Review Open Access

Thermoanaerobacter Species: The Promising Candidates for Lignocellulosic Biofuel Production

Synthetic Biology and Engineering. 2023, 1(1), 10005; https://doi.org/10.35534/sbe.2023.10005
Kaiqun Dai 1    Chunyun Qu 2,3    Hongxin Fu 1    Jufang Wang 1,4 *   
1
School of Biology and Biological Engineering, South China University of Technology, Guangzhou 510006, China
2
College of Light Industry and Food Science, Guangdong Provincial Key Laboratory of Science and Technology of Lingnan Special Food Science and Technology, Zhongkai University of Agriculture and Engineering, Guangzhou 510225, China
3
Key Laboratory of Green Processing and Intelligent Manufacturing of Lingnan Specialty Food, Ministry of Agriculture, Guangzhou 510225, China
4
Guangdong Provincial Key Laboratory of Fermentation and Enzyme Engineering, South China University of Technology, Guangzhou 510006, China
*
Authors to whom correspondence should be addressed.

Received: 31 Jan 2023    Accepted: 09 Mar 2023    Published: 15 Mar 2023   

Abstract

Thermoanaerobacter species, which have broad substrate range and high operating temperature, can directly utilize lignocellulosic materials for biofuels production. Compared with the mesophilic process, thermophilic process shows greater prospects in consolidated bioprocessing (CBP) due to its relatively higher efficiency of lignocellulose degradation and lower risk of microbial contamination. Additionally, thermophilic conditions can reduce cooling costs, and further facilitate downstream product recovery. This review comprehensively summarizes the advances of Thermoanaerobacter species in lignocellulosic biorefinery, including their performance on substrates utilization, and genetic modification or other strategies for enhanced biofuels production. Furthermore, bottlenecks of sugar co-fermentation, metabolic engineering, and bioprocessing are also discussed.

References

1.
El-Dalatony MM, Saha S, Govindwar SP, Abou-Shanab RAI, Jeon BH. Biological Conversion of Amino Acids to Higher Alcohols. Trends Biotechnol. 2019, 37, 855–869. [Google Scholar]
2.
Riaz S, Mazhar S, Abidi SH, Syed Q, Abbas N, Saleem Y, et al. Biobutanol production from sustainable biomass process of anaerobic ABE fermentation for industrial applications. Arch. Microbiol. 2022, 204, 672. [Google Scholar]
3.
Busic A, Mardetko N, Kundas S, Morzak G, Belskaya H, Ivancic Santek M, et al. Bioethanol Production from Renewable Raw Materials and Its Separation and Purification: A Review. Food Technol. Biotechnol. 2018, 56, 289–311. [Google Scholar]
4.
Broda M, Yelle DJ, Serwańska K. Bioethanol Production from Lignocellulosic Biomass-Challenges and Solutions. Molecules 2022, 27, 8717. [Google Scholar]
5.
Abo BO, Gao M, Wang Y, Wu C, Ma H, Wang Q. Lignocellulosic biomass for bioethanol: An overview on pretreatment, hydrolysis and fermentation processes. Rev. Environ. Health 2019, 34, 57–68. [Google Scholar]
6.
Guo Y, Liu Y, Guan M, Tang H, Wang Z, Lin L, et al. Production of butanol from lignocellulosic biomass: recent advances, challenges, and prospects. RSC Adv. 2022, 12, 18848–18863. [Google Scholar]
7.
Kaparaju P, Serrano M, Thomsen AB, Kongjan P, Angelidaki I. Bioethanol, biohydrogen and biogas production from wheat straw in a biorefinery concept. Bioresour. Technol. 2009, 100, 2562–2568. [Google Scholar]
8.
Kim JS, Park SC, Kim JW, Park JC, Park SM, Lee JS. Production of bioethanol from lignocellulose: Status and perspectives in Korea. Bioresour. Technol. 2010, 101, 4801–4805. [Google Scholar]
9.
Awasthi MK, Sarsaiya S, Patel A, Juneja A, Singh RP, Yan B, et al. Refining biomass residues for sustainable energy and bio-products: An assessment of technology, its importance, and strategic applications in circular bio-economy. Renew. Sustain. Energy Rev. 2020, 127, 109876. [Google Scholar]
10.
Parascanu MM, Sanchez N, Sandoval-Salas F, Carreto CM, Soreanu G, Sanchez-Silva L. Environmental and economic analysis of bioethanol production from sugarcane molasses and agave juice. Environ. Sci. Pollut. Res. Int. 2021, 28, 64374–64393. [Google Scholar]
11.
Aparicio E, Rodríguez-Jasso RM, Pinales-Márquez CD, Loredo-Treviño A, Robledo-Olivo A, Aguilar CN, et al. High-pressure technology for Sargassum spp biomass pretreatment and fractionation in the third generation of bioethanol production. Bioresour. Technol. 2021, 329, 124935. [Google Scholar]
12.
Kim SR, Ha SJ, Wei N, Oh EJ, Jin YS. Simultaneous co-fermentation of mixed sugars: a promising strategy for producing cellulosic ethanol. Trends Biotechnol. 2012, 30, 274–282. [Google Scholar]
13.
Kazemi Shariat Panahi H, Dehhaghi M, Dehhaghi S, Guillemin GJ, Shiung Lam S, Aghbashlo M, et al. Engineered bacteria for valorizing lignocellulosic biomass into bioethanol. Bioresour. Technol. 2021, 344, 126212. [Google Scholar]
14.
Liu Y, Cruz-Morales P, Zargar A, Belcher MS, Pang B, Englund E, et al. Biofuels for a sustainable future. Cell 2021, 184, 1636–1647. [Google Scholar]
15.
Dietrich K, Dumont MJ, Del Rio LF, Orsat V. Sustainable PHA production in integrated lignocellulose biorefineries. New Biotechnol. 2019, 49, 161–168. [Google Scholar]
16.
Zhang C, Wen H, Chen C, Cai D, Fu C, Li P, et al. Simultaneous saccharification and juice co-fermentation for high-titer ethanol production using sweet sorghum stalk. Renew. Energy 2019, 134, 44–53. [Google Scholar]
17.
Parisutham V, Chandran SP, Mukhopadhyay A, Lee SK, Keasling JD. Intracellular cellobiose metabolism and its applications in lignocellulose-based biorefineries. Bioresour. Technol. 2017, 239, 496–506. [Google Scholar]
18.
Zhao T, Tashiro Y, Zheng J, Sakai K, Sonomoto K. Semi-hydrolysis with low enzyme loading leads to highly effective butanol fermentation. Bioresour. Technol. 2018, 264, 335–342. [Google Scholar]
19.
Gorke B, Stulke J. Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat. Rev. Microbiol. 2018, 6, 613–624. [Google Scholar]
20.
Qu CY, Zhang Y, Dai KQ, Fu HX, Wang JF. Metabolic engineering of Thermoanaerobacterium aotearoense SCUT27 for glucose and cellobiose co-utilization by identification and overexpression of the endogenous cellobiose operon. Biochem. Eng. J. 2021, 167, 107922. [Google Scholar]
21.
Rahayu F, Kawai Y, Iwasaki Y, Yoshida K, Kita A, Tajima T, et al. Thermophilic ethanol fermentation from lignocellulose hydrolysate by genetically engineered Moorella thermoacetica Bioresour. Technol. 2017, 245, 1393–1399. [Google Scholar]
22.
Zhu M, Lu Y, Wang J, Li S, Wang X. Carbon Catabolite Repression and the Related Genes of ccpA, ptsH and hprK in Thermoanaerobacterium aotearoense. PloS ONE 2015, 10, e0142121. [Google Scholar]
23.
Lin L, Song H, Tu Q, Qin Y, Zhou A, Liu W, et al. The Thermoanaerobacter glycobiome reveals mechanisms of pentose and hexose co-utilization in bacteria.  PLoS Genet. 2011, 7, e1002318. [Google Scholar]
24.
Currie DH, Raman B, Gowen CM, Tschaplinski TJ, Land ML, Brown SD, et al. Genome-scale resources for Thermoanaerobacterium saccharolyticum. BMC Syst. Biol. 2015, 9, 30. [Google Scholar]
25.
Zhou J, Ouyang J, Xu Q, Zheng Z. Cost-effective simultaneous saccharification and fermentation of l-lactic acid from bagasse sulfite pulp by Bacillus coagulans CC17.  Bioresour. Technol. 2016, 222, 431–438. [Google Scholar]
26.
Taylor MP, Eley KL, Martin S, Tuffin MI, Burton SG, Cowan DA. Thermophilic ethanologenesis: Future prospects for second-generation bioethanol production. Trends Biotechnol. 2009, 27, 398–405. [Google Scholar]
27.
Rydzak T, Garcia D, Stevenson DM, Sladek M, Klingeman DM, Holwerda EK, et al. Deletion of Type I glutamine synthetase deregulates nitrogen metabolism and increases ethanol production in Clostridium thermocellum. Metab. Eng. 2017,, 41, 182–191. [Google Scholar]
28.
Holwerda EK, Olson DG, Ruppertsberger NM, Stevenson DM, Murphy SJL, Maloney MI, et al. Metabolic and evolutionary responses of Clostridium thermocellum to genetic interventions aimed at improving ethanol production. Biotechnol. Biofuels 2020, 13, 40. [Google Scholar]
29.
Mazzoli R, Olson DG, Lynd LR. Construction of lactic acid overproducing Clostridium thermocellum through enhancement of lactate dehydrogenase expression. Enzyme Microb. Technol. 2020, 141, 109645. [Google Scholar]
30.
Jiang Y, Lu J, Lv Y, Wu R, Dong W, Zhou J, et al. Efficient hydrogen production from lignocellulosic feedstocks by a newly isolated thermophlic Thermoanaerobacterium sp. strain F6. Int. J. Hydrog. Energy 2019, 44, 14380–14386. [Google Scholar]
31.
O-Thong S, Prasertsan P, Karakashev D, Angelidaki I. Thermophilic fermentative hydrogen production by the newly isolated Thermoanaerobacterium thermosaccharolyticum PSU-2. Int. J. Hydrog. Energy 2008, 33, 1204–1214. [Google Scholar]
32.
Deutschmann R, Dekker RF. From plant biomass to bio-based chemicals: latest developments in xylan research. Biotechnol. Adv. 2012, 30, 1627–1640. [Google Scholar]
33.
Hemme CL, Fields MW, He Q, Deng Y, Lin L, Tu Q, et al. Correlation of genomic and physiological traits of thermoanaerobacter species with biofuel yields. Appl. Environ Microbiol. 2011, 77, 7998–8008. [Google Scholar]
34.
Shaw AJ, Podkaminer KK, Desai SG, Bardsley JS, Rogers SR, Thorne PG, et al. Metabolic engineering of a thermophilic bacterium to produce ethanol at high yield.  Proc. Natl. Acad. Sci. USA 2008, 105, 13769–13774. [Google Scholar]
35.
Ai H, Zhang J, Yang M, Yu P, Li S, Zhu M, et al. Draft Genome Sequence of an Anaerobic, Thermophilic Bacterium, Thermoanaerobacterium aotearoense SCUT27, Isolated from a Hot Spring in China. Genome Announc. 2014, 2, e00041-14. [Google Scholar]
36.
Huang X, Li Z, Du C, Wang J, Li S. Improved Expression and Characterization of a Multidomain Xylanase from Thermoanaerobacterium aotearoense SCUT27 in Bacillus subtilis.  J. Agric. Food Chem. 2015, 63, 6430–6439. [Google Scholar]
37.
Xu T, Huang X, Li Z, Lin CS, Li S. Enhanced Purification Efficiency and Thermal Tolerance of Thermoanaerobacterium aotearoense β-Xylosidase through Aggregation Triggered by Short Peptides. J. Agric. Food Chem. 2018, 66, 4182–4188. [Google Scholar]
38.
Currie DH, Guss AM, Herring CD, Giannone RJ, Johnson CM, Lankford PK, et al. Profile of secreted hydrolases, associated proteins, and SlpA in Thermoanaerobacterium saccharolyticum during the degradation of hemicellulose. Appl. Environ. Microbiol. 2014, 80, 5001–5011. [Google Scholar]
39.
Tsakraklides V, Shaw AJ, Miller BB, Hogsett DA, Herring CD. Carbon catabolite repression in Thermoanaerobacterium saccharolyticum. Biotechnol. Biofuels 2012, 5, 85. [Google Scholar]
40.
Deutscher J, Francke C, Postma PW. How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol. Mol. Biol. Rev. 2016, 70, 939–1031. [Google Scholar]
41.
Deutscher J, Ake FM, Derkaoui M, Zebre AC, Cao TN, Bouraoui H, et al. The bacterial phosphoenolpyruvate:carbohydrate phosphotransferase system: regulation by protein phosphorylation and phosphorylation-dependent protein-protein interactions. Microbiol. Mol. Biol. Rev. 2014, 78, 231–256. [Google Scholar]
42.
Galinier A, Deutscher J. Sophisticated Regulation of Transcriptional Factors by the Bacterial Phosphoenolpyruvate: Sugar Phosphotransferase System. J. Mol. Biol. 2017, 429, 773–789. [Google Scholar]
43.
Nie X, Yang B, Zhang L, Gu Y, Yang S, Jiang W, et al. PTS regulation domain-containing transcriptional activator CelR and sigma factor σ54 control cellobiose utilization in Clostridium acetobutylicum. Mol. Microbiol. 2016, 100, 289–302. [Google Scholar]
44.
Qu C, Chen L, Fu H, Wang J. Engineering Thermoanaerobacterium aotearoense SCUT27 with argR knockout for enhanced ethanol production from lignocellulosic hydrolysates. Bioresour. Technol. 2020, 310, 123435. [Google Scholar]
45.
Li T, Zhang C, Yang KL, He J.  Unique genetic cassettes in a Thermoanaerobacterium contribute to simultaneous conversion of cellulose and monosugars into butanol.  Sci. Adv. 2018, 4, e1701475. [Google Scholar]
46.
Lin HY, Chuang HH, Lin FP. Biochemical characterization of engineered amylopullulanase from Thermoanaerobacter ethanolicus 39E-implicating the non-necessity of its 100 C-terminal amino acid residues. Extremophiles 2008, 12, 641–650. [Google Scholar]
47.
Vieille C, Zeikus GJ. Hyperthermophilic enzymes: Sources, uses, and molecular mechanisms for thermostability. Microbiol. Mol. Biol. Rev. 2001, 65, 1–43. [Google Scholar]
48.
Hon S, Tian L, Zheng T, Cui J, Lynd LR, Olson DG. Methods for Metabolic Engineering of Thermoanaerobacterium saccharolyticum. Methods Mol. Biol. 2020, 2096, 21–43. [Google Scholar]
49.
Herring CD, Kenealy WR, Joe Shaw A, Covalla SF, Olson DG, Zhang J, et al. Strain and bioprocess improvement of a thermophilic anaerobe for the production of ethanol from wood. Biotechnol. Biofuels 2016, 9, 125. [Google Scholar]
50.
Singhania RR, Patel AK, Sukumaran RK, Larroche C, Pandey A. Role and significance of beta-glucosidases in the hydrolysis of cellulose for bioethanol production. Bioresour. Technol. 2013, 127, 500–507. [Google Scholar]
51.
Vinuselvi P, Lee SK. Engineering Escherichia coli for efficient cellobiose utilization. Appl. Microbiol. Biotechnol. 2011, 92, 125–132. [Google Scholar]
52.
Parisutham V, Kim TH, Lee SK. Feasibilities of consolidated bioprocessing microbes: From pretreatment to biofuel production. Bioresour. Technol. 2014, 161, 431–440. [Google Scholar]
53.
Kim IJ, Bornscheuer UT, Nam KH. Biochemical and Structural Analysis of a Glucose-Tolerant β-Glucosidase from the Hemicellulose-Degrading Thermoanaerobacterium saccharolyticum. Molecules 2022, 27, 290. [Google Scholar]
54.
Herring CD, Kenealy WR, Shaw AJ, Raman B, Tschaplinski TJ, Brown SD, et al. Final Report on Development of Thermoanaerobacterium saccharolyticum for the Conversion of Lignocellulose to Ethanol; U.S. Department of Energy OSTI: Oak Ridge, TN, USA, 2012; Technical Report.
55.
Zhu M, Zhang L, Yang F, Cha Y, Li S, Zhuo M, Huang S, Li J. A Recombinant β-Mannanase from Thermoanaerobacterium aotearoense SCUT27: Biochemical Characterization and Its Thermostability Improvement. J. Agric. Food Chem. 2020, 68, 818–825. [Google Scholar]
56.
Jacobson TB, Korosh TK, Stevenson DM, Foster C, Maranas C, Olson DG, Lynd LR, Amador-Noguez D. In Vivo Thermodynamic Analysis of Glycolysis in Clostridium thermocellum and Thermoanaerobacterium saccharolyticum Using (13)C and (2)H Tracers. mSystems 2022, 5, e00736-19. [Google Scholar]
57.
Lopez G, Canas-Duarte SJ, Pinzon-Velasco AM, Vega-Vela NE, Rodriguez M, Restrepo S, Baena S. Description of a new anaerobic thermophilic bacterium, Thermoanaerobacterium butyriciformans sp. nov. Syst. Appl. Microbiol. 2017, 40, 86–91. [Google Scholar]
58.
Hu BB, Zhu MJ. Direct hydrogen production from dilute-acid pretreated sugarcane bagasse hydrolysate using the newly isolated Thermoanaerobacterium thermosaccharolyticum MJ1.  Microb. Cell Factories 2017, 16, 77. [Google Scholar]
59.
Yao S, Mikkelsen MJ. Metabolic engineering to improve ethanol production in hermoanaerobacter mathranii.  Appl. Microbiol. Biotechnol. 2010, 88, 199–208. [Google Scholar]
60.
Katsyv A, Jain S, Basen M, Muller V. Electron carriers involved in autotrophic and heterotrophic acetogenesis in the thermophilic bacterium Thermoanaerobacter kivui. Extremophiles 2021, 25, 513–526. [Google Scholar]
61.
Weghoff MC, Muller V. CO Metabolism in the Thermophilic Acetogen Thermoanaerobacter kivui Appl. Environ. Microbiol. 2016, 82, 2312–2319. [Google Scholar]
62.
Shaw AJ, Hogsett DA, Lynd LR. Natural competence in Thermoanaerobacter and Thermoanaerobacterium species. Appl. Environ. Microbiol. 2010, 76, 4713–4719. [Google Scholar]
63.
Mai V, Lorenz WW, Wiegel J. Transformation of Thermoanaerobacterium sp. strain JW/SL-YS485 with plasmid pIKM1 conferring kanamycin resistance. FEMS Microbiol. Lett. 1997, 148, 163–167. [Google Scholar]
64.
Peng H, Fu B, Mao Z, Shao W. Electrotransformation of Thermoanaerobacter ethanolicus JW200. Biotechnol. Lett. 2006, 28, 1913–1917. [Google Scholar]
65.
Groom J, Chung D, Olson DG, Lynd LR, Guss AM, Westpheling J. Promiscuous plasmid replication in thermophiles: Use of a novel hyperthermophilic replicon for genetic manipulation of Clostridium thermocellum at its optimum growth temperature. Metab. Eng. Commun. 2016, 3, 30–38. [Google Scholar]
66.
Le Y, Fu Y, Sun J. Genome Editing of the Anaerobic Thermophile Thermoanaerobacter ethanolicus Using Thermostable Cas9. Appl. Environ Microbiol. 2020, 87, e01773-20. [Google Scholar]
67.
Shaw AJ, Covalla SF, Miller BB, Firliet BT, Hogsett DA, Herring CD. Urease expression in a Thermoanaerobacterium saccharolyticum ethanologen allows high titer ethanol production. Metab. Eng. 2012, 14, 528–532. [Google Scholar]
68.
Li Y, Hu J, Qu C, Chen L, Guo X, Fu H, et al. Engineered Thermoanaerobacterium aotearoense with nfnAB knockout for improved hydrogen production from lignocellulose hydrolysates. Biotechnol. Biofuels 2019, 12, 214. [Google Scholar]
69.
Li S, Lai C, Cai Y, Yang X, Yang S, Zhu M, et al. High efficiency hydrogen production from glucose/xylose by the ldh-deleted Thermoanaerobacterium strain. Bioresour. Technol. 2010, 101, 8718–8724. [Google Scholar]
70.
Shaw AJ, Covalla SF, Hogsett DA, Herring CD. Marker removal system for Thermoanaerobacterium saccharolyticum and development of a markerless ethanologen. Appl. Environ. Microbiol. 2011, 77, 2534–2536. [Google Scholar]
71.
Basen M, Geiger I, Henke L, Müller V, Elliot MA. A Genetic System for the Thermophilic Acetogenic Bacterium Thermoanaerobacter kivui. Appl. Environ Microbiol. 2018, 84, e02210-17. [Google Scholar]
72.
Zheng T, Olson DG, Murphy SJ, Shao X, Tian L, Lynd LR. Both adhE and a Separate NADPH-Dependent Alcohol Dehydrogenase Gene, adhA, Are Necessary for High Ethanol Production in Thermoanaerobacterium saccharolyticum. J. Bacteriol. 2017, 199, e00542-16. [Google Scholar]
73.
Shao X, Zhou J, Olson DG, Lynd LR. A markerless gene deletion and integration system for Thermoanaerobacter ethanolicus. Biotechnol. Biofuels 2016, 9, 100. [Google Scholar]
74.
Mougiakos I, Mohanraju P, Bosma EF, Vrouwe V, Finger Bou M, Naduthodi MIS, et al.  Characterizing a thermostable Cas9 for bacterial genome editing and silencing.  Nat. Commun. 2017, 8, 1647. [Google Scholar]
75.
Song Y, He S, Jopkiewicz A, Setroikromo R, van Merkerk R, Quax WJ. Development and application of CRISPR-based genetic tools in Bacillus species and Bacillus phages. J. Appl. Microbiol. 2022, 133, 2280–2298. [Google Scholar]
76.
Dai K, Fu H, Guo X, Qu C, Lan Y, Wang J. Exploiting the Type I-B CRISPR Genome Editing System in Thermoanaerobacterium aotearoense SCUT27 and Engineering the Strain for Enhanced Ethanol Production. Appl. Environ Microbiol. 2022, 88, e0075122. [Google Scholar]
77.
Zhou X, Wang X, Luo H, Wang Y, Wang Y, Tu T, et al. Exploiting heterologous and endogenous CRISPR-Cas systems for genome editing in the probiotic Clostridium butyricum Biotechnol. Bioeng. 2021, 118, 2448–2459. [Google Scholar]
78.
Walker JE, Lanahan AA, Zheng T, Toruno C, Lynd LR, Cameron JC, et al. Development of both type I-B and type II CRISPR/Cas genome editing systems in the cellulolytic bacterium Clostridium thermocellum. Metab. Eng. Commun. 2020, 10, e00116. [Google Scholar]
79.
Bruder MR, Pyne ME, Moo-Young M, Chung DA, Chou CP. Extending CRISPR-Cas9 Technology from Genome Editing to Transcriptional Engineering in the Genus Clostridium Appl. Environ Microbiol. 2016, 82, 6109–6119. [Google Scholar]
80.
Li Q, Chen J, Minton NP, Zhang Y, Wen Z, Liu J, et al. CRISPR-based genome editing and expression control systems in Clostridium acetobutylicum and Clostridium beijerinckii Biotechnol. J. 2016, 11, 961–972. [Google Scholar]
81.
Woolston BM, Emerson DF, Currie DH, Stephanopoulos G. Rediverting carbon flux in Clostridium ljungdahlii using CRISPR interference (CRISPRi). Metab. Eng. 2018, 48, 243–253. [Google Scholar]
82.
Shen A. A Xylose-Inducible Expression System and a CRISPR Interference Plasmid for Targeted Knockdown of Gene Expression in Clostridioides difficile. J. Bacteriol. 2019, 201, e00711-18. [Google Scholar]
83.
Ganguly J, Martin-Pascual M, van Kranenburg R. CRISPR interference (CRISPRi) as transcriptional repression tool for Hungateiclostridium thermocellum DSM 1313. Microb. Biotechnol. 2020, 13, 339–349. [Google Scholar]
84.
Maier LK, Stachler AE, Brendel J, Stoll B, Fischer S, Haas KA, et al. The nuts and bolts of the Haloferax CRISPR-Cas system I-B. RNA Biol. 2019, 16, 469–480. [Google Scholar]
85.
Pickar-Oliver A, Black JB, Lewis MM, Mutchnick KJ, Klann TS, Gilcrest KA, et al. Targeted transcriptional modulation with type I CRISPR-Cas systems in human cells. Nat. Biotechnol. 2019, 37, 1493–1501. [Google Scholar]
86.
Young JK, Gasior SL, Jones S, Wang L, Navarro P, Vickroy B, et al. The repurposing of type I-E CRISPR-Cascade for gene activation in plants. Commun. Biol. 2019, 2, 383. [Google Scholar]
87.
Beri D, York WS, Lynd LR, Pena MJ, Herring CD. Development of a thermophilic coculture for corn fiber conversion to ethanol. Nat. Commun. 2020, 11, 1937. [Google Scholar]
88.
Zhang J, Hu L, Zhang H, He ZG. Cyclic di-GMP triggers the hypoxic adaptation of Mycobacterium bovis through a metabolic switching regulator ArgR. Environ. Microbiol. 2022, 24, 4382–4400. [Google Scholar]
89.
Charlier D, Bervoets I. Regulation of arginine biosynthesis, catabolism and transport in Escherichia coli. Amino Acids 2019, 51, 1103–1127. [Google Scholar]
90.
Qu C, Chen L, Li Y, Fu H, Wang J. The redox-sensing transcriptional repressor Rex is important for regulating the products distribution in Thermoanaerobacterium aotearoense SCUT27. Appl. Microbiol. Biotechnol. 2020, 104, 5605–5617. [Google Scholar]
91.
Jiang Y, Liu J, Dong W, Zhang W, Fang Y, Ma J, et al. The Draft Genome Sequence of Thermophilic Thermoanaerobacterium thermosaccharolyticum M5 Capable of Directly Producing Butanol from Hemicellulose. Curr. Microbiol. 2018, 75, 620–623. [Google Scholar]
92.
Yang X, Zhu M, Huang X, Lin CS, Wang J, Li S. Valorisation of mixed bakery waste in non-sterilized fermentation for L-lactic acid production by an evolved Thermoanaerobacterium sp. strain. Bioresour. Technol. 2015, 198, 47–54. [Google Scholar]
93.
Iodice P, Senatore A, Langella G, Amoresano A. Advantages of ethanol-gasoline blends as fuel substitute for last generation Si engines. Environ. Progress Sustain. Energy 2017, 36, 1173–1179. [Google Scholar]
94.
Toor M, Kumar SS, Malyan SK, Bishnoi NR, Mathimani T, Rajendran K, Pugazhendhi A. An overview on bioethanol production from lignocellulosic feedstocks. Chemosphere 2020, 242, 125080. [Google Scholar]
95.
Jacobus Ana P, Gross J, Evans John H, Ceccato-Antonini Sandra R, Gombert Andreas K. Saccharomyces cerevisiae strains used industrially for bioethanol production. Essays Biochem. 2021, 65, 147–161. [Google Scholar]
96.
Zhang L, Tang Y, Guo ZP, Ding ZY, Shi GY. Improving the ethanol yield by reducing glycerol formation using cofactor regulation in Saccharomyces cerevisiae. Biotechnol. Lett. 2011, 33, 1375–1380. [Google Scholar]
97.
Yan X, Wang X, Yang Y, Wang Z, Zhang H, Li Y, et al. Cysteine supplementation enhanced inhibitor tolerance of Zymomonas mobilis for economic lignocellulosic bioethanol production.  Bioresour. Technol. 2022, 349, 126878. [Google Scholar]
98.
Todhanakasem T, Wu B, Simeon S. World J. Perspectives and new directions for bioprocess optimization using Zymomonas mobilis in the ethanol production. Microbiol. Biotechnol. 2020, 36, 112. [Google Scholar]
99.
Koppolu V, Vasigala VK. Role of Escherichia coli in Biofuel Production. Microbiol. Insights 2016, 9, 29–35. [Google Scholar]
100.
Cai Y, Lai C, Li S, Liang Z, Zhu M, Liang S, et al. Disruption of lactate dehydrogenase through homologous recombination to improve bioethanol production in Thermoanaerobacterium aotearoense. Enzyme Microb. Technol. 2011, 48, 155–161. [Google Scholar]
101.
Fu HX, Luo S, Dai KQ, Qu CY, Wang JF. Engineering Thermoanaerobacterium aotearoense SCUT27/Delta ldh with pyruvate formate lyase-activating protein (PflA) knockout for enhanced ethanol tolerance and production. Process Biochem. 2021, 106, 184–190. [Google Scholar]
102.
Olson DG, Sparling R, Lynd LR. Ethanol production by engineered thermophiles. Curr. Opin. Biotechnol. 2015, 33, 130–141. [Google Scholar]
103.
Cui J, Olson DG, Lynd LR. Characterization of the Clostridium thermocellum AdhE, NfnAB, ferredoxin and Pfor proteins for their ability to support high titer ethanol production in Thermoanaerobacterium saccharolyticum. Metab. Eng. 2019, 51, 32–42. [Google Scholar]
104.
Hitschler L, Kuntz M, Langschied F, Basen M. Thermoanaerobacter species differ in their potential to reduce organic acids to their corresponding alcohols. Appl. Microbiol. Biotechnol. 2018, 102, 8465–8476. [Google Scholar]
105.
Scully SM, Orlygsson J. Biotransformation of Carboxylic Acids to Alcohols: Characterization of Thermoanaerobacter Strain AK152 and 1-Propanol Production via Propionate Reduction. Microorganisms 2020, 8, 945. [Google Scholar]
106.
Borchers A, Pieler T. Programming pluripotent precursor cells derived from Xenopus embryos to generate specific tissues and organs.  Genes 2010, 1, 413–426. [Google Scholar]
107.
Lo J, Zheng T, Hon S, Olson DG, Lynd LR. The bifunctional alcohol and aldehyde dehydrogenase gene, adhE, is necessary for ethanol production in Clostridium thermocellum and Thermoanaerobacterium saccharolyticum. J. Bacteriol. 2015, 197, 1386–1393. [Google Scholar]
108.
Zheng T, Olson DG, Tian L, Bomble YJ, Himmel ME, Lo J, et al. Cofactor Specificity of the Bifunctional Alcohol and Aldehyde Dehydrogenase (AdhE) in Wild-Type and Mutant Clostridium thermocellum and Thermoanaerobacterium saccharolyticum. J. Bacteriol. 2015, 197, 2610–2619. [Google Scholar]
109.
Desai SG, Guerinot ML, Lynd LR. Cloning of L-lactate dehydrogenase and elimination of lactic acid production via gene knockout in Thermoanaerobacterium saccharolyticum JW/SL-YS485. Appl. Microbiol. Biotechnol. 2004, 65, 600–605. [Google Scholar]
110.
Shaw AJ, Hogsett DA, Lynd LR. Identification of the [FeFe]-hydrogenase responsible for hydrogen generation in Thermoanaerobacterium saccharolyticum and demonstration of increased ethanol yield via hydrogenase knockout. J. Bacteriol. 2009, 191, 6457–6464. [Google Scholar]
111.
Eminoğlu A, Murphy SJ-L, Maloney M, Lanahan A, Giannone RJ, Hettich RL, et al. Deletion of the hfsB gene increases ethanol production in Thermoanaerobacterium saccharolyticum and several other thermophilic anaerobic bacteria.  Biotechnol. Biofuels 2017, 10, 282. [Google Scholar]
112.
Fu H, Yang X, Qu C, Li Y, Wang J. Enhanced ethanol production from lignocellulosic hydrolysates by inhibiting the hydrogen synthesis in Thermoanaerobacterium aotearoense SCUT27(Δldh). J. Chem. Technol. Biotechnol. 2019, 94, 3305–3314. [Google Scholar]
113.
Tian L, Lo J, Shao X, Zheng T, Olson DG, Lynd LR. Ferredoxin:NAD+ Oxidoreductase of Thermoanaerobacterium saccharolyticum and Its Role in Ethanol Formation. Appl. Environ Microbiol. 2016, 82, 7134–7141. [Google Scholar]
114.
Lo J, Zheng T, Olson DG, Ruppertsberger N, Tripathi SA, Tian L, et al. Deletion of nfnAB in Thermoanaerobacterium saccharolyticum and Its Effect on Metabolism. J. Bacteriol. 2015, 197, 2920–2929. [Google Scholar]
115.
Beri D, Olson DG, Holwerda EK, Lynd LR. Nicotinamide cofactor ratios in engineered strains of Clostridium thermocellum and Thermoanaerobacterium saccharolyticum FEMS Microbiol. Lett. 2016, 363, fnw091. [Google Scholar]
116.
Lovitt RW, Shen GJ, Zeikus JG. Ethanol production by thermophilic bacteria: Biochemical basis for ethanol and hydrogen tolerance in Clostridium thermohydrosulfuricum J. Bacteriol. 1988, 170, 2809–2815. [Google Scholar]
117.
Shaw AJ, Miller BB, Rogers SR, Kenealy WR, Meola A, Bhandiwad A, et al. Anaerobic detoxification of acetic acid in a thermophilic ethanologen. Biotechnol. Biofuels 2015, 8, 75. [Google Scholar]
118.
Yanase H, Miyawaki H, Sakurai M, Kawakami A, Matsumoto M, Haga K, et al. Ethanol production from wood hydrolysate using genetically engineered Zymomonas mobilis. Appl. Microbiol. Biotechnol. 2012, 94, 1667–1678. [Google Scholar]
119.
Haque S, Singh R, Pal DB, Faidah H, Ashgar SS, Areeshi MY, et al. Thermophilic biohydrogen production strategy using agro industrial wastes: Current update, challenges, and sustainable solutions. Chemosphere 2022, 307, 136120. [Google Scholar]
120.
Ubando AT, Chen WH, Hurt DA, Conversion A, Rajendran S, Lin SL. Biohydrogen in a circular bioeconomy: A critical review.  Bioresour. Technol. 2022, 366, 128168. [Google Scholar]
121.
Soboh B, Linder D, Hedderich R. A multisubunit membrane-bound [NiFe] hydrogenase and an NADH-dependent Fe-only hydrogenase in the fermenting bacterium Thermoanaerobacter tengcongensis. Microbiology 2004, 150, 2451–2463. [Google Scholar]
122.
Carere CR, Rydzak T, Verbeke TJ, Cicek N, Levin DB, Sparling R. Linking genome content to biofuel production yields: a meta-analysis of major catabolic pathways among select H2 and ethanol-producing bacteria. BMC Microbiol. 2012, 12, 295. [Google Scholar]
123.
Li P, Zhu M. A consolidated bio-processing of ethanol from cassava pulp accompanied by hydrogen production. Bioresour. Technol. 2011, 102, 10471–10479. [Google Scholar]
124.
Cheng J, Zhu M. A novel anaerobic co-culture system for bio-hydrogen production from sugarcane bagasse. Bioresour. Technol. 2013, 144, 623–631. [Google Scholar]
125.
Jiang Y, Guo D, Lu J, Dürre P, Dong W, Yan W, et al. Consolidated bioprocessing of butanol production from xylan by a thermophilic and butanologenic Thermoanaerobacterium sp. M5. Biotechnol. Biofuels 2018, 11, 89. [Google Scholar]
126.
Bhandiwad A, Shaw AJ, Guss A, Guseva A, Bahl H, Lynd LR. Metabolic engineering of Thermoanaerobacterium saccharolyticum for n-butanol production. Metab. Eng. 2014, 21, 17–25. [Google Scholar]
127.
Liu Y, Yu P, Song X, Qu Y. Hydrogen production from cellulose by co-culture of Clostridium thermocellum JN4 and Thermoanaerobacterium thermosaccharolyticum GD17.  Int. J. Hydrog. Energy 2008, 33, 2927–2933. [Google Scholar]
128.
Kremer F, Blank LM, Jones PR, Akhtar MK. A Comparison of the Microbial Production and Combustion Characteristics of Three Alcohol Biofuels: Ethanol, 1-Butanol, and 1-Octanol. Front. Bioeng. Biotechnol. 2015, 3, 122. [Google Scholar]
129.
Jiang Y, Lv Y, Wu R, Lu J, Dong W, Zhou J, et al. Consolidated bioprocessing performance of a two-species microbial consortium for butanol production from lignocellulosic biomass. Biotechnol. Bioeng. 2020, 117, 2985–2995. [Google Scholar]
130.
Morvan C, Folgosa F, Kint N, Teixeira M, Martin-Verstraete I. Responses of Clostridia to oxygen: From detoxification to adaptive strategies. Environ. Microbiol. 2021, 23, 4112–4125. [Google Scholar]
131.
Qu C, Dai K, Fu H, Wang J. Enhanced ethanol production from lignocellulosic hydrolysates by Thermoanaerobacterium aotearoense SCUT27/ΔargR1864 with improved lignocellulose-derived inhibitors tolerance.  Renew. Energy 2021, 173, 652–661. [Google Scholar]
132.
Lynd LR, Baskaran S, Casten S. Salt accumulation resulting from base added for pH control, and not ethanol, limits growth of Thermoanaerobacterium thermosaccharolyticum HG-8 at elevated feed xylose concentrations in continuous culture. Biotechnol. Progress 2001, 17, 118–125. [Google Scholar]
133.
Atalah J, Caceres-Moreno P, Espina G, Blamey JM. Thermophiles and the applications of their enzymes as new biocatalysts. Bioresour. Technol. 2019, 280, 478–488. [Google Scholar]
134.
Wang F, Wang M, Zhao Q, Niu K, Liu S, He D, et al. Exploring the Relationship between Clostridium thermocellum JN4 and Thermoanaerobacterium thermosaccharolyticum GD17. Front. Microbiol. 2019, 10, 2035. [Google Scholar]
135.
Cheng J, Yu Y, Zhu M. Enhanced biodegradation of sugarcane bagasse by Clostridium thermocellum with surfactant addition. Green Chem. 2014, 16, 2689–2695. [Google Scholar]
136.
Lynd LR, Guss AM, Himmel ME, Beri D, Herring C, Holwerda EK, et al. Advances in Consolidated Bioprocessing Using Clostridium thermocellum and Thermoanaerobacter saccharolyticum. In Industrial Biotechnology; Wiley-VCH: Weinheim, Germany, 2017; pp. 365–394
Creative Commons

© 2024 by the authors; licensee SCIEPublish, SCISCAN co. Ltd. This article is an open access article distributed under the CC BY license (https://creativecommons.org/licenses/by/4.0/).