A mini-review on the microbial continuum: consideration of a link between judicious consumption of a varied diet of macroalgae and human health and nutrition

  • M. Lynn CornishEmail author
  • Ole G. Mouritsen
  • Alan T. Critchley


As the primordial, prokaryotic inhabitants on Earth, microbial entities were responsible for significant influences on the pathways taken in the development of life as we know it. The manifestation of numerous pathologies in humans is considered to be intrinsically associated with microbial dysbiosis in the gut (i.e. a poorly balanced microbiota). Such adverse health conditions include obesity, chronic fatigue syndrome, cancer, cardiovascular issues, neurological disorders, colitis, irritable bowel syndrome (IBS), and rheumatoid arthritis. Endosymbiotic events at the single cell level took place billions of years ago, eventually leading to eukaryotes, photosynthesis, and multicellularity. Macroalgae (seaweeds) were amongst the first organisms to develop these characteristics. Microbes and macroalgae interacted in a pattern of co-evolution, a process that applies to most, if not all living organisms. It is recognized that the normal human microbiome consists of over a trillion microorganisms, including about 2 000 commensal bacterial species typically stationed in the gut. Many of these live in the colon, where they function in the digestion of foods, releasing bio-available nutrients, bioactive molecules, and various metabolites. They mediate communication signals between the gut and the brain, and promote the normal development of immune function, metabolic activities, behaviour, and neurological stability. As very early humans foraged for food, some would have benefitted from coastal diets, rich in seaweeds and associated microbes. Such diets would have consistently provided all the nutrients essential for survival and growth, and as such, could have conveyed competitive advantages and contributed to enhanced cognitive sophistication. This mini-review article highlights studies regarding the health benefits of dietary fibres and the production of short chain fatty acids (SCFA). Insights are offered regarding the positive effects the inclusion of macroalgae into the standard, Western diet can deliver in terms of providing appropriate fodder for those microbial populations deemed beneficial to human health and wellness.


microbiota macroalgae fibre short chain fatty acids (SCFA) nutrition 


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The work by OGM was supported by Nordeafonden via a center grant to the national Danish center Taste for Life.

The authors would like to thank anonymous reviewers of the journal for their careful scrutiny and constructive comments which improved the manuscript.


  1. Alam M Z, Braun G, Norrie J, Hodges D M. 2013. Effect of Ascophyllum extract application on plant growth, fruit yield and soil microbial communities of strawberry. Can. J. Plant Sci., 93 (1): 23–36.CrossRefGoogle Scholar
  2. Alam M Z, Braun G, Norrie J, Hodges D M. 2014. Ascophyllum extract application can promote plant growth and root yield in carrot associated with increased root-zone soil microbial activity. Can. J. Plant Sci., 94 (2): 337–348.CrossRefGoogle Scholar
  3. Armstrong E, Yan L M, Boyd K G, Wright P C, Burgess J G. 2001. The symbiotic role of marine microbes on living surfaces. Hydrobiologia, 461 (1-3): 37–40.CrossRefGoogle Scholar
  4. Augustin R, Schröder K, Rincón A P M, Fraune S, Anton- Erxleben F, Herbst E M, Wittlieb J, Schwentner M, Grötzinger J, Wassenaar T M, Bosch T C G. 2017. A secreted antibacterial neuropeptide shapes the microbiome of Hydra. Nat. Commun., 8 (1): 698, CrossRefGoogle Scholar
  5. Bajury D M, Rawi M H, Sazali I H, Abdullah A, Sarbini S R. 2017. Prebiotic evaluation of red seaweed (Kappaphycus alvarezii) using in vitro colon model. Int. J. Food Sci. Nutr., 68 (7): 821–828, CrossRefGoogle Scholar
  6. Benedict C, Vogel H, Jonas W, Woting A, Blaut M, Schürmann A, Cedernaes J. 2016. Gut microbiota and glucometabolic alterations in response to recurrent partial sleep deprivation in normal-weight young individuals. Mol. Metab., 5 (12): 1 175-1 186.CrossRefGoogle Scholar
  7. Blaser M J, Cardon Z G, Cho M K, Dangl J L, Donohue T J, Green J L, Knight R, Maxon M E, Northen T R, Pollard K S, Brodie E L. 2016. Toward a predictive understanding of Earth’s microbiomes to address 21st century challenges. mBio, 7 (3): e00714–16, CrossRefGoogle Scholar
  8. Blaser M J, Falkow S. 2009. What are the consequences of the disappearing human microbiota? Nat. Rev. Microbiol., 7 (12): 887–894.Google Scholar
  9. Blaser M J. 2018. The past and future biology of the human microbiome in an age of extinctions. Cell, 172 (6): 1 173–1 177.CrossRefGoogle Scholar
  10. Blottière H M, Buecher B, Galmiche J P, Cherbut C. 2003. Molecular analysis of the effect of short-chain fatty acids on intestinal cell proliferation. Proc. Nutr. Soc., 62 (1): 101–106.CrossRefGoogle Scholar
  11. Bourassa M W, Alim I, Bultman S J, Ratan R R. 2016. Butyrate, neuroepigenetics and the gut microbiome: can a high fiber diet improve brain health? Neurosci. Let., 625: 56–63.Google Scholar
  12. Cani P D, Everard A. 2016. Talking microbes: when gut bacteria interact with diet and host organs. Mol. Nutr. Food Res., 60 (1): 58–66.CrossRefGoogle Scholar
  13. Cantarel B L, Lombard V, Henrissat B. 2012. Complex carbohydrate utilization by the healthy human microbiome. PLoS One, 7 (6): e28742.CrossRefGoogle Scholar
  14. Chen L G, Xu W, Chen D, Chen G J, Liu J W, Zeng X X, Shao R, Zhu H J. 2018. Digestibility of sulfated polysaccharide from the brown seaweed Ascophyllum nodosum and its effect on the human gut microbiota in vitro. Int. J. Biol. Macromol., 112: 1 055–1 061.CrossRefGoogle Scholar
  15. Chow J, Lee S M, Shen Y, Khosravi A, Mazmanian S K. 2010. Host-bacterial symbiosis in health and disease. Adv. Immunol., 107: 243–274.CrossRefGoogle Scholar
  16. Cian R E, Drago S R, de Medina F S, Martínez-Augustin O. 2015. Proteins and carbohydrates from red seaweeds: evidence for beneficial effects on gut function and microbiota. Mar. Drugs, 13 (8): 5 358–5 383.CrossRefGoogle Scholar
  17. Clemente J C, Ursell L K, Parfrey L W, Knight R. 2012. The impact of the gut microbiota on human health: an integrative view. Cell, 148 (6): 1 258–1 270.CrossRefGoogle Scholar
  18. Cock J M, Sterck L, Rouzé P, Scornet D, Allen A E, Amoutzias G, Anthouard V, Artiguenave F, Aury J M, Badger J H, Beszteri B, Billiau K, Bonnet E, Bothwell J H, Bowler C, Boyen C, Brownlee C, Carrano C J, Charrier B, Cho G Y, Coelho S M, Collén J, Corre E, Da Silva C, Delage L, Delaroque N, Dittami S M, Doulbeau S, Elias M, Farnham G, Gachon C M, Gschloessl B, Heesch S, Jabbari K, Jubin C, Kawai H, Kimura K, Kloareg B, Küpper F C, Lang D, Le Bail A, Leblanc C, Lerouge P, Lohr M, Lopez P J, Martens C, Maumus F, Michel G, Miranda-Saavedra D, Morales J, Moreau H, Motomura T, Nagasato C, Napoli C A, Nelson D R, Nyvall-Collén P, Peters A F, Pommier C, Potin P, Poulain J, Quesneville H, Read B, Rensing S A, Ritter A, Rousvoal S, Samanta M, Samson G, Schroeder D C, Ségurens B, Strittmatter M, Tonon T, Tregear J W, Valentin K, Von Dassow P, Yamagishi T, Van De Peer Y, Wincker P. 2010. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature, 465 (7298): 617–621.CrossRefGoogle Scholar
  19. Cockburn D W, Koropatkin N M. 2016. Polysaccharide degradation by the intestinal microbiota and its influence on human health and disease. J. Mol. Biol., 428 (16): 3 230–3 252.CrossRefGoogle Scholar
  20. Collén J, Porcel B, Carré W, Ball S G, Chaparro C, Tonon T, Barbeyron T, Michel G, Noel B, Valentin K, Elias M, Artiguenave F, Arun A, Aury J M, Barbosa-Neto J F, Bothwell J H, Bouget F Y, Brillet L, Cabello-Hurtado F, Capella-Gutiérrez S, Charrier B, Cladière L, Cock J M, Coelho S M, Colleoni C, Czjzek M, Da Silva C, Delage L, Denoeud F, Deschamps P, Dittami S M, Gabaldón T, Gachon C M, Groisillier A, Hervé C, Jabbari K, Katinka M, Kloareg B, Kowalczyk N, Labadie K, Leblanc C, Lopez P J, McLachlan D H, Meslet-Cladiere L, Moustafa A, Nehr Z, Nyvall Collén P, Panaud O, Partensky F, Poulain J, Rensing S A, Rousvoal S, Samson G, Symeonidi A, Weissenbach J, Zambounis A, Wincker P, Boyen C. 2013. Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc. Natl. Acad. Sci. U. S. A., 110 (13): 5 247–5 252.CrossRefGoogle Scholar
  21. Cornish M L, Critchley A T, Mouritsen O G. 2017. Consumption of seaweeds and the human brain. J. Appl. Phycol., 29 (5): 2 377–2 398.CrossRefGoogle Scholar
  22. Cox S, Turley G H, Rajauria G, Abu-Ghannam N, Jaiswal A K. 2014. Antioxidant potential and antimicrobial efficacy of seaweed ( Himanthalia elongata ) extract in model food systems. J. Appl. Phycol., 26 (4): 1 823–1 831.CrossRefGoogle Scholar
  23. Croft M T, Lawrence A D, Raux-Deery E, Warren M J, Smith A G. 2005. Algae acquire vitamin B 12 through a symbiotic relationship with bacteria. Nature, 438 (7064): 90–93.CrossRefGoogle Scholar
  24. Croft M T, Warren M J, Smith A G. 2006. Algae need their vitamins. Eukar yot Cell, 5 (8): 1 175–1 183.CrossRefGoogle Scholar
  25. Crowley E K, Long-Smith C M, Murphy A, Patterson E, Murphy K, O’Gorman D M, Stanton C, Nolan Y M. 2018. Dietary supplementation with a magnesium-rich marine mineral blend enhances the diversity of gastrointestinal microbiota. Mar. Drugs, 16 (6): 216, CrossRefGoogle Scholar
  26. Cryan J F, Dinan T G. 2012. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci., 13 (10): 701–712.CrossRefGoogle Scholar
  27. Cunnane S C, Crawford M A. 2014. Energetic and nutritional constraints on infant brain development: implications for brain expansion during human evolution. J. Human Evol., 77: 88–98.CrossRefGoogle Scholar
  28. Das A, Srinivasan M, Ghosh T S, Mande S S. 2016. Xenobiotic metabolism and gut microbiomes. PLoS One, 11 (10): e0163099.CrossRefGoogle Scholar
  29. Davenport E R, Sanders J G, Song S J, Amato K R, Clark A G, Knight R. 2017. The human microbiome in evolution. BMC Biol., 15: 127, CrossRefGoogle Scholar
  30. De Clerck O, Bogaert K A, Leliaert F. 2012. Diversity and evolution of algae: primary endosymbiosis. Adv. Bot. Res., 64: 56–86.Google Scholar
  31. De Jesus Raposo M F, De Morais A M M B, De Morais R M S C. 2016. Emergent sources of prebiotics: seaweeds and microalgae. Mar. Drugs, 14 (2): 27.CrossRefGoogle Scholar
  32. Den Besten G, Van Eunen K, Groen A K, Venema K, Reijngoud D J, Bakker B M. 2013. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res., 54 (9): 2 325–2 340.CrossRefGoogle Scholar
  33. Devillé C, Gharbi M, Dandrifosse G, Peulen O. 2007. Study on the effects of laminarin, a polysaccharide from seaweed, on gut characteristics. J. Sci. Food Agric., 87 (9): 1 717–1 725.CrossRefGoogle Scholar
  34. Dillehay T D, Ramírez C, Pino M, Collins M B, Rossen J, Pino-Navarro J D. 2008. Monte Verde: seaweed, food, medicine, and the peopling of South America. Science, 320 (5877): 784–786.CrossRefGoogle Scholar
  35. Donia M S, Cimermancic P, Schulze C J, Brown L C W, Martin J, Mitreva M, Clardy J, Linington R G, Fischbach M A. 2014. A systematic analysis of biosynthetic gene clusters in the human microbiome reveals a common family of antibiotics. Cell, 158 (6): 1 402–1 414.CrossRefGoogle Scholar
  36. Duncan S H, Lobley G E, Holtrop G, Ince J, Johnstone A M, Louis P, Flint H J. 2008. Human colonic microbiota associated with diet, obesity and weight loss. Int. J. Obes., 32 (11): 1 720–1 724.CrossRefGoogle Scholar
  37. El Kaoutari A, Armougom F, Gordon J I, Raoult D, Henrissat B. 2013. The abundance and variety of carbohydrateactive enzymes in the human gut microbiota. Nat. Rev. Microbiol., 11 (7): 497–504.CrossRefGoogle Scholar
  38. Elson C O. 2000. Commensal bacteria as targets in Crohn’s disease. Gastroenterology, 119 (1): 254–257.CrossRefGoogle Scholar
  39. Erny D, Hrabě De Angelis A L, Jaitin D, Wieghofer P, Staszewski O, David E, Keren-Shaul H, Mahlakoiv T, Jakobshagen K, Buch T, Schwierzeck V, Utermöhlen O, Chun E, Garrett W S, McCoy K D, Diefenbach A, Staeheli P, Stecher B, Amit I, Prinz M. 2015. Host microbiota constantly control maturation and function of microglia in the CNS. Nat. Neurosci., 18 (7): 965–977.CrossRefGoogle Scholar
  40. Farzi A, Fröhlich E E, Holzer P. 2018. Gut microbiota and the neuroendocrine system. Neurotherapeutics, 15 (1): 5–22.CrossRefGoogle Scholar
  41. Flórez L V, Biedermann P H W, Engl T, Kaltenpoth M. 2015. Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms. Nat. Prod. Rep., 32 (7): 904–936.CrossRefGoogle Scholar
  42. Garbary D J, London J F. 1995. The Ascophylluml Polysiphonial Mycosphaerella symbiosis V. Fungal infection protects A. nosodum from desiccation. Bot. Mar., 38 (1-6): 529–533.Google Scholar
  43. Gibson G R, Hutkins R, Sanders M E, Prescott S L, Reimer R A, Salminen S J, Scott K, Stanton C, Swanson K S, Cani P D, Verbeke K, Reid G. 2017. Expert consensus document: the international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat. Rev. Gastroenterol. Hepatol., 14 (8): 491–502.Google Scholar
  44. Gibson G R, Scott K P, Rastall R A, Tuohy K M, Hotchkiss A, Dubert-Ferrandon A, Gareau M G, Murphy E F, Saulnier D M, Loh G, Macfarlane S, Delzenne N, Ringel Y, Kozianowski G, Dickmann R, Lenoir-Wijnkoop I, Walker C, Buddington R K. 2010. Dietary prebiotics: current status and new definition. Food Sci. Technol. Bull.: Funct. Foods, 7 (1): 1–19.Google Scholar
  45. Gibson G, Dworkin I. 2004. Uncovering cryptic genetic variation. Nat. Rev. Genet., 5. (9): 681–690.CrossRefGoogle Scholar
  46. Global Burden of Disease Collaborators. 2017. Global, regional, and national incidence, prevalence, and years lived with disability for 328 diseases and injuries for 195 countries, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. The Lancet, 390 (10100): 1 211–1 259, Google Scholar
  47. Goecke F, Labes A, Wiese J, Imhoff J F. 2010. Chemical interactions between marine macroalgae and bacteria. Mar. Ecol. Prog. Ser., 409: 267–300.CrossRefGoogle Scholar
  48. Goraya J S, Kaur S, Mehra B. 2015. Neurology of nutritional vitamin B 12 deficiency in infants: case series from India and literature review. J. Child. Neurol., 30 (13): 1 831–1837.CrossRefGoogle Scholar
  49. Haygood R, Fedrigo O, Hanson B, Yokoyama K D, Wray G A. 2007. Promoter regions of many neural- and nutritionrelated genes have experienced positive selection during human evolution. Nat. Genet., 39 (9): 1 140–1 144.CrossRefGoogle Scholar
  50. Hehemann J H, Correc G, Barbeyron T, Helbert W, Czjzek M, Michel G. 2010. Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature, 464 (7290): 908–912.CrossRefGoogle Scholar
  51. Hehemann J H, Kelly A G, Pudlo N A, Martens E C, Boraston A B. 2012. Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes. Proc. Natl. Acad. Sci. U. S. A., 109 (48): 19 786–19 791.CrossRefGoogle Scholar
  52. Helliwell K E, Collins S, Kazamia E, Purton S, Wheeler G L, Smith A. 2015. Fundamental shift in vitamin B 12 ecophysiology of a model alga demonstrated by experimental evolution. ISME J., 9 (6): 1 446–1 455.CrossRefGoogle Scholar
  53. Holdt S L, Kraan S. 2011. Bioactive compounds in seaweed: functional food applications and legislation. J. Appl. Phycol., 23 (3): 543–597.CrossRefGoogle Scholar
  54. Holloway R L, Sherwood C C, Hof P R, Rilling J K. 2009. Evolution of the brain in humans-paleoneurology. In: Binder M D, Hirokawa N, Windhorst U eds. Encyclopedia of Neuroscience. Springer-Verlag, Berlin. p.1 326–1 334.CrossRefGoogle Scholar
  55. Hoyles L, Snelling T, Umlai U K, Nicholson J K, Carding S R, Glen R C, McArthur S. 2018. Microbiome-host systems interactions: protective effects of propionate upon the blood-brain barrier. Microbiome, 6: 55, CrossRefGoogle Scholar
  56. Hutkins R W, Krumbeck J A, Bindels L B, Cani P D, Fahey G Jr, Goh Y J, Hamaker B, Martens E C, Mills D A, Rastal R A, Vaughan E, Sanders M E. 2016. Prebiotics: why definitions matter. Curr. Opin. Biotechnol., 37: 1–7.CrossRefGoogle Scholar
  57. Ikeda S, Okubo T, Anda M, Nakashita H, Yasuda M, Sato S, Kaneko T, Tabata S, Eda S, Momiyama A, Terasawa K, Mitsui H, Minamisawa K. 2010. Community- and genome-based views of plant-associated bacteria: plantbacterial interactions in soybean and rice. Plant Cell Physiol., 51 (9): 1 398–1 410.CrossRefGoogle Scholar
  58. Jiménez-Escrig A, Gómez-Ordóñez E, Tenorio M D, Rupérez P. 2013. Antioxidant and prebiotic effects of dietary fiber co-travelers from sugar Kombu in healthy rats. J. Appl. Phycol., 25 (2): 503–512.CrossRefGoogle Scholar
  59. Jocken J W E, González Hernández M A, Hoebers N T H, Van Der Beek C M, Essers Y P G, Blaak E E, Canfora E E. 2018. Short-chain fatty acids differentially affect intracellular lipolysis in a human white adipocyte model. Front. Endocrinol., 8: 372, CrossRefGoogle Scholar
  60. Jutur P P, Nesamma A A, Shaikh M R. 2016. Algae-derived marine oligosaccharides and their biological applications. Front. Mar. Sci., 3 (39): 83.Google Scholar
  61. Kadam S U, O’Donnell C P, Rai D K, Hossain M B, Burgess C M, Walsh D, Tiwari B K. 2015. Laminarin from Irish brown seaweeds Ascophyllum nodosum and Laminaria hyperborea: ultrasound assisted extraction, characterization and bioactivity. Mar. Drugs, 13 (7): 4 270–4 280.CrossRefGoogle Scholar
  62. Kausalya M, Narasimha Rao G M. 2015. Antimicrobial activity of marine algae. J. Algal Biomass Utln., 6 (1): 78–87.Google Scholar
  63. Kazamia E, Czesnick H, Van Nguyen T T, Croft M T, Sherwood E, Sasso S, Hodson S J, Warren M J, Smith A G. 2012. Mutualistic interactions between vitamin B 12-dependent algae and heterotrophic bacteria exhibit regulation. Environ. Microbiol., 14 (6): 1 466–1 476.CrossRefGoogle Scholar
  64. Kearney S M, Gibbons S M, Erdman S E, Alm E J. 2018. Orthogonal dietary niche enables reversible engraftment of a gut bacterial commensal. BioRxiv, Google Scholar
  65. Kim J Y, Kwon Y M, Kim I S, Kim J A, Yu D Y, Adhikari B, Lee S S, Choi I S, Cho K K. 2018. Effects of the brown seaweed Laminaria japonica supplementation on serum concentrations of IgG, triglycerides, and cholesterol, and intestinal microbiota composition in rats. Front. Nutr., 5: 23, CrossRefGoogle Scholar
  66. Kim J Y, Yu D Y, Kim J A, Choi E Y, Lee C Y, Hong Y H, Kim C W, Lee S S, Choi I S, Cho K K. 2016. Effects of Undaria pinnatifida and Laminaria japonica on rat’s intestinal microbiota and metabolite. J. Nutr. Food Sci., 6 (3): 502, Google Scholar
  67. Knoll A H. 2011. The multiple origins of complex multicellularity. Annu. Rev. Earth Planet. Sci., 39: 217–239.CrossRefGoogle Scholar
  68. Kovatcheva-Datchary P, Nilsson A, Akrami R, Lee Y S, De Vadder F, Arora T, Hallen A, Martens E, Björck I, Bäckhed F. 2015. Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of Prevotella. Cell Metab., 22 (6): 971–982.CrossRefGoogle Scholar
  69. Kulshreshtha G, Rathgeber B, Stratton G, Thomas N, Evans F, Critchley A, Hafting J, Prithiviraj B. 2014. Feed supplementation with red seaweeds, Chondrus crispus and Sarcodiotheca gaudichaudii, affects performance, egg quality, and gut microbiota of layer hens. Poul t. Sci., 93 (12): 2 991–3 001, CrossRefGoogle Scholar
  70. Kyriacou K, Parkington J E, Marais A D, Braun D R. 2014. Nutrition, modernity and the archaeological record: coastal resources and nutrition among Middle Stone Age hunter-gatherers on the Western Cape coast of South Africa. J. Human Evol., 77: 64–73.CrossRefGoogle Scholar
  71. Lahaye M. 1991. Marine algae as sources of fibres: determination of soluble and insoluble dietary fibre contents in some ‘sea vegetables’. J. Sci. Food Agric., 54 (4): 587–594.CrossRefGoogle Scholar
  72. Le Chatelier E, Nielsen T, Qin J J, Prifti E, Hildebrand F, Falony G, Almeida M, Arumugam M, Batto J M, Kennedy S, Leonard P, Li J H, Burgdorf K, Grarup N, Jørgensen T, Brandslund I, Nielsen H B, Juncker A S, Bertalan M, Levenez F, Pons N, Rasmussen S, Sunagawa S, Tap J, Tims S, Zoetendal E G, Brunak S, Clément K, Doré J, Kleerebezem M, Kristiansen K, Renault P, Sicheritz-Ponten T, De Vos W M, Zucker J D, Raes J, Hansen T, MetaHIT Consortium, Bork P, Wang J, Ehrlich S D, Pedersen O. 2013. Richness of human gut microbiome correlates with metabolic markers. Nature, 500 (7464): 541–546.CrossRefGoogle Scholar
  73. Leliaert F, Tronholm A, Lemieux C, Turmel M, DePriest M S, Bhattacharya D, Karol K G, Fredericq S, Zechman F W, Lopez-Bautista J M. 2016. Chloroplast phylogenomic analyses reveal the deepest-branching lineage of the Chlorophyta, Palmophyllophyceae class. nov. Sci. Rep., 6: 25 367, CrossRefGoogle Scholar
  74. Ley R E, Bäckhed F, Turnbaugh P J, Lozupone C A, Knight R D, Gordon J I. 2005. Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. U. S. A., 102 (31): 11 070–11 075.CrossRefGoogle Scholar
  75. Ley R E, Hamady M, Lozupone C, Turnbaugh P J, Ramey R R, Bircher J S, Schlegel M L, Tucker T A, Schrenzel M D, Knight R, Gordon J I. 2008. Evolution of mammals and their gut microbes. Science, 320 (5883): 1 647–1 651.CrossRefGoogle Scholar
  76. Ley R E, Turnbaugh P J, Klein S, Gordon J I. 2006. Microbial ecology: Human gut microbes associated with obesity. Nature, 444 (7122): 1 022–1 023.CrossRefGoogle Scholar
  77. Liu J H, Kandasamy S, Zhang J Z, Kirby C W, Karakach T, Hafting J, Critchley A T, Evans F, Prithiviraj B. 2015. Prebiotic effects of diet supplemented with the cultivated red seaweed Chondrus crispus or with fructo-oligosaccharide on host immunity, colonic microbiota and gut microbial metabolites. BMC Complement. Altern. Med., 15: 279, CrossRefGoogle Scholar
  78. Lloyd-Price J, Abu-Ali G, Huttenhower C. 2016. The healthy human microbiome. Genome Med., 8 (1): 51, CrossRefGoogle Scholar
  79. Long S R. 2001. Genes and signals in the Rhizobium -legume symbiosis. Plant Physiol., 125 (1): 69–72.CrossRefGoogle Scholar
  80. MacFabe D. 2013. Autism: metabolism, mitochondria, and the microbiome. Global Adv. Health Med., 2 (6): 52–66.CrossRefGoogle Scholar
  81. Margulis L. 1974. Origin and evolution of the eukaryotic cell. Taxono, 23 (2-3): 225–226.Google Scholar
  82. Margulis L. 1993. Symbiosis in Cell Evolution: Microbial Communities in the Archean and Proterozoic Eons. 2 nd edn. Freeman, New York. 448p.Google Scholar
  83. Marshall K, Joint I, Callow M E, Callow J A. 2006. Effect of marine bacterial isolates on the growth and morphology of axenic plantlets of the green alga Ulva linza. Microbial Ecol., 52 (2): 302–310.CrossRefGoogle Scholar
  84. Martens E C, Kelly A G, Tauzin A S, Brumer H. 2014. The devil lies in the details: how variations in polysaccharide fine-structure impact the physiology and evolution of gut microbes. J Mol. Biol., 426 (23): 3 851–3 865.CrossRefGoogle Scholar
  85. Mazmanian S K, Liu C H, Tzianabos A O, Kasper D L. 2005. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell, 122 (1): 107–118.CrossRefGoogle Scholar
  86. Mazmanian S K, Round J L, Kasper D L. 2008. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature, 453 (7195): 620–625.CrossRefGoogle Scholar
  87. Miranda L N, Hutchison K, Grossman A R, Brawley S H. 2013. Diversity and abundance of the bacterial community of the red macroalga Porphyra umbilicalis: did bacterial farmers produce macroalgae? PLoS One, 8 (3): e58269.CrossRefGoogle Scholar
  88. Moeller A H, Caro-Quintero A, Mjungu D, Georgiev A V, Lonsdorf E V, Muller M N, Pusey A E, Peeters M, Hahn B H, Ochman H. 2016. Cospeciation of gut microbiota with hominids. Science, 353 (6297): 380–382, CrossRefGoogle Scholar
  89. Moos W H, Faller D V, Harpp D N, Kanara I, Pernokas J, Powers W R, Steliou K. 2016. Microbiota and neurological disorders: a gut feeling. BioRes. Open Access, 5 (1): 137–145.CrossRefGoogle Scholar
  90. Mouritsen O G. 2013. Seaweeds: Edible, Available & Sustainable. University of Chicago Press, Chicago.CrossRefGoogle Scholar
  91. Moya-Pérez A, Luczynski P, Renes I B, Wang S G, Borre Y, Ryan C A, Knol J, Stanton C, Dinan T G, Cryan J F. 2017. Intervention strategies for cesarean section-induced alterations in the microbiota-gut-brain axis. Nutr. Rev., 75 (4): 225–240.CrossRefGoogle Scholar
  92. Muegge B D. 2013. The Influence of Diet on the Mammalian Gut Microbiome. Washington University, St. Louis, Missouri.Google Scholar
  93. Nanjundappa R H, Ronchi F, Wang J G, Clemente-Casares X, Yamanouchi J, Umeshappa C S, Yang Y, Blanco J, Bassolas-Molina H, Salas A, Khan H, Slattery R M, Wyss M, Mooser C, Macpherson A J, Sycuro L K, Serra P, McKay D M, McCoy K D, Santamaria P. 2017. A gut microbial mimic that hijacks diabetogenic autoreactivity to suppress colitis. Cell, 171 (3): 655–667.e17.CrossRefGoogle Scholar
  94. Nowack E C M, Weber A P M. 2018. Genomics-informed insights into endosymbiotic organelle evolution in photosynthetic eukaryotes. Annu. Rev. Plant Biol., 69: 51–84, CrossRefGoogle Scholar
  95. O’Doherty J V, Dillon S, Figat S, Callan J J, Sweeney T. 2010. The effects of lactose inclusion and seaweed extract derived from Laminaria spp. on performance, digestibility of diet components and microbial populations in newly weaned pigs. Anim. Feed Sci. Technol., 157 (3-4): 173–180.CrossRefGoogle Scholar
  96. O’Hara A M, Shanahan F. 2006. The gut flora as a forgotten organ. EMBO Rep., 7 (7): 688–693.CrossRefGoogle Scholar
  97. Okolie C L, Rajendran S R C K, Udenigwe C C, Aryee A N A, Mason B. 2017. Prospects of brown seaweed polysaccharides (BSP) as prebiotics and potential immunomodulators. J. Food Biochem., 41 (5): e12392, CrossRefGoogle Scholar
  98. Oriach C S, Robertson R C, Stanton C, Cryan J F, Dinan T G. 2016. Food for thought: the role of nutrition in the microbiota-gut-brain axis. Clin. Nutr. Exp., 6: 25–38.CrossRefGoogle Scholar
  99. Pérez M J, Falqué E, Domínguez H. 2016. Antimicrobial action of compounds from marine seaweed. Mar. Drugs, 14 (3): 52, CrossRefGoogle Scholar
  100. Perry R J, Peng L, Barry N A, Cline G W, Zhang D Y, Cardone R L, Petersen K F, Kibbey R G, Goodman A L, Shulman G I. 2016. Acetate mediates a microbiome-brain-β-cell axis to promote metabolic syndrome. Nature, 534 (7606): 213–217.CrossRefGoogle Scholar
  101. Popper Z A, Michel G, Hervé C, Domozych D S, Willats W G T, Tuohy M G, Kloareg B, Stengel D B. 2011. Evolution and diversity of plant cell walls: from algae to flowering plants. Annu. Rev. Plant Biol., 62: 567–590.CrossRefGoogle Scholar
  102. Provasoli L, Pintner I J. 1980. Bacteria induced polymorphism in an axenic laboratory strain of Ulva lactuca (Chlorophyceae). J. Phycol., 16 (2): 196–200.CrossRefGoogle Scholar
  103. Qin J J, Li R Q, Raes J, Arumugam M, Burgdorf K S, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende D R, Li J H, Xu J M, Li S C, Li D F, Cao J J, Wang B, Liang H Q, Zheng H S, Xie Y L, Tap J, Lepage P, Bertalan M, Batto J M, Hansen T, Le Paslier D, Linneberg A, Nielsen H B, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H M, Yu C, Li S T, Jian M, Zhou Y, Li Y R, Zhang X Q, Li S G, Qin N, Yang H M, Wang J, Brunak S, Doré J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J; MetaHIT Consortium, Bork P, Ehrlich S D, Wang J. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature, 464 (7285): 59–65, CrossRefGoogle Scholar
  104. Rauma A L, Törrönen R, Hänninen O, Mykkänen H. 1995. Vitamin B-12 status of long-term adherents of a strict uncooked vegan diet (“living food diet”) is compromised. J. Nutr., 125. (10): 2 511–2 515.Google Scholar
  105. Rebuffet E, Groisillier A, Thompson A, Jeudy A, Barbeyron T, Czjzek M, Michel G. 2011. Discovery and structural characterization of a novel glycosidase family of marine origin. Environ. Microbiol., 13 (5): 1 253–1 270.CrossRefGoogle Scholar
  106. Ríos-Covián D, Ruas-Madiedo P, Margolles A, Gueimonde M, De Los Reyes-Gavilán C G, Salazar N. 2016. Intestinal short chain fatty acids and their link with diet and human health. Front. Microbiol., 7: 185, CrossRefGoogle Scholar
  107. Riscuta G, Xi D, Pierre-Victor D, Starke-Reed P, Khalsa J, Duffy L. 2018. Diet, microbiome, and epigenetics in the era of precision medicine. In: Dumitrescu R G, Verma M eds. Cancer Epigenetics for Precision Medicine. Humana Press, New York, NY. p.141–156.CrossRefGoogle Scholar
  108. Roszyk E, Puszczewicz M. 2017. Role of human microbiome and selected bacterial infections in the pathogenesis of rheumatoid arthritis. Reumatol ogia, 55 (5): 242–250.CrossRefGoogle Scholar
  109. Roumeliotis N, Dix D, Lipson A. 2012. Vitamin B 12 deficiency in infants secondary to maternal causes. CMAJ, 184 (14): 1 593–1 598.CrossRefGoogle Scholar
  110. Round J L, Mazmanian S K. 2009. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol., 9 (5): 313–323.CrossRefGoogle Scholar
  111. Salvia-Trujillo L, Sun Q, Um B H, Park Y, McClements D J. 2015. In vitro and in vivo study of fucoxanthin bioavailability from nanoemulsion-based delivery systems: impact of lipid carrier type. J. Func. Foods, 17: 293–304.CrossRefGoogle Scholar
  112. Sawicki C M, Livingston K A, Obin M, Roberts S B, Chung M, McKeown N M. 2017. Dietary fiber and the human gut microbiota: application of evidence mapping methodology. Nutrients, 9 (2): 125, CrossRefGoogle Scholar
  113. Schoenemann P T. 2006. Evolution of the size and functional areas of the human brain. Annu. Rev. Anthropol., 35: 379–406.CrossRefGoogle Scholar
  114. Seetharam B, Alpers D H. 1982. Absorption and transport of cobalamin (vitamin B 12). Annu. Rev. Nutr., 2: 343–369.CrossRefGoogle Scholar
  115. Siavoshian S, Segain J P, Kornprobst M, Bonnet C, Cherbut C, Galmiche J P, Blottière H M. 2000. Butyrate and trichostatin A effects on the proliferation/differentiation of human intestinal epithelial cells: induction of cyclin D3 and p21 expression. Gut, 46 (4): 507–514.CrossRefGoogle Scholar
  116. Singh R P, Bijo A J, Baghel R S, Reddy C R K, Jha B. 2011. Role of bacterial isolates in enhancing the bud induction in the industrially important red alga Gracilaria dura. FEMS Microbiol. Ecol., 76 (2): 381–392.CrossRefGoogle Scholar
  117. Singh R P, Reddy C R K. 2014. Seaweed-microbial interactions: key functions of seaweed-associated bacteria. FEMS Microbiol. Ecol., 88 (2): 213–230.CrossRefGoogle Scholar
  118. Sonnenburg E D, Smits S A, Tikhonov M, Higginbottom S K, Wingreen N S, Sonnenburg J L. 2016. Diet-induced extinctions in the gut microbiota compound over generations. Nature, 529 (7585): 212–215.CrossRefGoogle Scholar
  119. Sonnenburg J L. 2010. Genetic pot luck. Nature, 464 (7920): 837–838.CrossRefGoogle Scholar
  120. Stengel D B, Connan S, Popper Z A. 2011. Algal chemodiversity and bioactivity: sources of natural variability and implications for commercial application. Biotechnol. Adv., 29 (5): 483–501.CrossRefGoogle Scholar
  121. Stevens C E, Hume I D. 1998. Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol. Rev., 78 (2): 393–427.CrossRefGoogle Scholar
  122. Tattersall I. 2014. Diet as driver and constraint in human evolution. J. Human Evol., 77: 141–142.CrossRefGoogle Scholar
  123. The Human Microbiome Project Consortium. 2012. Structure, function and diversity of the healthy human microbiome. Nature, 486 (7402): 207–214.CrossRefGoogle Scholar
  124. Thiba A, Umar C A, Myende S, Nweke E, Rumbold K, Candy G. 2017. Differences in microbiome in rat models of cardiovascular disease. S. Afr. J. Surg., 55 (2): 71.Google Scholar
  125. Thomas F, Hehemann J H, Rebuffet E, Czjzek M, Michel G. 2011. Environmental and gut Bacteroidetes: the food connection. Front. Microbiol., 2: 93, CrossRefGoogle Scholar
  126. Tramontano M, Andrejev S, Pruteanu M, Klünemann M, Kuhn M, Galardini M, Jouhten P, Zelezniak A, Zeller G, Bork P, Typas A, Patil K R. 2018. Nutritional preferences of human gut bacteria reveal their metabolic idiosyncrasies. Nat. Microbiol., 3 (4): 514–522.CrossRefGoogle Scholar
  127. Verhaegen M, Munro S. 2011. Pachyosteosclerosis suggests archaic Homo frequently collected sessile littoral foods. HOMO, 62 (4): 237–247.CrossRefGoogle Scholar
  128. Vital M, Karch A, Pieper D H. 2017. Colonic butyrateproducing communities in humans: an overview using omics data. mSystems, 2 (6): e00130–17, CrossRefGoogle Scholar
  129. Von Schenck U, Bender-Götze C, Koletzko B. 1997. Persistence of neurological damage induced by dietary vitamin B-12 deficiency in infancy. Arch. Dis. Child., 77 (2): 137–139.CrossRefGoogle Scholar
  130. Wang M P, Chen L, Li YT, Chen L, Liu Z Y, Wang X J, Yan P S, Qin S. 2018a. Responses of soil microbial communities to a short-term application of seaweed fertilizer revealed by deep amplicon sequencing. Appl. Soil Ecol., 125: 288–296, CrossRefGoogle Scholar
  131. Wang S G, Harvey L, Martin R, Van Der Beek E M, Knol J, Cryan J, Renes I B. 2018b. Targeting the gut microbiota to influence brain development and function in early life. Neurosci. Biobehav. Rev., 95: 191–201, CrossRefGoogle Scholar
  132. Wanyonyi S, Du Preez R, Brown L, Paul N A, Panchal S K. 2017. Kappaphycus alvarezii as a food supplement prevents diet-induced metabolic syndrome in rats. Nutrients, 9 (11): 1 261.CrossRefGoogle Scholar
  133. Watanabe F, Yabuta Y, Bito T, Teng F. 2014. Vitamin B 12 - containing plant food sources for vegetarians. Nutrients, 6 (5): 1 861–1 873.CrossRefGoogle Scholar
  134. Wells M L, Potin P, Craigie J S, Raven J A, Merchant S S, Helliwell K E, Smith A G, Camire M E, Brawley S H. 2017. Algae as nutritional and functional food sources: revisiting our understanding. J. Appl. Phycol., 29 (2): 949–982.CrossRefGoogle Scholar
  135. West C E, Jenmalm M C, Prescott S L. 2015. The gut microbiota and its role in the development of allergic disease: a wider perspective. Clin. Exp. Allergy, 45 (1): 43–53.CrossRefGoogle Scholar
  136. WHO (World Health Organization). 2018. World Health Statistics 2018: Monitoring Health for the SDGs, Sustainable Development Goals. Google Scholar
  137. Williams A G, Withers S, Sutherland A D. 2013. The potential of bacteria isolated from ruminal contents of seaweedeating North Ronaldsay sheep to hydrolyse seaweed components and produce methane by anaerobic digestion in vitro. Microb. Biotech nol., 6 (1): 45–52, CrossRefGoogle Scholar
  138. Woznica A, Gerdt J P, Hulett R E, Clardy J, King N. 2017. Mating in the closest living relatives of animals is induced by a bacterial chondroitinase. Cell, 170 (6): 1 175–1 183. e11.CrossRefGoogle Scholar
  139. Wu G D, Chen J, Hoffman C, Bittinger K, Chen Y Y, Keilbaugh S A, Bewtra M, Knights D, Walters W A, Knight R, Sinha R, Gilroy E, Gupta K, Baldassano R, Nessel L, Li H Z, Bushman F D, Lewis J D. 2011. Linking long-term dietary patterns with gut microbial enterotypes. Science, 334 (6052): 105–108.CrossRefGoogle Scholar
  140. Xiong Y Q, Yang R, Sun X X, Yang H T, Chen H M. 2017. Effect of the epiphytic bacterium Bacillus sp. WPySW2 on the metabolism of Pyropia haitanensis. J. Appl. Phycol., 30 (2): 1 225–1 237, CrossRefGoogle Scholar
  141. You X M, Einson J E, Lopez-Pena C L, Song M Y, Xiao H, McClements D J, Sela D A. 2017. Food-grade cationic antimicrobial ɛ-polylysine transiently alters the gut microbial community and predicted metagenome function in CD-1 mice. NPJ Sci. Food, 1: 8. CrossRefGoogle Scholar
  142. Zhang Z S, Wang X M, Han S W, Liu C D, Liu F. 2018. Effect of two seaweed polysaccharides on intestinal microbiota in mice evaluated by illumina PE250 sequencing. Int. J. Biol. Macromol., 112: 796–802.CrossRefGoogle Scholar
  143. Zhou M, Hunerberg M, Chen Y H, Reuter T, McAllister T A, Evans F, Critchley A T, Guan L L. 2018. Air-dried brown seaweed, Ascophyllum nodosum, alters the rumen microbiome in a manner that changes rumen fermentation profiles and lowers the prevalence of foodborne pathogens. mSphere, 3 (1): e00017–18. CrossRefGoogle Scholar
  144. Zilber-Rosenberg I, Rosenberg E. 2008. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev., 32 (5): 723–735.CrossRefGoogle Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • M. Lynn Cornish
    • 1
    Email author
  • Ole G. Mouritsen
    • 2
  • Alan T. Critchley
    • 3
  1. 1.Acadian Seaplants Limited, James S. Craigie Research CenterCornwallisCanada
  2. 2.University of Copenhagen, Department of Food Science and Taste for Life, Design and Consumer Behavior, Nordic Food LabFrederiksbergDenmark
  3. 3.Verschuren Centre for Sustainability in Energy and the EnvironmentCape Breton UniversitySydneyCanada

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