Interfacing biosynthetic CdS with engineered Rhodopseudomonas palustris for efficient visible light-driven CO2–CH4 conversion
Yu Zhang1, Yulei Qian1, Zhenye Tong1, Su Yan1, Xiaoyu Yong1, Yang-Chun Yong2, Jun Zhou1()
1. Bioenergy Research Institute, College of Biotechnology and Pharmaceutical Engineering, Nanjing Tech University, Nanjing 211816, China 2. Biofuels Institute, Jiangsu Collaborative Innovation Center of Technology and Material of Water Treatment, School of Emergency Management & School of Environment and Safety Engineering, Jiangsu University, Zhenjiang 212013, China
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.
Nitrogenase iron-molybdenum cofactor biosynthesis protein nifN
2.29
3.80
HZF03_RS23215
nifE
Nitrogenase iron-molybdenum cofactor biosynthesis protein nifE
5.10
6.71
HZF03_RS23220
nifK
Nitrogenase molybdenum-iron protein subunit beta
12.18
28.67
HZF03_RS23225
nifD
Nitrogenase molybdenum-iron protein alpha chain
7.20
13.07
HZF03_RS23230
nifH
Nitrogenase iron protein
6.06
10.21
HZF03_RS07010
anfO
Fe-only nitrogenase accessory protein anfO
4.91
2.54
HZF03_RS07015
anfK
Fe-only nitrogenase subunit beta
13.71
10.90
HZF03_RS07020
anfG
Fe-only nitrogenase subunit delta
2.46
1.93
HZF03_RS07025
anfD
Nitrogenase iron-iron protein%2C alpha chain
6.55
6.39
HZF03_RS07030
–
Nitrogenase iron protein
2.96
2.73
HZF03_RS12740
–
vanadium nitrogenase
3.48
2.87
Tab.2
Gene ID
Gene name
Gene description
R. palustris, TPM
R. palustris-CdS, TPM
HZF03_RS09970
–
MotA/TolQ/ExbB proton channel family protein
21.26
48.69
HZF03_RS19870
flgK
Flagellar hook-associated protein flgK
12.82
28.93
HZF03_RS19875
–
Flagellar hook-basal body complex protein
32.3
104.51
HZF03_RS06590
–
Flagellar basal body rod modification protein flgD
12.65
38.98
HZF03_RS02405
–
Pilus assembly protein
9.01
19.69
HZF03_RS18575
–
Flp family type IVb pilin
4759.8
9872.82
Tab.3
Fig.6
Fig.7
1
J X Cao , J Zhang , Y Chen , R Fan , L Xu , E T Wu , Y Xue , J L Yang , Y M Chen , B Yang . et al.. Current status, future prediction and offset potential of fossil fuel CO2 emissions in China. Journal of Cleaner Production, 2023, 426: 139207 https://doi.org/10.1016/j.jclepro.2023.139207
2
J X Zhu , J T Li , R H Lu , R H Yu , S Y Zhao , C B Li , L Lv , L X Xia , X B Chen , W W Cai . et al.. Surface passivation for highly active, selective, stable, and scalable CO2 electroreduction. Nature Communications, 2023, 14(1): 4670 https://doi.org/10.1038/s41467-023-40342-6
3
L Lv , R H Lu , J X Zhu , R H Yu , W Zhang , E H Cui , X B Chen , Y H Dai , L M Cui , J Li . et al.. Coordinating the edge defects of bismuth with sulfur for enhanced CO2 electroreduction to formate. Angewandte Chemie International Edition, 2023, 62(25): e202303117 https://doi.org/10.1002/anie.202303117
4
B SuM ZhengW LinX F LuD LuanS B WangX W D. Lou X W Lou. S-scheme Co9S8@Cd0.8Zn0.2S-DETA hierarchical nanocages bearing organic CO2 activators for photocatalytic syngas production. Advanced Energy Materials, 2023, 13(15): 2203290
5
Y F Zhao , G B Chen , T Bian , C Zhou , G I N Waterhouse , L Z Wu , C H Tung , L J Smith , D O’Hare , T R Zhang . Defect-rich ultrathin ZnAl-layered double hydroxide nanosheets for efficient photoreduction of CO2 to CO with water. Advanced Materials, 2015, 27(47): 7824–7831 https://doi.org/10.1002/adma.201503730
6
J X Zhu , L Lv , S Zaman , X B Chen , Y H Dai , S H Chen , G J He , D S Wang , L Q Mai . Advances and challenges in single-site catalysts towards electrochemical CO2 methanation. Energy & Environmental Science, 2023, 16(11): 4812–4833 https://doi.org/10.1039/D3EE02196C
7
Y Wang , C B Zhang , R G Li . Modulating the selectivity of photocatalytic CO2 reduction in barium titanate by introducing oxygen vacancies. Transactions of Tianjin University, 2022, 28(4): 227–235 https://doi.org/10.1007/s12209-022-00334-x
8
N S Weliwatte , S D Minteer . Photo-bioelectrocatalytic CO2 reduction for a circular energy landscape. Joule, 2021, 5(10): 2564–2592 https://doi.org/10.1016/j.joule.2021.08.003
9
M Kumar , P C Sahoo , S Srikanth , R Bagai , S K Puri , S S V Ramakumar . Photosensitization of electro-active microbes for solar assisted carbon dioxide transformation. Bioresource Technology, 2019, 272: 300–307 https://doi.org/10.1016/j.biortech.2018.10.031
10
M Martins , C Toste , I A C Pereira . Enhanced light-driven hydrogen production by self-photosensitized biohybrid systems. Angewandte Chemie International Edition, 2021, 60(16): 9055–9062 https://doi.org/10.1002/anie.202016960
11
J Ye , J Yu , Y Y Zhang , M Chen , X Liu , S G Zhou , Z He . Light-driven carbon dioxide reduction to methane by Methanosarcina barkeri-CdS biohybrid. Applied Catalysis B: Environmental, 2019, 257: 117916 https://doi.org/10.1016/j.apcatb.2019.117916
12
J Ye , G P Ren , L Kang , Y Y Zhang , X Liu , S G Zhou , Z He . Efficient photoelectron capture by Ni decoration in Methanosarcina barkeri-CdS biohybrids for enhanced photocatalytic CO2-to-CH4 conversion. iScience, 2020, 23(7): 101287 https://doi.org/10.1016/j.isci.2020.101287
13
L Y Liu , G J Xie , J Ding , B F Liu , D F Xing , N Q Ren , Q Wang . Microbial methane emissions from the non-methanogenesis processes: a critical review. Science of the Total Environment, 2022, 806: 151362 https://doi.org/10.1016/j.scitotenv.2021.151362
14
M Bižić , T Klintzsch , D Ionescu , M Y Hindiyeh , M Günthel , A M Muro-Pastor , W Eckert , T Urich , F Keppler , H P Grossart . Aquatic and terrestrial cyanobacteria produce methane. Science Advances, 2020, 6(3): eaax5343 https://doi.org/10.1126/sciadv.aax5343
15
Y T Zhang , W Wei , Y Wang , B J Ni . Enhancing methane production from algae anaerobic digestion using diatomite. Journal of Cleaner Production, 2021, 315: 128138 https://doi.org/10.1016/j.jclepro.2021.128138
16
K Lenhart , M Bunge , S Ratering , T R Neu , I Schüttmann , M Greule , C Kammann , S Schnell , C Müller , H Zorn . et al.. Evidence for methane production by saprotrophic fungi. Nature Communications, 2012, 3(1): 1046 https://doi.org/10.1038/ncomms2049
17
Y N Zheng , D F Harris , Z Yu , Y F Fu , S Poudel , R N Ledbetter , K R Fixen , Z Y Yang , E S Boyd , M E Lidstrom . et al.. A pathway for biological methane production using bacterial iron-only nitrogenase. Nature Microbiology, 2018, 3(3): 281–286 https://doi.org/10.1038/s41564-017-0091-5
18
L Q Ma , Z Fang , Y Z Wang , J Zhou , Y C Yong . Photo-driven highly efficient one-step CO2 biomethanation with engineered photo-synthetic bacteria Rhodopseudomonas palustris. ACS Sustainable Chemistry & Engineering, 2020, 8(26): 9616–9621 https://doi.org/10.1021/acssuschemeng.0c02703
19
B Wang , K M Xiao , Z F Jiang , J F Wang , J C Yu , P K Wong . Biohybrid photoheterotrophic metabolism for significant enhancement of biological nitrogen fixation in pure microbial cultures. Energy & Environmental Science, 2019, 12(7): 2185–2191 https://doi.org/10.1039/C9EE00705A
20
L Shang , B Tong , H J Yu , G I N Waterhouse , C Zhou , Y F Zhao , M Tahir , L Z Wu , C H Tung , T Zhang . CdS nanoparticle-decorated Cd nanosheets for efficient visible light-driven photocatalytic hydrogen evolution. Advanced Energy Materials, 2016, 6(3): 1501241 https://doi.org/10.1002/aenm.201501241
21
B LaSarre , D T Kysela , B D Stein , A Ducret , Y V Brun , J B McKinlay . Restricted localization of photosynthetic intracytoplasmic membranes (ICMs) in multiple genera of purple nonsulfur bacteria. MBio, 2018, 9(4): e00780–18 https://doi.org/10.1128/mBio.00780-18
22
B Wang , Z F Jiang , J C Yu , J F Wang , P K Wong . Enhanced CO2 reduction and valuable C2+ chemical production by a CdS-photosynthetic hybrid system. Nanoscale, 2019, 11(19): 9296–9301 https://doi.org/10.1039/C9NR02896J
23
J Wang , T Xia , L Wang , X S Zheng , Z M Qi , C Gao , J F Zhu , Z Q Li , H X Xu , Y J Xiong . 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 https://doi.org/10.1002/anie.201810550
24
H J Bai , Z M Zhang , Y Guo , G E Yang . Biosynthesis of cadmium sulfide nanoparticles by photosynthetic bacteria Rhodopseudomonas palustris. Colloids and Surfaces. B, Biointerfaces, 2009, 70(1): 142–146 https://doi.org/10.1016/j.colsurfb.2008.12.025
25
K K Sakimoto , A B Wong , P Yang . Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science, 2016, 351(6268): 74–77 https://doi.org/10.1126/science.aad3317
26
S F Huang , J H Tang , X Liu , G W Dong , S G Zhou . Fast light-driven biodecolorization by a Geobacter sulfurreducens-CdS biohybrid. ACS Sustainable Chemistry & Engineering, 2019, 7(18): 15427–15433 https://doi.org/10.1021/acssuschemeng.9b02870
27
D Gupta , M S Guzman , A Bose . Extracellular electron uptake by autotrophic microbes: physiological, ecological, and evolutionary implications. Journal of Industrial Microbiology & Biotechnology, 2020, 47(9–10): 863–876 https://doi.org/10.1007/s10295-020-02309-0
28
G J Chen , Z R Zhou , B F Li , X H Lin , C Yang , Y X Fang , W Lin , Y D Hou , G G Zhang , S Wang , S B Wang . S-Scheme heterojunction of crystalline carbon nitride nanosheets and ultrafine WO3 nanoparticles for photocatalytic CO2 reduction. Journal of Environmental Sciences, 2024, 140: 103–112 https://doi.org/10.1016/j.jes.2023.05.028
29
X ZhuangY D HouR S YuanZ X DingO Wee-JunS B Wang. 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
M Y Chen , Z Fang , L X Xu , D Zhou , X J Yang , H J Zhu , Y C Yong . Enhancement of photo-driven biomethanation under visible light by nano-engineering of Rhodopseudomonas palustris. Bioresources and Bioprocessing, 2021, 8(1): 30 https://doi.org/10.1186/s40643-021-00383-5
31
S Jin , Y Jeon , M S Jeon , J Shin , Y Song , S Kang , J Bae , S Cho , J K Lee , D R Kim . et al.. 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 https://doi.org/10.1073/pnas.2020552118
32
D Gupta , M C Sutherland , K Rengasamy , J M Meacham , R G Kranz , A Bose . Photoferrotrophs produce a pioAB electron conduit for extracellular electron uptake. MBio, 2019, 10(6): e02668–19 https://doi.org/10.1128/mBio.02668-19
33
M Grattieri . Purple bacteria photo-bioelectrochemistry: enthralling challenges and opportunities. Photochemical & Photobiological Sciences, 2020, 19(4): 424–435 https://doi.org/10.1039/c9pp00470j
34
O Czarnecki , B Grimm . Post-translational control of tetrapyrrole biosynthesis in plants, algae, and cyanobacteria. Journal of Experimental Botany, 2012, 63(4): 1675–1687 https://doi.org/10.1093/jxb/err437
35
J J Buggy , M W Sganga , C E Bauer . 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 https://doi.org/10.1128/jb.176.22.6936-6943.1994
36
M S Guzman , K Rengasamy , M M Binkley , C Jones , T O Ranaivoarisoa , R Singh , D A Fike , J M Meacham , A Bose . Phototrophic extracellular electron uptake is linked to carbon dioxide fixation in the bacterium Rhodopseudomonas palustris. Nature Communications, 2019, 10(1): 1355 https://doi.org/10.1038/s41467-019-09377-6
37
Y Zeng , X Zhou , R L Qi , N Dai , X C Fu , H Zhao , K Peng , H T Yuan , Y M Huang , F T Lv . et al.. Photoactive conjugated polymer-based hybrid biosystems for enhancing cyanobacterial photosynthesis and regulating redox state of protein. Advanced Functional Materials, 2021, 31(8): 2007814 https://doi.org/10.1002/adfm.202007814
38
J B McKinlay , C S Harwood . 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 https://doi.org/10.1073/pnas.1006175107
39
Y N Zheng , C S Harwood . 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 https://doi.org/10.1128/AEM.02671-18
40
Y Kim , S A Shin , J Lee , K D Yang , K T Nam . Hybrid system of semiconductor and photosynthetic protein. Nanotechnology, 2014, 25(34): 342001 https://doi.org/10.1088/0957-4484/25/34/342001
41
K A Brown , D F Harris , M B Wilker , A Rasmussen , N Khadka , H Hamby , S Keable , G Dukovic , J W Peters , L C Seefeldt . et al.. Light-driven dinitrogen reduction catalyzed by a CdS:nitrogenase MoFe protein biohybrid. Science, 2016, 352(6284): 448–450 https://doi.org/10.1126/science.aaf2091
42
D Z Cui , J Q Wang , H Wang , Y Yang , M Zhao . The cytotoxicity of endogenous CdS and Cd2+ ions during CdS NPs biosynthesis. Journal of Hazardous Materials, 2021, 409: 124485 https://doi.org/10.1016/j.jhazmat.2020.124485
43
B Weng , M Y Qi , C Han , Z R Tang , Y J Xu . Photocorrosion inhibition of semiconductor-based photocatalysts: basic principle, current development, and future perspective. ACS Catalysis, 2019, 9(5): 4642–4687 https://doi.org/10.1021/acscatal.9b00313
44
P L Tremblay , M Y Xu , Y M Chen , T Zhang . Nonmetallic abiotic-biological hybrid photocatalyst for visible water splitting and carbon dioxide reduction. iScience, 2020, 23(1): 100784 https://doi.org/10.1016/j.isci.2019.100784
45
M Gürgan , H Koku , I Eroglu , M Yücel . 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 https://doi.org/10.1016/j.ijhydene.2020.03.108
46
K Venkidusamy , M Megharaj , U Schröder , F Karouta , S V Mohan , R Naidu . Electron transport through electrically conductive nanofilaments in Rhodopseudomonas palustris strain RP2. RSC Advances, 2015, 5(122): 100790–100798 https://doi.org/10.1039/C5RA08742B
