Long-Term Autotrophic Growth and Solar-to-Chemical Conversion in Shewanella Oneidensis MR-1 through Light-Driven Electron Transfer
Yan Shi
School of Metallurgy and Environment, Central South University, Changsha, 410083 China
Chinese National Engineering Research Centre for Control & Treatment of Heavy Metal Pollution, Changsha, 410083 China
These authors contributed equally to this work.
Search for more papers by this authorKejing Zhang
School of Metallurgy and Environment, Central South University, Changsha, 410083 China
These authors contributed equally to this work.
Search for more papers by this authorJianxin Chen
School of Metallurgy and Environment, Central South University, Changsha, 410083 China
Search for more papers by this authorBingtian Zhang
School of Environmental Science and Engineering, Southern University of Science and Technology, Shenzhen, 518055 China
Search for more papers by this authorXun Guan
Department of Chemistry and Biochemistry, University of California, Los Angeles, Los Angeles, CA 90095 USA
Search for more papers by this authorXin Wang
Department of Microbiology and Cell Science, University of Florida, Gainesville, FL
Department of Microbiology, Miami University, Oxford, OH 45056 USA
Search for more papers by this authorTong Zhang
College of Environmental Science and Engineering, Ministry of Education Key Laboratory of Pollution Processes and Environmental Criteria, Tianjin Key Laboratory of Environmental Remediation and Pollution Control, Nankai University, Tianjin, 300350 China
Search for more papers by this authorHan Song
School of Environment and Energy, Guangdong Provincial Key Laboratory of Solid Wastes Pollution Control and Recycling, South China University of Technology, Guangzhou, Guangdong, 510006 China
Search for more papers by this authorLong Zou
School of Metallurgy and Environment, Central South University, Changsha, 410083 China
Search for more papers by this authorXiangfeng Duan
Department of Chemistry and Biochemistry, University of California, Los Angeles, Los Angeles, CA 90095 USA
California NanoSystems Institute, University of California, Los Angeles, Los Angeles, CA 90095 USA
Search for more papers by this authorHaichun Gao
Institute of Microbiology and College of Life Sciences, Zhejiang University, Zhejiang, Hangzhou, 310058 China
Search for more papers by this authorCorresponding Author
Zhang Lin
School of Metallurgy and Environment, Central South University, Changsha, 410083 China
Chinese National Engineering Research Centre for Control & Treatment of Heavy Metal Pollution, Changsha, 410083 China
Search for more papers by this authorYan Shi
School of Metallurgy and Environment, Central South University, Changsha, 410083 China
Chinese National Engineering Research Centre for Control & Treatment of Heavy Metal Pollution, Changsha, 410083 China
These authors contributed equally to this work.
Search for more papers by this authorKejing Zhang
School of Metallurgy and Environment, Central South University, Changsha, 410083 China
These authors contributed equally to this work.
Search for more papers by this authorJianxin Chen
School of Metallurgy and Environment, Central South University, Changsha, 410083 China
Search for more papers by this authorBingtian Zhang
School of Environmental Science and Engineering, Southern University of Science and Technology, Shenzhen, 518055 China
Search for more papers by this authorXun Guan
Department of Chemistry and Biochemistry, University of California, Los Angeles, Los Angeles, CA 90095 USA
Search for more papers by this authorXin Wang
Department of Microbiology and Cell Science, University of Florida, Gainesville, FL
Department of Microbiology, Miami University, Oxford, OH 45056 USA
Search for more papers by this authorTong Zhang
College of Environmental Science and Engineering, Ministry of Education Key Laboratory of Pollution Processes and Environmental Criteria, Tianjin Key Laboratory of Environmental Remediation and Pollution Control, Nankai University, Tianjin, 300350 China
Search for more papers by this authorHan Song
School of Environment and Energy, Guangdong Provincial Key Laboratory of Solid Wastes Pollution Control and Recycling, South China University of Technology, Guangzhou, Guangdong, 510006 China
Search for more papers by this authorLong Zou
School of Metallurgy and Environment, Central South University, Changsha, 410083 China
Search for more papers by this authorXiangfeng Duan
Department of Chemistry and Biochemistry, University of California, Los Angeles, Los Angeles, CA 90095 USA
California NanoSystems Institute, University of California, Los Angeles, Los Angeles, CA 90095 USA
Search for more papers by this authorHaichun Gao
Institute of Microbiology and College of Life Sciences, Zhejiang University, Zhejiang, Hangzhou, 310058 China
Search for more papers by this authorCorresponding Author
Zhang Lin
School of Metallurgy and Environment, Central South University, Changsha, 410083 China
Chinese National Engineering Research Centre for Control & Treatment of Heavy Metal Pollution, Changsha, 410083 China
Search for more papers by this authorGraphical Abstract
Shewanella oneidensis MR-1 achieved months-long autotrophic growth and acetate production through CO2 fixation coupled to sulfur oxidation, driven by biogenic CdS nanoparticles under light.
Abstract
Members of the genus Shewanella are known for their versatile electron accepting routes, which allow them to couple decomposition of organic matter to reduction of various terminal electron acceptors for heterotrophic growth in diverse environments. Here, we report autotrophic growth of Shewanella oneidensis MR-1 with photoelectrons provided by illuminated biogenic CdS nanoparticles. This hybrid system enables photosynthetic oscillatory acetate production from CO2 for over five months, far exceeding other inorganic-biological hybrid system that can only sustain for hours or days. Biochemical, electrochemical and transcriptomic analyses reveal that the efficient electron uptake of S. oneidensis MR-1 from illuminated CdS nanoparticles supplies sufficient energy to stimulate the previously overlooked reductive glycine pathway for CO2 fixation. The continuous solar-to-chemical conversion is achieved by photon induced electric recycling in sulfur species. Overall, our findings demonstrate that this mineral-assisted photosynthesis, as a widely existing and unique model of light energy conversion, could support the sustained photoautotrophic growth of non-photosynthetic microorganisms in nutrient-lean environments and mediate the reversal of coupled carbon and sulfur cycling, consequently resulting in previously unknown environmental effects. In addition, the hybrid system provides a sustainable and flexible platform to develop a variety of solar products for carbon neutrality.
Conflict of Interests
The authors declare no conflict of interest.
Open Research
Data Availability Statement
The data that support the findings of this study are available in the supplementary material of this article.
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References
- 1J. K. Fredrickson, M. F. Romine, A. S. Beliaev, J. M. Auchtung, M. E. Driscoll, T. S. Gardner, K. H. Nealson, A. L. Osterman, G. Pinchuk, J. L. Reed, D. A. Rodionov, J. L. M. Rodrigues, D. A. Saffarini, M. H. Serres, A. M. Spormann, I. B. Zhulin, J. M. Tiedje, Nat. Rev. Microbiol. 2008, 6, 592–603.
- 2H. H. Hau, J. A. Gralnick, Annu. Rev. Microbiol. 2007, 61, 237–258.
- 3
- 3aX. Fang, S. Kalathil, E. Reisner, Chem. Soc. Rev. 2020, 49, 4926–4952;
- 3bN. J. Claassens, D. Z. Sousa, V. A. P. M. dos Santos, W. M. de Vos, J. van der Oost, Nat. Rev. Microbiol. 2016, 14, 692–706;
- 3cH. Chen, O. Simoska, K. Lim, M. Grattieri, M. Yuan, F. Dong, Y. S. Lee, K. Beaver, S. Weliwatte, E. M. Gaffney, S. D. Minteer, Chem. Rev. 2020, 120, 12903–12993;
- 3dD. R. Lovley, D. E. Holmes, Nat. Rev. Microbiol. 2022, 20, 5–19;
- 3eK. Rabaey, R. A. Rozendal, Nat. Rev. Microbiol. 2010, 8, 706–716.
- 4
- 4aI. 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;
- 4bI. A. Figueroa, T. P. Barnum, P. Y. Somasekhar, C. I. Carlstrom, A. L. Engelbrektson, J. D. Coates, Proc. Natl. Acad. Sci. USA 2018, 115, 92–101.
- 5
- 5aO. Yishai, M. Bouzon, V. Doering, A. Bar-Even, ACS Synth. Biol. 2018, 7, 2023–2028;
- 5bS. T. de Vries, S. Yilmaz, A. Bar-Even, N. J. Claassens, G. Bordanaba-Florit, C. A. R. Cotton, A. De Maria, M. Finger-Bou, L. Friedeheim, N. Giner-Laguarda, M. Munar-Palmer, W. Newell, G. Scarinci, J. Verbunt, Metab. Eng. 2020, 62, 30–41;
- 5cJ. G. de la Cruz, F. Machens, K. Messerschmidt, A. Bar-Even, ACS Synth. Biol. 2019, 8, 911–917.
- 6
- 6aC. Liu, J. J. Gallagher, K. K. Sakimoto, E. M. Nichols, C. J. Chang, M. C. Y. Chang, P. Yang, Nano Lett. 2015, 15, 3634–3639;
- 6bK. K. Sakimoto, A. B. Wong, P. Yang, Science 2016, 351, 74–77.
- 7M. Martins, C. Toste, I. A. C. Pereira, Angew. Chem. Int. Ed. 2021, 60, 9055–9062.
- 8
- 8aP. Gai, W. Yu, H. Zhao, R. Qi, F. Li, L. Liu, F. Lv, S. Wang, Angew. Chem. Int. Ed. 2020, 59, 7224–7229;
- 8bH. Zhang, H. Liu, Z. Tian, D. Lu, Y. Yu, S. Cestellos-Blanco, K. K. Sakimoto, P. Yang, Nat. Nanotechnol. 2018, 13, 900–905.
- 9B. Wang, Z. Jiang, J. C. Yu, J. Wang, P. K. Wong, Nanoscale 2019, 11, 9296–9301.
- 10
- 10aY. A. Gorby, S. Yanina, J. S. McLean, K. M. Rosso, D. Moyles, A. Dohnalkova, T. J. Beveridge, I. S. Chang, B. H. Kim, K. S. Kim, D. E. Culley, S. B. Reed, M. F. Romine, D. A. Saffarini, E. A. Hill, L. Shi, D. A. Elias, D. W. Kennedy, G. Pinchuk, K. Watanabe, S. i. Ishii, B. Logan, K. H. Nealson, J. K. Fredrickson, Proc. Natl. Acad. Sci. USA 2006, 103, 11358–11363;
- 10bP. Subramanian, S. Pirbadian, M. Y. El-Naggar, G. J. Jensen, Proc. Natl. Acad. Sci. USA 2018, 115, E3246–E3255.
- 11G. F. White, Z. Shi, L. Shi, Z. Wang, A. C. Dohnalkova, M. J. Marshall, J. K. Fredrickson, J. M. Zachara, J. N. Butt, D. J. Richardson, T. A. Clarke, Proc. Natl. Acad. Sci. USA 2013, 110, 6346–6351.
- 12
- 12aR. Wang, H. Li, J. Sun, L. Zhang, J. Jiao, Q. Wang, S. Liu, Adv. Mater. 2021, 33, 2004051;
- 12bX. Wu, F. Zhao, N. Rahunen, J. R. Varcoe, C. Avignone-Rossa, A. E. Thumser, R. C. T. Slade, Angew. Chem. Int. Ed. 2011, 50, 427–430;
- 12cB. Cao, Z. Zhao, L. Peng, H.-Y. Shiu, M. Ding, F. Song, X. Guan, C. K. Lee, J. Huang, D. Zhu, X. Fu, G. C. L. Wong, C. Liu, K. Nealson, P. S. Weiss, X. Duan, Y. Huang, Science 2021, 373, 1336–1340.
- 13
- 13aP. G. Heytler, Biochemistry 1963, 2, 357–361;
- 13bM. S. Guzman, K. Rengasamy, M. M. Binkley, C. Jones, T. O. Ranaivoarisoa, R. Singh, D. A. Fike, J. M. Meacham, A. Bose, Nat. Commun. 2019, 10, 1355.
- 14
- 14aD. J. Horgan, T. P. Singer, J. E. Casida, J. Biol. Chem. 1968, 243, 834–843;
- 14bG. Palmer, D. J. Horgan, H. Tisdale, T. P. Singer, H. Beinert, J. Biol. Chem. 1968, 243, 844–847.
- 15
- 15aP. Xu, J. Liu, P. Yan, C. Miao, K. Ye, K. Cheng, J. Yin, D. Cao, K. Li, G. Wang, J. Mater. Chem. A 2016, 4, 4920–4928;
- 15bI. Rathinamala, I. M. Babu, J. J. William, G. Muralidharan, N. Prithivikumaran, Mater. Sci. Semicond. Process. 2020, 105, 104677.
- 16Y. Li, Y. Li, Y. Liu, Y. Wu, J. Wu, B. Wang, H. Ye, H. Jia, X. Wang, L. Li, M. Zhu, H. Ding, Y. Lai, C. Wang, J. Dick, A. Lu, Sci. Adv. 2020, 6, eabc3687.
- 17X. V. Zhang, S. T. Martin, C. M. Friend, M. A. A. Schoonen, H. D. Holland, J. Am. Chem. Soc. 2004, 126, 11247–11253.
- 18X. Deng, N. Dohmae, K. H. Nealson, K. Hashimoto, A. Okamoto, Sci. Adv. 2018, 4, eaao5682.
- 19S. Shirodkar, S. Reed, M. Romine, D. Saffarini, Environ. Microbiol. 2011, 13, 108–115.
- 20
- 20aY. Xu, Ph.D. thesis, State University of New York at Stony Brook (United States – New York), 1997;
- 20bD. J. O′Brien, F. B. Birkner, Environ. Sci. Technol. 1977, 11, 1114–1120;
- 20cJ. F. Read, J. John, J. MacPherson, C. Schaubel, A. Theriault, Inorg. Chim. Acta 2001, 315, 96–106.
- 21F. Calisto, F. M. Sousa, F. V. Sena, P. N. Refojo, M. M. Pereira, Chem. Rev. 2021, 121, 1804–1844.
- 22A. R. Rowe, F. Salimijazi, L. Trutschel, J. Sackett, O. Adesina, I. Anzai, L. H. Kugelmass, M. H. Baym, B. Barstow, Commun. Biol. 2021, 4, 957.
- 23J. L. Burns, T. J. DiChristina, Appl. Environ. Microbiol. 2009, 75, 5209–5217.
- 24X. Jiang, B. Burger, F. Gajdos, C. Bortolotti, Z. Futera, M. Breuer, J. Blumberger, Proc. Natl. Acad. Sci. USA 2019, 116, 3425–3430.
- 25
- 25aY. Tachibana, L. Vayssieres, J. R. Durrant, Nat. Photonics 2012, 6, 511–518;
- 25bB. Zhang, L. Sun, Chem. Soc. Rev. 2019, 48, 2216–2264;
- 25cM. D. Karkas, O. Verho, E. V. Johnston, B. Akermark, Chem. Rev. 2014, 114, 11863–12001.
- 26
- 26aN. Kornienko, J. Z. Zhang, K. K. Sakimoto, P. Yang, E. Reisner, Nat. Nanotechnol. 2018, 13, 890–899;
- 26bX. Guan, 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, S. Ersan, Nat. Catal. 2022, 5, 1019.
- 27
- 27aK. Schuchmann, V. Mueller, Nat. Rev. Microbiol. 2014, 12, 809–821;
- 27bJ. B. Russell, F. Diez-Gonzalez, Adv. Microb. Physiol. 1998, 39, 205–234;
- 27cK. Valgepea, R. d. S. P. Lemgruber, K. Meaghan, R. W. Palfreyman, T. Abdalla, B. D. Heijstra, J. B. Behrendorff, R. Tappel, M. Kopke, S. D. Simpson, L. K. Nielsen, E. Marcellin, Cell Syst. 2017, 4, 505–515.
