations