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Biomethane Production from Sugar Beet Pulp Under Cocultivation With Tomita et al. AMB Expr (2019) 9:28 https://doi.org/10.1186/s13568-019-0752-2 ORIGINAL ARTICLE Open Access Biomethane production from sugar beet pulp under cocultivation with Clostridium cellulovorans and methanogens Hisao Tomita1, Fumiyoshi Okazaki1,2,3 and Yutaka Tamaru1,2,3* Abstract This study was demonstrated with a coculture fermentation system using sugar beet pulp (SBP) as a carbon source combining the cellulose-degrading bacterium Clostridium cellulovorans with microbial fora of methane production (MFMP) for the direct conversion of cellulosic biomass to methane (CH4). The MFMP was taken from a commercial methane fermentation plant and extremely complicated. Therefore, the MFMP was analyzed by a next-generation sequencing system and the microbiome was identifed and classifed based on several computer programs. As a result, Methanosarcina mazei (1.34% of total counts) and the other methanogens were found in the MFMP. Interest- ingly, the simultaneous utilization of hydrogen (H2) and carbon dioxide (CO2) for methanogenesis was observed in the coculture with Consortium of C. cellulovorans with the MFMP (CCeM) including M. mazei. Furthermore, the CCeM degraded 87.3% of SBP without any pretreatment and produced 34.0 L of CH4 per 1 kg of dry weight of SBP. Thus, a gas metabolic shift in the fermentation pattern of C. cellulovorans was observed in the CCeM coculture. These results indicated that degradation of agricultural wastes was able to be carried out simultaneously with CH 4 production by C. cellulovorans and the MFMP. Keywords: Methanogenesis, Cellulosic biomass degradation, Coculture, Gas metabolism Introduction Cellulose is comprised of a linear chain of d-glucose Although frst-generation biofuels are made from cones monomers and has strong crystalline (Brethauer and and sugarcanes to mainly produce bioethanol by using Studer 2015). Moreover, cellulosic biomass is composed yeast, they are crops and foods without doubt that led of cellulose, hemicellulose and lignin, and has rigid and accordingly to the food problem. For certain reasons, complex structures (Gray et al. 2006). Hemicellulose is second-generation biofuels are produced from non-edi- heteropolymer such as xylan, glucuronoxylan, arabinoxy- ble biomass such as agricultural wastes and cellulosic lan, glucomannan, and xyloglucan. In addition, lignin, substrates (Naik et al. 2010; Schenk et al. 2008). Further- phenol compounds, are assembled with cellulose and more, the investigation of third-generation biofuels made hemicellulose. Tus, since rigid and complex structures from algae has been started (Alam et al. 2015). Tus, con- are constructed in cellulosic biomass, it is very difcult to sidering competition with food supply in response to an degrade them enzymatically. increase in global population, it is desirable to overcome About 20% of the world’s sugars is supplied by a root frst-generation biofuels, proceeding to next-generation of a sugar beet (Beta vulgaris L.), which are cultivated biofuels. all over the world mostly in Europe, North America and Russia (FAO—agribusiness handbook 2013). Sugar beet pulp is a by-product of the production of sugar from the sugar beet. Te extraction of sugar starts with the clean- *Correspondence: [email protected] ing of the sugar beet delivered to the factory, after which 1 Department of Life Sciences, Graduate School of Bioresources, Mie University, 1577 Kurimamachiya, Tsu, Mie 514-8507, Japan the sugar beet is sliced up into small strips (pulp) and Full list of author information is available at the end of the article then mashed by heating with water to a temperature of © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Tomita et al. AMB Expr (2019) 9:28 Page 2 of 10 approximately 70 °C to dissolve sugars from the pulp. Methane fermentation is conventional-generation Furthermore, the sugar water and the pulp are separated biofuels, and many researches have been reported in a in an extraction tower. Tus, since sugar beet pulp (SBP) wide range of study felds (Guo et al. 2015). Since meth- is the residue and non-edible biomass, it was the sub- ane production is carried out by the complex microbial ject of research into a raw material of second-generation fora included methanogens, it was formerly difcult to biofuels (Bellido et al. 2015; Zheng et al. 2013). Further- grasp the whole of the microbial fora. However, it has more, SBP is mainly composed of cellulose, arabinan now become possible to analyze the whole aspect of and pectin, has less lignin. Terefore, SBP is a suitable the microbiome characteristics using the next-genera- raw material for second-generation biofuels, because a tion sequencing system (Spang et al. 2017). It has been pretreatment process is not necessary to remove lignin reported on coculturing with C. cellulovorans and one of (Table 1). the famous methanogens such Methanosarcina spp. (Lu Some species of Clostridia are known to have ability et al. 2017). Since C. cellulovorans and methanogens were to degrade cellulosic biomass efciently using a multi- able to grow anaerobically under mesophilic condition, it enzyme complex called the cellulosome and secreted was possible to cultivate both of them in a single tank and non-cellulosomal enzymes (Doi and Kosugi 2004). simultaneously with both the degradation of cellulosic Among those species, we have been studying on Clostrid- biomass and production of methane (CH4). ium cellulovorans, which is a mesophilic and anaerobic In the present study, we investigated a process for pro- cellulolytic bacterium (Sleat et al. 1984). C. cellulovorans ducing CH4 and hydrogen (H 2) via the coculture of C. cel- utilizes not only cellulose but also hemicelluloses consist- lulovorans with microbial fora of methane production ing of xylose, fructose, galactose, and mannose (Koukie- (MFMP) that called the Consortium of C. cellulovorans kolo et al. 2005; Beukes et al. 2008; Dredge et al. 2011). with MFMP (CCeM) with carbon sources such as SBP Whole-genome sequencing of C. cellulovorans and the and Avicel. First, we analyzed 16 s rRNA sequences in exoproteome profles revealed 57 cellulosomal protein- the MFMP by using a next-generation sequencer. Based encoding genes and 168 secreted-carbohydrase-encoding on the result of identifcation of the MFMP microbiome, genes (Tamaru et al. 2010; Matsui et al. 2013). Further- both C. cellulovorans and the MFMP monocultures and more, since high ability of degradation on plant cell walls the CCeM coculture were carried out to evaluate concen- has so far been reported (Tamaru et al. 2002), researches trations of sugars, organic acids, and biogas (H2 and CH4) have continued to study on degradation mechanism for yield after cultivation. cellulosic biomass such as rice straw by C. cellulovorans (Nakajima et al. 2017). Materials and methods Materials SBP was obtained from a sugar factory in Hokkaido, Table 1 Component of sugar beet pulp Japan. It was dried up, milled and sieved through 80 mesh. Te substrate concentration of SBP and Avicel Component Weigh (g) per dry matter (100 g) (Sigma, MO, USA) was 0.5% (w/v) of dry weight. Hadden et al. (1986) Zheng et al. (2013) Microorganism and culture condition Ash 3.42 g/100 g 2.51 g/100 g Te medium was partially modifed by Clostridium Proteins 11.42 g/100 g 11.42 g/100 g cellulovorans medium (Sleat et al. 1984). One litter Lipids 1.63 g/100 g – medium containing 4 g of yeast extract, 1 mg of Resa- Sugarsa 5.2 g/100 g – zurin salt, 1 g of l-cysteine-HCl, 5 g of NaHCO 3, 0.45 g Starch 0.99 g/100 g – of K2HPO4, 0.45 g of KH2PO4, 0.3675 g of NH4Cl, 0.9 g Lignin 2.38 g/100 g 1.16 g/100 g of NaCl, 0.1575 g of MgCl2∙6H2O, 0.12 g of CaCl2∙2H2O, Glucan 17.34 g/100 gb 22.7 g/100 g 0.85 mg of MnCl2∙4H2O, 0.942 mg of CoCl 2∙6H2O, 5.2 mg Xylan 1.36 g/100 gb 5.14 g/100 g of Na2EDTA, 1.5 mg of FeCl2∙4H2O, 0.07 mg of ZnCl2, Galactan 4.88 g/100 gb 5.92 g/100 g 0.1 mg H3BO3, 0.017 mg of CuCl2∙2H2O, 0.024 mg of Arabinan 16.83 g/100 gb 23.73 g/100g NiCl2∙6H2O, 0.036 mg of Na2MoO4∙2H2O, 6.6 mg of Mannan 1.58 g/100gb 1.85 g/100g FeSO4∙7H2O, and 0.1 g of p-aminobenzoic acid and was b Pectin 21.15 g/100g 22.84 g/100g adjusted to pH7. C. cellulovorans 743B (ATCC 35296) Others – 2.73 g/100g was used and anaerobically cultivated in 0.5% (w/v) cel- a Total value of rest of fructose, glucose, sucrose and fructan lobiose (Sigma, MO, USA) at 37 °C for 19 h stationary. b Conversion of values to polysaccharides in the paper Te MFMP was obtained from methane fermentation Tomita et al. AMB Expr (2019) 9:28 Page 3 of 10 digested liquid on January, 2017 at Gifu in Japan. Te ATP concentration correlates with cell growth (Miyake MFMP was anaerobically cultivated in Clostridium cel- et al. 2016). Cell growth was estimated by measuring ATP lulovorans medium with 0.5% (w/v) glucose (Wako) and concentration of 0.1 mL of cell culture according to the 0.25% (w/v) cellobiose at 37 °C for 19 h stationary.
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