Interfacing biosynthetic CdS with engineered Rhodopseudomonas palustris for efficient visible light-driven CO₂–CH₄ conversion

Abstract

Engineered photosynthetic bacterium Rhodopseudomonas palustris is excellent at one-step CO₂ biomethanation and can use near-infrared light sources, overcoming the limitations of conventional photosynthetic systems. The current study constructed a biohybrid system that deposited CdS nanoparticles on R. palustris. This biohybrid system broadens the capture of sustainable solar energy, achieving a 155 nmol·mL^–1 biological CH₄ production under full visible light irradiation, 13.4-fold of that by the pure R. palustris. The transcriptome profiles revealed that gene expression related to photosynthetic electron transfer chain, nitrogenase, nanofilaments, and redox stress defense was activated. Accordingly, we attributed the much-enhanced CO₂ biomethanation in the biohybrid system to the remarkable increase in the intracellular reducing power and the stronger rigidity of the cells assisted by photoexcited electrons from CdS nanoparticles. Our discovery offers insight and a promising strategy for improving the current CO₂–CH₄ biomanufacturing system.

Graphical abstract

Keywords

CO₂ methanation / Rhodopseudomonas palustris / CdS nanoparticles / green catalysis

References

[1] Cao J X , Zhang J , Chen Y , Fan R , Xu L , Wu E T , Xue Y , Yang J L , Chen Y M , Yang B . . Current status, future prediction and offset potential of fossil fuel CO₂ emissions in China. Journal of Cleaner Production, 2023, 426: 139207

[2] Zhu J X , Li J T , Lu R H , Yu R H , Zhao S Y , Li C B , Lv L , Xia L X , Chen X B , Cai W W . . Surface passivation for highly active, selective, stable, and scalable CO₂ electroreduction. Nature Communications, 2023, 14(1): 4670

[3] Lv L , Lu R H , Zhu J X , Yu R H , Zhang W , Cui E H , Chen X B , Dai Y H , Cui L M , Li J . . Coordinating the edge defects of bismuth with sulfur for enhanced CO₂ electroreduction to formate. Angewandte Chemie International Edition, 2023, 62(25): e202303117

[4] SuBZhengMLinWLuX FLuanDWangS BLouX W D. Lou X W. S-scheme Co₉S₈@Cd_0.8Zn_0.2S-DETA hierarchical nanocages bearing organic CO₂ activators for photocatalytic syngas production. Advanced Energy Materials, 2023, 13(15): 2203290

[5] Zhao Y F , Chen G B , Bian T , Zhou C , Waterhouse G I N , Wu L Z , Tung C H , Smith L J , O’Hare D , Zhang T R . Defect-rich ultrathin ZnAl-layered double hydroxide nanosheets for efficient photoreduction of CO₂ to CO with water. Advanced Materials, 2015, 27(47): 7824–7831

[6] Zhu J X , Lv L , Zaman S , Chen X B , Dai Y H , Chen S H , He G J , Wang D S , Mai L Q . Advances and challenges in single-site catalysts towards electrochemical CO₂ methanation. Energy & Environmental Science, 2023, 16(11): 4812–4833

[7] Wang Y , Zhang C B , Li R G . Modulating the selectivity of photocatalytic CO₂ reduction in barium titanate by introducing oxygen vacancies. Transactions of Tianjin University, 2022, 28(4): 227–235

[8] Weliwatte N S , Minteer S D . Photo-bioelectrocatalytic CO₂ reduction for a circular energy landscape. Joule, 2021, 5(10): 2564–2592

[9] Kumar M , Sahoo P C , Srikanth S , Bagai R , Puri S K , Ramakumar S S V . Photosensitization of electro-active microbes for solar assisted carbon dioxide transformation. Bioresource Technology, 2019, 272: 300–307

[10] Martins M , Toste C , Pereira I A C . Enhanced light-driven hydrogen production by self-photosensitized biohybrid systems. Angewandte Chemie International Edition, 2021, 60(16): 9055–9062

[11] Ye J , Yu J , Zhang Y Y , Chen M , Liu X , Zhou S G , He Z . Light-driven carbon dioxide reduction to methane by Methanosarcina barkeri-CdS biohybrid. Applied Catalysis B: Environmental, 2019, 257: 117916

[12] Ye J , Ren G P , Kang L , Zhang Y Y , Liu X , Zhou S G , He Z . Efficient photoelectron capture by Ni decoration in Methanosarcina barkeri-CdS biohybrids for enhanced photocatalytic CO₂-to-CH₄ conversion. iScience, 2020, 23(7): 101287

[13] Liu L Y , Xie G J , Ding J , Liu B F , Xing D F , Ren N Q , Wang Q . Microbial methane emissions from the non-methanogenesis processes: a critical review. Science of the Total Environment, 2022, 806: 151362

[14] Bižić M , Klintzsch T , Ionescu D , Hindiyeh M Y , Günthel M , Muro-Pastor A M , Eckert W , Urich T , Keppler F , Grossart H P . Aquatic and terrestrial cyanobacteria produce methane. Science Advances, 2020, 6(3): eaax5343

[15] Zhang Y T , Wei W , Wang Y , Ni B J . Enhancing methane production from algae anaerobic digestion using diatomite. Journal of Cleaner Production, 2021, 315: 128138

[16] Lenhart K , Bunge M , Ratering S , Neu T R , Schüttmann I , Greule M , Kammann C , Schnell S , Müller C , Zorn H . . Evidence for methane production by saprotrophic fungi. Nature Communications, 2012, 3(1): 1046

[17] Zheng Y N , Harris D F , Yu Z , Fu Y F , Poudel S , Ledbetter R N , Fixen K R , Yang Z Y , Boyd E S , Lidstrom M E . . A pathway for biological methane production using bacterial iron-only nitrogenase. Nature Microbiology, 2018, 3(3): 281–286

[18] Ma L Q , Fang Z , Wang Y Z , Zhou J , Yong Y C . Photo-driven highly efficient one-step CO₂ biomethanation with engineered photo-synthetic bacteria Rhodopseudomonas palustris. ACS Sustainable Chemistry & Engineering, 2020, 8(26): 9616–9621

[19] Wang B , Xiao K M , Jiang Z F , Wang J F , Yu J C , Wong P K . Biohybrid photoheterotrophic metabolism for significant enhancement of biological nitrogen fixation in pure microbial cultures. Energy & Environmental Science, 2019, 12(7): 2185–2191

[20] Shang L , Tong B , Yu H J , Waterhouse G I N , Zhou C , Zhao Y F , Tahir M , Wu L Z , Tung C H , Zhang T . CdS nanoparticle-decorated Cd nanosheets for efficient visible light-driven photocatalytic hydrogen evolution. Advanced Energy Materials, 2016, 6(3): 1501241

[21] LaSarre B , Kysela D T , Stein B D , Ducret A , Brun Y V , McKinlay J B . Restricted localization of photosynthetic intracytoplasmic membranes (ICMs) in multiple genera of purple nonsulfur bacteria. MBio, 2018, 9(4): e00780–18

[22] Wang B , Jiang Z F , Yu J C , Wang J F , Wong P K . Enhanced CO₂ reduction and valuable C₂₊ chemical production by a CdS-photosynthetic hybrid system. Nanoscale, 2019, 11(19): 9296–9301

[23] Wang J , Xia T , Wang L , Zheng X S , Qi Z M , Gao C , Zhu J F , Li Z Q , Xu H X , Xiong Y J . Enabling visible-light-driven selective CO₂ reduction by doping quantum dots: trapping electrons and suppressing H₂ evolution. Angewandte Chemie International Edition, 2018, 57(50): 16447–16451

[24] Bai H J , Zhang Z M , Guo Y , Yang G E . Biosynthesis of cadmium sulfide nanoparticles by photosynthetic bacteria Rhodopseudomonas palustris. Colloids and Surfaces. B, Biointerfaces, 2009, 70(1): 142–146

[25] Sakimoto K K , Wong A B , Yang P . Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science, 2016, 351(6268): 74–77

[26] Huang S F , Tang J H , Liu X , Dong G W , Zhou S G . Fast light-driven biodecolorization by a Geobacter sulfurreducens-CdS biohybrid. ACS Sustainable Chemistry & Engineering, 2019, 7(18): 15427–15433

[27] Gupta D , Guzman M S , Bose A . Extracellular electron uptake by autotrophic microbes: physiological, ecological, and evolutionary implications. Journal of Industrial Microbiology & Biotechnology, 2020, 47(9–10): 863–876

[28] Chen G J , Zhou Z R , Li B F , Lin X H , Yang C , Fang Y X , Lin W , Hou Y D , Zhang G G , Wang S , Wang S B . S-Scheme heterojunction of crystalline carbon nitride nanosheets and ultrafine WO₃ nanoparticles for photocatalytic CO₂ reduction. Journal of Environmental Sciences, 2024, 140: 103–112

[29] ZhuangXHouY DYuanR SDingZ XWee-JunOWangS B. Hollow NiCo₂S₄ nanospheres as a cocatalyst to support ZnIn₂S₄ nanosheets for visible-light-driven hydrogen production. Acta Physico-Chimica Sinica, 2022, 38(7): 2111021 (in Chinese)

[30] Chen M Y , Fang Z , Xu L X , Zhou D , Yang X J , Zhu H J , Yong Y C . Enhancement of photo-driven biomethanation under visible light by nano-engineering of Rhodopseudomonas palustris. Bioresources and Bioprocessing, 2021, 8(1): 30

[31] Jin S , Jeon Y , Jeon M S , Shin J , Song Y , Kang S , Bae J , Cho S , Lee J K , Kim D R . . Acetogenic bacteria utilize light-driven electrons as an energy source for autotrophic growth. Proceedings of the National Academy of Sciences of the United States of America, 2021, 118(9): e2020552118

[32] Gupta D , Sutherland M C , Rengasamy K , Meacham J M , Kranz R G , Bose A . Photoferrotrophs produce a pioAB electron conduit for extracellular electron uptake. MBio, 2019, 10(6): e02668–19

[33] Grattieri M . Purple bacteria photo-bioelectrochemistry: enthralling challenges and opportunities. Photochemical & Photobiological Sciences, 2020, 19(4): 424–435

[34] Czarnecki O , Grimm B . Post-translational control of tetrapyrrole biosynthesis in plants, algae, and cyanobacteria. Journal of Experimental Botany, 2012, 63(4): 1675–1687

[35] Buggy J J , Sganga M W , Bauer C E . Characterization of a light-responding transactivator responsible for differentially controlling reaction-center and light-harvesting-I gene-expression in rhodobacter-capsulatus. Journal of Bacteriology, 1994, 176(22): 6936–6943

[36] Guzman M S , Rengasamy K , Binkley M M , Jones C , Ranaivoarisoa T O , Singh R , Fike D A , Meacham J M , Bose A . Phototrophic extracellular electron uptake is linked to carbon dioxide fixation in the bacterium Rhodopseudomonas palustris. Nature Communications, 2019, 10(1): 1355

[37] Zeng Y , Zhou X , Qi R L , Dai N , Fu X C , Zhao H , Peng K , Yuan H T , Huang Y M , Lv F T . . Photoactive conjugated polymer-based hybrid biosystems for enhancing cyanobacterial photosynthesis and regulating redox state of protein. Advanced Functional Materials, 2021, 31(8): 2007814

[38] McKinlay J B , Harwood C S . Carbon dioxide fixation as a central redox cofactor recycling mechanism in bacteria. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(26): 11669–11675

[39] Zheng Y N , Harwood C S . Influence of energy and electron availability on in vivo methane and hydrogen production by a variant molybdenum nitrogenase. Applied and Environmental Microbiology, 2019, 85(9): e02671–18

[40] Kim Y , Shin S A , Lee J , Yang K D , Nam K T . Hybrid system of semiconductor and photosynthetic protein. Nanotechnology, 2014, 25(34): 342001

[41] Brown K A , Harris D F , Wilker M B , Rasmussen A , Khadka N , Hamby H , Keable S , Dukovic G , Peters J W , Seefeldt L C . . Light-driven dinitrogen reduction catalyzed by a CdS:nitrogenase MoFe protein biohybrid. Science, 2016, 352(6284): 448–450

[42] Cui D Z , Wang J Q , Wang H , Yang Y , Zhao M . The cytotoxicity of endogenous CdS and Cd²⁺ ions during CdS NPs biosynthesis. Journal of Hazardous Materials, 2021, 409: 124485

[43] Weng B , Qi M Y , Han C , Tang Z R , Xu Y J . Photocorrosion inhibition of semiconductor-based photocatalysts: basic principle, current development, and future perspective. ACS Catalysis, 2019, 9(5): 4642–4687

[44] Tremblay P L , Xu M Y , Chen Y M , Zhang T . Nonmetallic abiotic-biological hybrid photocatalyst for visible water splitting and carbon dioxide reduction. iScience, 2020, 23(1): 100784

[45] Gürgan M , Koku H , Eroglu I , Yücel M . Transcriptome analysis of the effects of light and dark cycle on hydrogen production metabolism of Rhodobacter capsulatus DSM1710. International Journal of Hydrogen Energy, 2020, 45(60): 34707–34719

[46] Venkidusamy K , Megharaj M , Schröder U , Karouta F , Mohan S V , Naidu R . Electron transport through electrically conductive nanofilaments in Rhodopseudomonas palustris strain RP2. RSC Advances, 2015, 5(122): 100790–100798

Competing interests

The authors declare that they have no competing interests.

Acknowledgements

This work was supported by the 2022 Carbon Dafeng and Carbon Neutral Science and Technology Innovation Special Fund in Jiangsu Province (Grant No. BK20220003), the National Natural Science Foundation of China (Grant No. 32371538), the Special Funds for Jiangsu Provincial Science and technology plan (Grant No. BZ2022052), the Jiangsu Agriculture Science and Technology Innovation Fund (Grant No. CX(21)2015), and the Jiangsu Synergetic Innovation Center for Advanced Bio-Manufacture (Grant No. XTD2204).

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11705-024-2460-y and is accessible for authorized users.

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