Light-driven CO2 utilization for chemical production in bacterium biohybrids

doi:10.1016/S1872-2067(23)64643-1

Abstract

Abstract:

Artificial photosynthetic systems provide an alternative approach for the sustainable, efficient, and versatile production of biofuels and biochemicals. However, improving the efficiency of electron transfer between semiconductor materials and microbial cells remains a challenge. In this study, an inorganic-biological photosynthetic biohybrid system (IBPHS) consisting of photocatalytic and biocatalytic modules was developed by integrating cadmium telluride quantum dots (CdTe QDs) with Escherichia coli cells. A photocatalytic module was constructed by biosynthesizing CdTe QDs to capture light and generate electrons. The biocatalytic module was built by converting photo-induced electrons to enhance NADH regeneration; thus, the NADH content in E. coli under blue light increased by 5.1-fold compared to that in darkness. Finally, IBPHS was utilized to drive CO₂ reduction pathways for versatile bioproduction such as formate and pyruvate, with CO₂ utilization rates up to 51.98 and 21.92 mg/gDCW/h, respectively, exceeding that of cyanobacteria. This study offers a promising platform for the rational design of biohybrids for efficient biomanufacturing processes with high complexity and functionality.

Key words: Artificial photosynthetic system, CO₂ utilization, Solar energy conversion, CdTe biosynthesis, NADH regeneration

Yamei Gan, Tiantian Chai, Jian Zhang, Cong Gao, Wei Song, Jing Wu, Liming Liu, Xiulai Chen. Light-driven CO₂ utilization for chemical production in bacterium biohybrids[J]. Chinese Journal of Catalysis, 2024, 60: 294-303.

×
share this article

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.cjcatal.com/EN/10.1016/S1872-2067(23)64643-1

https://www.cjcatal.com/EN/Y2024/V60/I5/294

Figures/Tables 5

Fig. 1. Designing inorganic-biological photosynthetic biohybrid system (IBPHS) for CO2 utilization. IBPHS consisted of the photocatalytic and biocatalytic modules. The photocatalytic module was constructed by biosynthesizing CdTe QDs to capture light and then generate electrons. The biocatalytic module was built by converting photo-induced electrons to enhance NADH regeneration. IBPHS was utilized to drive CO2 reduction pathways for versatile bioproduction such as formate and pyruvate. VB: valence band; CB: conduction band; e?: electron; CO2: carbon dioxide; HWLS: half-Wood-Ljungdahl-formolase.

Fig. 2. Constructing inorganic-biological photosynthetic biohybrid system (IBPHS). (a) ICP-MS showing the absorption of Cd2+ ions. (b?d) CLSM image showing the biosynthesis of CdTe nanoparticles in E. coli JZ. (e) Cross-section TEM image showing the localization of CdTe nanoparticles in E. coli cells. The black dots represent CdTe nanoparticles. HAADF-STEM images (f?i) and EDS mapping (j) of CdTe nanoparticles. (k) XPS analysis of CdTe nanoparticles. (l) HETEM image and lattice fringes of CdTe nanoparticles.

Fig. 3. Evaluating inorganic-biological photosynthetic biohybrid system (IBPHS). (a) UV-vis diffuse reflectance spectra of E. coli strains. (b) Bandgap width of CdTe QDs. (c) Transient photocurrent of IBPHS. (d) Electrochemical impedance spectroscopy of IBPHS. (e,f) Intracellular NADH contents of IBPHS. (g,h) Evaluation of the regenerated NADH for bioproduction in vivo and in vitro, respectively.

Fig. 4. Converting CO2 to formate by the inorganic-biological photosynthetic biohybrid system (IBPHS). (a) Photocatalytic reduction of CO2 for formate production in vitro. (b) Photocatalytic reduction of CO2 for formate production in vivo. (c) Optimizing FDH expression by coupling the ribosome-binding site with plasmids. (d) Formate production by optimizing FDH expression.

Fig. 5. Converting CO2 to pyruvate by the inorganic-biological photosynthetic biohybrid system (IBPHS). (a) Photocatalytic reduction of CO2 for pyruvate production in vivo. (b) Engineered E. coli strains for pyruvate production. (c) Pyruvate production with E. coli FH under light and dark conditions. (d) CO2-fixing rate of E. coli FH under light and dark conditions. pyk: pyruvate kinase; Fhs: formyl-tetrahydrofolate cyclohydrolase; FchA: methylene-THF dehydrogenase; FolD: methylene-THF reductase; FLS: formolase; DHAK: dihydroxyacetone kinase.

References

[1]	Q. Wang, C. Pornrungroj, S. Linley, E. Reisner, Nat. Energy, 2022, 7, 13-24.
[2]	X. G. Zhu, S. P. Long, D. R. Ort, Curr. Opin. Biotechnol., 2008, 19, 153-159.
[3]	N. Kornienko, J. Z. Zhang, K. K. Sakimoto, P. Yang, E. Reisner, Nat. Nanotechnol., 2018, 13, 890-899.
[4]	S. Kim, S. N. Lindner, S. Aslan, O. Yishai, S. Wenk, K. Schann, A. Bar-Even, Nat. Chem. Biol., 2020, 16, 538-545.
[5]	R. E. Blankenship, D. M. Tiede, J. Barber, G. W. Brudvig, G. Fleming, M. Ghirardi, M. R. Gunner, W. Junge, D. M. Kramer, A. Melis, T. A. Moore, C. C. Moser, D. G. Nocera, A. J. Nozik, D. R. Ort, W. W. Parson, R. C. Prince, R. T. Sayre, Science, 2011, 332, 805-809.
[6]	T. Tong, X. Chen, G. Hu, X. L. Wang, G. Q. Liu, L. M. Liu, Biotechnol. Adv., 2021, 53, 107841.
[7]	R. J. Spreitzer, M. E. Salvucci, Annu. Rev. Plant. Biol., 2002, 53, 449-475.
[8]	K. Izui, H. Matsumura, T. Furumoto, Y. Kai, Annu. Rev. Plant. Biol., 2004, 55, 69-84.
[9]	I. Sanchez-Andrea, I. A. Guedes, B. Hornung, S. Boeren, C. E. Lawson, D. Z. Sousa, A. Bar-Even, N. J. Claassens, A. J. M. Stams, Nat. Commun., 2020, 11, 5090.
[10]	T. Schwander, L. S. V. Borzyskowski, S. Burgener, N. S. Cortina, T. J. Erb, Science, 2016, 354, 900-904.
[11]	S. E. Payer, K. Faber, S. M. Glueck, Adv. Synth. Catal., 2019, 361, 2402-2420.
[12]	G. A. Aleku, G. W. Roberts, G. R. Titchiner, D. Leys, ChemSusChem, 2021, 14, 1781-1804.
[13]	A. Saaret, A. Balaikaite, D. Leys, Enzymes, 2020, 47, 517-549.
[14]	M. Calvin, A. A. Benso, Science, 1948, 107, 476-480.
[15]	L. Steffens, E. Pettinato, T. M. Steiner, A. Mall, S. König, W. Eisenreich, I. A. Berg, Nature, 2021, 592, 784-788.
[16]	S. W. Ragsdale, E. Pierce, Biochim. Biophys. Acta, 2008, 1784, 1873-1898.
[17]	M. Scheffen, D. G. Marchal, T. Beneyton, S. K. Schuller, M. Klose, C. Diehl, J. Lehmann, P. Pfister, M. Carrillo, H. He, S. Aslan, N. S. Cortina, P. Claus, D. Bollschweiler, J.-C. Baret, J. M. Schuller, J. Zarzycki, A. Bar-Even, T. J. Erb, Nat. Catal., 2021, 4, 105-115.
[18]	T. Cai, H. B. Sun, J. Qiao, L. L. Zhu, F. Zhang, Z. J, Z. J. Tang, X. L. Wei, J. G. Yang, Q. Q. Yuan, W. Y. Wang, X. Yang, H. Y. Chu, C. Y. Q. Wang, H. W. Ma, Y. X. Sun, Y. Li, C. Li, H. F. Jiang, Q. H. Wang, Y. H. Ma, Science, 2021, 373, 1523-1527.
[19]	L. Xiao, G. Liu, F. Gong, H. Zhu, Y. Zhang, Z. Cai, Y. Li, ACS Catal., 2021, 12, 799-808.
[20]	K. K. Sakimoto, P. D. Yang, Science, 2016, 351, 74-77.
[21]	X. Y. Wang, K. Li, B. An, Y. Y. Wang, C. Zhong, Sci. Adv., 2022, 8, eabm7665.
[22]	X. Guan, S. Erşan, X. Hu, T. L. Atallah, Y. Xie, S. Lu, B. Cao, J. Sun, K. Wu, Y. Huang, X. Duan, J. R. Caram, Y. Yu, J. O. Park, C. Liu, Nat. Catal., 2022, 5, 1019-1029.
[23]	G. Liang, X. Xu, X. Chen, J. Wu, W. Song, W. Wei, J. Liu, X. Li, L. M. Liu, C. Gao, Chem. Eng. J., 2023, 477, 147152.
[24]	B. Luo, Y. Z. Wang, D. Li, H. Shen, L. X. Xu, Z. Fang, Z. Xia, J. Ren, W. Shi, Y. C. Yong, Adv. Energy Mater., 2021, 11, 2100256.
[25]	C. L. Zhao, X. Li, L. Guo, C. Gao, W. Song, W. Wei, J. Wu, L. M. Liu, X. L. Chen, Adv. Sci., 2023, 2307351.
[26]	Y. Li, P. Zhang, B. B. Chen, Z. Q. Tian, L. Li, B. Hu, D. W. Pang, Z. X. Xie, ACS Nano, 2013, 7, 2240-2248.
[27]	S. Theiner, K. Loehr, G. Koellensperger, L. Mueller, N. Jakubowski, J. Anal. Atomic Spectr., 2020, 35, 1784-1813.
[28]	B. Wang, Z. Jiang, J. C. Yu, J. Wang, P. K. Wong, Nanoscale, 2019, 11, 9296-9301.
[29]	L. J. Tian, W. W. Li, T. T. Zhu, J. J. Chen, W. K. Wang, P. F. An, L. Zhang, J. C. Dong, Y. Guan, D. F. Liu, N. Q. Zhou, G. Liu, Y. C. Tian, H. Q. Yu, J. Am. Chem. Soc., 2017, 139, 12149-12152.
[30]	L. Guo, W. Diao, C. Gao, G. P. Hu, Q. Ding, C. Ye, X. L. Chen, J. Liu, L. M. Liu, Nat. Catal., 2020, 3, 307-318.
[31]	R. J. Turner, J. H. Weiner, D. E. Taylor, BioMetals, 1998, 11, 223-227.
[32]	J. H. Jia, L. L. Yang, A. A. Liu, D. W. Pang, Synth. Biology J., 2022, 3, 385-398.
[33]	L. H. Xiong, R. Cui, Z. L. Zhang, X. Yu, Z. X. Xie, Y. B. Shi, D. W. Pang, ACS Nano, 2022, 8, 5116-5124.
[34]	Y. D. Zhou, Y. J. Li, X. S. Wu, G. S. Xu, J. X. Fang, D. Y. Tang, Infrared Technol., 2001, 23, 8-10.
[35]	X. H. An, R. P. Li, L. Tian, Z. G. He, R. Wu, Z. X. Li, Chinese Rare Earths, 2012, 33, 27-31.
[36]	G. P. Hu, Z. Li, D. Ma, C. Ye, L. Zhang, C. Gao, L. M. Liu, X. L. Chen, Nat. Catal., 2021, 4, 395-406.
[37]	B. Wang, C. Zeng, K. H. Chu, D. Wu, H. Y. Yip, L. Ye, P. K. Wong, Adv. Energy Mater., 2017, 7, 1700611.
[38]	W. Wei, P. Q. Sun, Z. Li, K. S. Song, W. Y. Su, B. Wang, Y. Z. Liu, J. Zhao, Sci. Adv, 2018, 4, eaap9253.
[39]	Y. L. Lin, J. Y. Shi, W. Feng, J. P. Yue, Y. Q. Luo, S. Chen, B. Yang, Y. W. Jiang, H. C. Hu, C. K. Zhou, F. Y. Shi, A. Prominski, D. V. Talapin, W. Xiong, X. Gao, B. Z. Tian, Sci. Adv., 2023, 9, eadg5858.
[40]	J. Ye, J. Yu, Y. Zhang, M. Chen, X. Liu, S. Zhou, Z. He, Appl. Catal. B, 2019, 257, 117916.
[41]	P. Gai, W. Yu, H. Zhao, R. Qi, F. Li, L. Liu, F. Lv, S. Wang, Angew. Chem. Int. Ed., 2020, 59, 7224-7229.
[42]	X. Zhou, Y. Zeng, Y. Tang, Y. Huang, F. Lv, L. Liu, S. Wang, Sci. Adv., 2020, 6, eabc5237.
[43]	E. M. Nichols, J. J. Gallagher, C. Liu, Y. Su, J. Resasco, Y. Yu, Y. Sun, P. Yang, M. C. Y. Chang, C. J. Chang, Proc. Natl. Acad. Sci. U. S. A., 2015, 112, 11461-11466.
[44]	C. Liu, J. J. Gallagher, K. K. Sakimoto, E. M. Nichols, C. J. Chang, M. C. Y. Chang, P. D. Yang, Nano Lett., 2015, 15, 3634-3639.
[45]	J. P. Torella, C. J. Gagliardi, J. S. Chen, D. K. Bediako, B. Colón, J. C. Way, P. A. Silver, D. G. Nocera, Proc. Natl. Acad. Sci. U. S. A., 2015, 112, 2337-2342.
[46]	C. Liu, B. C. Colón, M. Ziesack, P. A. Silver, D. G. Nocera, Science, 2016, 352, 1210-1213.
[47]	Q. Hu, H. Hu, L. Cui, Z. Li, D. Svedruzic, J. L. Blackburn, M. C. Beard, J. Ni, W. Xiong, X. Gao, X. Chen, ACS Energy Lett., 2022, 8, 677-684.
[48]	Q. Wang, S. Kalathil, C. Pornrungroj, C. D. Sahm, E. Reisner, Nat. Catal., 2022, 5, 633-641.
[49]	J. Kim, S. C. Blanco, Y. X. Shen, R. Cai, P. D.Yang, Nano Lett., 2022, 22, 5503-5509.
[50]	S. Pi, W. Yang, W. Feng, R. Yang, W. Chao, W. Cheng, L. Cui, Z. Li, Y. Lin, N. Ren, C. Yang, L. Lu, X. Gao, Nat. Sustain., 2023, 6, 1673-1684.
[51]	F. Gao, G. Liu, A. Chen, Y. Hu, H. Wang, J. Pan, J. Feng, H. Zhang, Y. Wang, Y. Min, C. Gao, Y. Xiong, Nat. Commun., 2023, 14, 6783.
[52]	K. Liang, J. J. Richardson, J. Cui, F. Caruso, C. J. Doonan, and P. Falcaro, Adv. Mater., 2016, 28, 7910-7914.
[53]	S. C. Blanco, H. Zhang, P. D. Yang, Faraday Discu., 2019, 215, 54-65.
[54]	Y. Ding, J. R. Bertram, C. Eckert, R. R. Bommareddy, R. Patel, A. Conradie, S. Bryan, P. Nagpal, J. Am. Chem. Soc., 2019, 141, 10272-10282.

Light-driven CO₂ utilization for chemical production in bacterium biohybrids

RichHTML

PDF (PC)

Knowledge

Supporting Information

Abstract

Cite this article

share this article

share this article

Figures/Tables 5

References

Related Articles 7

Recommended Articles

Metrics

[1]	Jiali Liu, Huicong Dai, Xin Liu, Yiqi Ren, Maodi Wang, Qihua Yang. Pickering emulsion stabilized with charge separation and transfer modulated photocatalyst for enzyme-photo-coupled catalysis [J]. Chinese Journal of Catalysis, 2024, 57(2): 114-122.
[2]	Changcheng Wei, Wenna Zhang, Kuo Yang, Xiu Bai, Shutao Xu, Jinzhe Li, Zhongmin Liu. An efficient way to use CO₂ as chemical feedstock by coupling with alkanes [J]. Chinese Journal of Catalysis, 2023, 47(4): 138-149.
[3]	Pengye Zhang, Wenjin Dong, Yuanyuan Zhang, Li-Nan Zhao, Hualei Yuan, Chuanjun Wang, Wenshuo Wang, Hanxiao Wang, Hongyu Zhang, Jian Liu. Metalated carbon nitride with facilitated electron transfer pathway for selective NADH regeneration and photoenzyme-coupled CO₂ reduction [J]. Chinese Journal of Catalysis, 2023, 54(11): 188-198.
[4]	Huayang Zhang, Wenjie Tian, Xiaoguang Duan, Hongqi Sun, Yingping Huang, Yanfen Fang, Shaobin Wang. Single-atom catalysts on metal-based supports for solar photoreduction catalysis [J]. Chinese Journal of Catalysis, 2022, 43(9): 2301-2315.
[5]	Teera Chantarojsiri, Tassaneewan Soisuwan, Pornwimon Kongkiatkrai. Toward green syntheses of carboxylates: Considerations of mechanisms and reactions at the electrodes for electrocarboxylation of organohalides and alkenes [J]. Chinese Journal of Catalysis, 2022, 43(12): 3046-3061.
[6]	Sixue Lin, Jing Wang, Yangyang Mi, Senyou Yang, Zheng Wang, Wenming Liu, Daishe Wu, Honggen Peng. Trifunctional strategy for the design and synthesis of a Ni-CeO₂@SiO₂ catalyst with remarkable low-temperature sintering and coking resistance for methane dry reforming [J]. Chinese Journal of Catalysis, 2021, 42(10): 1808-1820.
[7]	Ruqun Guan, Xiaoming Zhang, Fangfang Chang, Nan Xue, Hengquan Yang. Incorporation of flexible ionic polymers into a Lewis acid-functionalized mesoporous silica for cooperative conversion of CO₂ to cyclic carbonates [J]. Chinese Journal of Catalysis, 2019, 40(12): 1874-1883.