Fermentation of mannitol extracts from brown macro algae by thermophilic Clostridia

Frontiers in Microbiology

Volumn 9, Issue AUG, 2018, Pages

  Chades, Theo ^a   Scully, Sean M ^a   Ingvadottir, Eva M ^a   Orlygsson, Johann ^a  

^a UNIVERSITY OF AKUREYRI   (Iceland)

Author keywords

Ascophyllum nodosum; Bioethanol; Bioprocessing; Extremophiles; Laminaria digitata; Seaweed; Thermoanaerobacter; Third generation biomass

Indexed keywords

ALCOHOL; ALGAL EXTRACT; MANNITOL; PHENOL DERIVATIVE;

ARTICLE; ASCOPHYLLUM; ASCOPHYLLUM NODOSUM; BROWN ALGA; CALDANAEROBACTER; CALDANAEROBACTER SUBTERRANEUS SUBSP. PACIFICUS; CALDANAEROBACTER SUBTERRANEUS SUBSP. SUBTERRANEUS; CALDANAEROBACTER SUBTERRANEUS SUBSP. TENGCONGENSIS; CALDANAEROBACTER SUBTERRANEUS SUBSP. YONSEIENSIS; CALDANAEROBACTER UZONENSIS; CALDANAEROBIUS; CALDANAEROBIUS FIJIENSIS; CALDANAEROBIUS POLYSACCHAROLYTICUS; CALDANAEROBIUS ZEAE; CALDICELLULOSIRUPTOR; CALDICELLULOSIRUPTOR ACETIGENUS; CALDICELLULOSIRUPTOR BESCII; CALDICELLULOSIRUPTOR CHANGBAIENSIS; CALDICELLULOSIRUPTOR HYDROTHERMALIS; CALDICELLULOSIRUPTOR KRISTJANSSONII; CALDICELLULOSIRUPTOR KRONOTSKIENSIS; CALDICELLULOSIRUPTOR LACTOACETICUS; CALDICELLULOSIRUPTOR OWENSIS; CALDICELLULOSIRUPTOR SACCHAROLYTICUS; CLOSTRIDIA; CONTROLLED STUDY; FERMENTATION; LAMINARIA; LAMINARIA DIGITATA; MICROBIAL BIOMASS; NONHUMAN; THERMOANAEROBACTER; THERMOANAEROBACTER ACETOETHYLICUS; THERMOANAEROBACTER BROCKII; THERMOANAEROBACTER BROCKII SUBSP. FINNII; THERMOANAEROBACTER BROCKII SUBSP. LACTIETHYLICUS; THERMOANAEROBACTER ETHANOLICUS; THERMOANAEROBACTER ITALICUS; THERMOANAEROBACTER KIVUI; THERMOANAEROBACTER MATHRANI SUBSP. MATHRANI; THERMOANAEROBACTER PENTOSACEUS; THERMOANAEROBACTER PSEUDOETHANOLICUS; THERMOANAEROBACTER SIDEROPHILUS; THERMOANAEROBACTER SULFURIGIGNENS; THERMOANAEROBACTER SULFUROPHILUS; THERMOANAEROBACTER THERMOHYDROSULFURICUS; THERMOANAEROBACTER UZONENSIS; THERMOANAEROBACTER WIEGELII; THERMOANAEROBACTERIUM; THERMOANAEROBACTERIUM ACIDITOLERANS; THERMOANAEROBACTERIUM AOTEAROENSE; THERMOANAEROBACTERIUM SACCHAROLYTICUM; THERMOANAEROBACTERIUM THERMOSACCHAROLYTICUM; THERMOANAEROBACTERIUM THERMOSTERCORIS; THERMOANAEROBACTERIUM THERMOSULFURIGENES; THERMOANAEROBACTERIUM XYLANOLYTICUM; THERMOBRACHIUM; THERMOBRACHIUM CELERE;

EID: 85051854119     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2018.01931     Document Type: Article

References (51)

1. Adams, J. M. M., Ross, A. B., Anastasakis, K., Hodgson, E. M., Gallagher, J. A., Jones, J. M., et al. (2011). Seasonal variation in the chemical composition of the bioenergy feedstock Laminaria digitata for thermochemical conversion. Bioresour. Technol. 102, 226-234. doi: 10.1016/j.biortech.2010.06.152
2. Bing, W., Wang, H., Zheng, B., Zhang, F., Zhu, G., Feng, Y., et al. (2015). Caldicellulosiruptor changbaiensis sp. nov., a cellulolytic and hydrogen-producing bacterium from a hot spring. Int. J. Syst. Evol. Microbiol. 65, 293-297. doi: 10.1099/ijs.0.065441-0
3. Black, W. A. P., Dewar, E. T., and Woodward, F. N. (1952). Manufacture of algal chemicals. IV.-laboratory-scale isolation of fucoidin from brown marine algae. J. Sci. Food Agric. 3, 122-129. doi: 10.1002/jsfa.2740030305
4. Blumer-Schuette, S. E., Giannone, R. J., Zurawski, J. V., Ozdemir, I., Ma, Q., Yin, Y., et al. (2012). Caldicellulosiruptor core and pangenomes reveal determinants for noncellulosomal thermophilic deconstruction of plant biomass. J. Bacteriol. 194, 4015-4028. doi: 10.1128/JB.00266-12
5. Bouanane-Darenfed, A., Fardeau, M.-L., Greégoire, P., Manon, J., Kebbouche-Gana, S., Benayad, T., et al. (2011). Caldicoprobacter algeriensis sp. nov. a new thermophilic anaerobic, xylanolytic bacterium isolated from an algerian hot spring. Curr. Opin. Microbiol. 62, 826-832. doi: 10.1007/s00284-010-9789-9
6. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254. doi: 10.1016/0003-2697(76)90527-3
7. Burgess, E. A., Wagner, I. C., and Wiegel, J. (2007). 'Thermophile environments and biodiversity,' in Physiology and Biochemistry of Extremophiles, eds C. Gerday and N. Glansdorff (Washington, DC: ASM Press), 13-29. doi: 10.1128/9781555815813.ch2
8. Carere, C. R., Rydzak, T., Verbeke, T. J., Cicek, N., Levin, D. B., and Sparling, R. (2012). Linking genome content to biofuel production yields: a meta-analysis of major catabolic pathways among select H2 and ethanol-producing bacteria. BMC Microbiol. 12:295. doi: 10.1186/1471-2180-12-295
9. Chang, T., and Yao, S. (2011). Thermophilic, lignocellulolytic bacteria for ethanol production: current state and perspectives. Appl. Microbiol. Biotechnol. 92, 13-27. doi: 10.1007/s00253-011-3456-3
10. Cook, G. M., Rainey, F. A., Patel, B. K. C., and Morgan, H. W. (1996). Characterization of a new obligately anaerobic thermophile, Thermoanaerobacter wiegelii sp. nov. Int. J. Syst. Bacteriol. 46, 123-127. doi: 10.1099/00207713-46-1-123
11. Crespo, C., Pozzo, T., Karlsson, E. N., Alvarez, M. T., and Mattiasson, B. (2012). Caloramator boliviensis sp. nov., a thermophilic, ethanol-producing bacterium isolated from a hot spring. Int. J. Syst. Evol. Microbiol. 62, 1679-1686. doi: 10.1099/ijs.0.032664-0
12. Daglia, M. (2012). Polyphenols as antimicrobial agents. Curr. Opin. Biotechnol. 23, 174-181. doi: 10.1016/j.copbio.2011.08.007
13. Daroch, M., Geng, S., and Wang, G. (2013). Recent advances in liquid biofuel production from algal feedstocks. Appl. Energy 102, 1371-1381. doi: 10.1016/j.apenergy.2012.07.031
14. Enquist-Newman, M., Faust, A. M. E., Bravo, D. D., Santos, C. N. S., Raisner, R. M., Hanel, A., et al. (2014). Efficient ethanol production from brown macroalgae sugars by a synthetic yeast platform. Nature 505, 239-243. doi: 10.1038/nature12771
15. Fardeau, M., Salinas, M. B., L'Haridon, S., Jeanthon, C., Verhé, F., Cayol, J., et al. (2004). Isolation from oil reservoirs of novel thermophilic anaerobes phylogenetically related to Thermoanaerobacter subterraneus: reassignment of T. subterraneus, Thermoanaerobacter yonseiensis, Thermoanaerobacter tengcongensis and Carboxydibrachium pacificum. Int. J. Syst. Evol. Microbiol. 54, 467-474. doi: 10.1099/ijs.0.02711-0
16. Heyndrickx, M., De Vos, P., Speybrouck, A., and De Ley, J. (1989). Fermentation of mannitol by Clostridium butyricum: role of acetate as an external hydrogen acceptor. Appl. Microbiol. Biotechnol. 31, 323-328. doi: 10.1007/BF00257597
17. Horn, S. J., Aasen, I. M., and Ostgaard, K. (2000). Ethanol production from seaweed extract. J. Ind. Microbiol. Biotechnol. 25, 249-254. doi: 10.1038/sj.jim.7000065
18. Hungate, R. E. (1969). A roll tube method for cultivation of strict anaerobes, in Methods in Microbiology, eds J. R. Norris and D. W. Ribbons (New York, NY: Academic Press), 117-132
19. Indergaard, M., and Minsaas, J. (1991). 'Animal and human nutrition,' in Seaweed Resources in Europe: Uses and Potential, eds M. D. Guiry and G. Blunden (Chichester: John Wiley & Sons, Ltd.), 21-64
20. Ingvadottir, E. M., Scully, S. M., and Orlygsson, J. (2017). Evaluation of the genus of Caldicellulosiruptor for producation of 1,2-propanediol from methylpentoses. Anaerobe 47, 86-88. doi: 10.1016/j.anaerobe.2017.04.015
21. Ji, S. Q., Wang, B., Lu, M., and Li, F. L. (2016a). Biotechnology for biofuels direct bioconversion of brown algae into ethanol by thermophilic bacterium Defluviitalea phaphyphila. Biotechnol. Biofuels 9, 1-10. doi: 10.1186/s13068-016-0494-1
22. Ji, S. Q., Wang, B., Lu, M., and Li, F. L. (2016b). Defluviitalea phaphyphila sp. nov., a novel thermophilic bacterium that degrades brown algae. Appl. Environ. Microbiol. 82, 868-877. doi: 10.1128/AEM.03297-15
23. Jiang, R., Ingle, K. N., and Golberg, A. (2016). Macroalgae (seaweed) for liquid transportation biofuel production: what is next? Algal Res. 14, 48-57. doi: 10.1016/j.algal.2016.01.001
24. Kaid, N., Al-shorgani, N., Hafez, M., Isa, M., Mohtar, W., Yusoff, W., et al. (2016). Isolation of a Clostridium acetobutylicum strain and characterization of its fermentation performance on agricultural wastes. Renew. Energy 86, 459-465. doi: 10.1016/j.renene.2015.08.051
25. Kawai, S., and Murata, K. (2016). Biofuel production based on carbohydrates from both brown and red macroalgae: recent developments in key biotechnologies. Int. J. Mol. Sci. 145, 1-17. doi: 10.3390/ijms17020145
26. Kazamias, M. T., and Sperry, J. F. (1995). Enhanced fermentation of mannitol and release of cytotoxin by Clostridium difficile in alkaline culture media. Appl. Environ. Microbiol. 61, 2425-2427
27. Kim, N., Li, H., Jung, K., Nam, H., and Cheon, P. (2011). Ethanol production from marine algal hydrolysates using Escherichia coli KO11. Bioresour. Technol. 102, 7466-7469. doi: 10.1016/j.biortech.2011.04.071
28. Leschine, S. (2005). 'Degradation of polymer: cellulose, xylan, pectin, starch,' in Handbook on Clostridia, ed. P. Durre (Boca Raton, FL: CRC Press), 101-131
29. Li, P., Lee, J., Jin, H., and Keun, K. (2013). Ethanol production from Saccharina japonica using an optimized extremely low acid pretreatment followed by simultaneous saccharification and fermentation. Bioresour. Technol. 127, 119-125. doi: 10.1016/j.biortech.2012.09.122
30. Mateus, H., Regenstein, J. M., and Baker, R. C. (1977). Studies to improve the extraction of mannitol and alginic acid from Macrocystis pyrifera, a marine brown algae. Econ. Bot. 31, 24-27. doi: 10.1007/BF02860648
31. Matsumura, Y., Sato, K., Al-saari, N., Nakagawa, S., and Sawabe, T. (2014). Enhanced hydrogen production by a newly described heterotrophic marine bacterium, Vibrio tritonius strain AM2, using seaweed as the feedstock. Int. J. Hydrogen Energy 39, 7270-7277. doi: 10.1016/j.ijhydene.2014.02.164
32. Milledge, J. J., Smith, B., Dyer, P. W., and Harvey, P. (2014). Macroalgae-derived biofuel: a review of methods of energy extraction from seaweed biomass. Energies 7, 7194-7222. doi: 10.3390/en7117194
33. Miller, T. L., and Wolin, M. J. (1974). A serum bottle modification of the Hungate technique for cultivating obligate anaerobes. Appl. Microbiol. 27, 985-987
34. Muty, U. S., and Banerjee, A. K. (2012). 'Seaweeds: the wealth of oceans,' in Handbook of Marine Macroalgae: Biotechnology and Applied Phycology, ed. S.-K. Kim (Hoboken, NJ: Wiley-Blackwell), 36-44
35. Onyenwoke, R. U., Lee, Y., Dabrowski, S., Ahring, B. K., and Wiegel, J. (2006). Reclassification of Thermoanaerobium acetigenum as Caldicellulosiruptor acetigenus comb. nov. and emendation of the genus description. Int. J. Syst. Evol. Microbiol. 56, 1391-1395. doi: 10.1099/ijs.0.63723-0
36. Orlygsson, J., and Baldursson, S. R. B. (2007). Phylogenetic and physiological studies of four hydrogen-producing thermoanareobes. Icel. Agric. Sci. 20, 93-105
37. Patil, Y., Junghare, M., Pester, M., and Mu, N. (2015). Anaerobium acetethylicum gen. nov., sp. nov., a strictly anaerobic, gluconate-fermenting bacterium isolated from a methanogenic bioreactor. Int. J. Syst. Evol. Microbiol. 65, 3289-3296. doi: 10.1099/ijsem.0.000410
38. Quain, D. E., and Boulton, C. A. (1987). Growth and metabolism of mannitol by strains of Saccharomyces cerevisiae. J. Gen. Microbiol. 133, 1675-1684. doi: 10.1099/00221287-133-7-1675
39. Radulovich, R., Neori, A., Valderrama, D., Reddy, C. R. K., Cronin, H., and Forster, J. (2015). 'Farming of seaweeds,' in Seaweed Sustainability: Food and Non-Food Applications, eds B. K. Tiwori and D. J. Troy (New York, NY: Academic Press), 27-59. doi: 10.1016/B978-0-12-418697-2.00003-9
40. Ren, N., Wang, A., Cao, G., Xu, J., and Gao, L. (2009). Bioconversion of lignocellulosic biomass to hydrogen: potential and challenges. Biotechnol. Adv. 27, 1051-1060. doi: 10.1016/j.biotechadv.2009.05.007
41. Rubiano-Labrador, C., Baena, S., Díaz-Cárdenas, C., and Patel, B. K. C. (2013). Caloramator quimbayensis sp. nov., an anaerobic, moderately thermophilic bacterium isolated from a terrestrial hot spring. Int. J. Syst. Evol. Microbiol. 63, 1396-1402. doi: 10.1099/ijs.0.037937-0
42. Sanchez, J. (1998). Colorimetric assay of alditols in complex biological samples. J. Agric. Food Chem. 46, 157-160. doi: 10.1021/jf970619t
43. Sánchez, O. J., and Cardona, C. A. (2008). Trends in biotechnological production of fuel ethanol from different feedstocks. Bioresour. Technol. 99, 5270-5295. doi: 10.1016/j.biortech.2007.11.013
44. Scully, S., and Orlygsson, J. (2015). Recent advances in second generation ethanol production by thermophilic bacteria. Energies 8, 1-30. doi: 10.3390/en8010001
45. Sittijunda, S., Tomás, A. F., Reungsang, A., O-thong, S., and Angelidaki, I. (2013). Ethanol production from glucose and xylose by immobilized Thermoanaerobacter pentosaceus at 70 °C in an up-flow anaerobic sludge blanket (UASB) reactor. Bioresour. Technol. 143, 598-607. doi: 10.1016/j.biortech.2013.06.056
46. Sveinsdottir, M., Beck, S. R., and Orlygsson, J. (2009). Ethanol production from monosugars and lignocellulosic biomass by thermophilic bacteria isolated from Icelandic hot springs. Icel. Agric. Sci. 22, 45-58
47. Tanghe, A., Prior, B., and Thevelein, J. M. (2005). 'Yeast responses to stresses,' in The Yeast Handbook: Biodiversity and Ecophysiology of Yeasts, eds C. A. Rosa and G. Péter (New York, NY: Springer), 175-195
48. Taylor, M. P., Eley, K. L., Martin, S., Tuffin, M. I., Burton, S. G., and Cowan, D. A. (2009). Thermophilic ethanologenesis: future prospects for second-generation bioethanol production. Trends Biotechnol. 27, 398-405. doi: 10.1016/j.tibtech.2009.03.006
49. Tomás, A. F., Karakashev, D., and Angelidaki, I. (2013). Thermoanaerobacter pentosaceus sp. nov., an anaerobic, extreme thermophilic, high ethanol-yielding bacterium isolated from household waste. Int. J. Syst. Evol. Microbiol. 63, 2396-2404. doi: 10.1099/ijs.0.045211-0
50. Wei, N., Quarterman, J., and Jin, Y.-S. (2013). Marine macroalgae: an untapped resource for producing fuels and chemicals. Trends Biotechnol. 31, 70-77. doi: 10.1016/j.tibtech.2012.10.009
51. Xia, A., Jacob, A., Herrmann, C., Tabassum, M. R., and Murphy, J. D. (2015). Production of hydrogen, ethanol and volatile fatty acids from the seaweed carbohydrate mannitol. Bioresour. Technol. 193, 488-497. doi: 10.1016/j.biortech.2015.06.130