Abstract
Electronic exchanges occur between semiconductor minerals and microorganisms. However, researchers have focused on the photocatalytic degradation of pollutants by semiconductor minerals, and there is a limited amount of studies on semiconductor photogenerated electrons that influence the growth and energetic mechanisms of bacteria. Bioelectrochemical systems (BES) are important new bioengineering technologies for investigating the mechanisms by which bacteria absorb electrons. In this work, we built a BES that used α-Fe2O3 nanorods as a photoanode and Citrobacter freundii as bio-cathode bacteria to explore the effect of photoelectrons on C. freundii growth and metabolism. The photoanode was prepared by a hydrothermal synthesis method. As confirmed by X-ray diffraction (XRD) and X-ray photoelectron spectroscopy (XPS), the photoanode was made of α-Fe2O3. Corresponding scanning electron microscope (SEM) images showed that α-Fe2O3 nanorod arrays formed with a diameter of 50 nm, and the band gap was 2.03 eV, as indicated by UV–vis diffuse reflectance spectroscopy (UV–vis DRS). The C. freundii growth metabolism changed significantly because of photoelectrons; under light conditions, the growth rate of C. freundii significantly accelerated, and as inferred from the three-dimensional fluorescence spectrum, the protein, humic acid, and NADH concentrations were significantly higher at 72 h. According to the changes in the organic acid content, photoelectrons participated in the reductive tricarboxylic acid cycle (rTCA) to enhance growth and metabolism. The results of the study have broad implications for advancing fields that study the effects of semiconductor minerals on electroactive microorganisms and the semiconductor-photoelectronic transport mechanisms of electroautotrophic microorganisms.
Key points
• For the first time, A BES was built that used α-Fe2O3 nanorods as a photoanode and C. freundii as a bio-cathode bacteria.
• Photoelectrons produced by α-Fe2O3 photoelectrode promote the growth of C. freundii.
• Effects of photoelectrons on C. freundii metabolism were conjectured by the changes of organic acids and NADH.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data used to support the findings of this study are available from the corresponding author upon request.
References
Ahmed DH, Sung HJ, Bae J, Lee DR (2008) Reactants flow behavior and water management for different current densities in PEMFC. Int J Heat Mass Tran 51(7–8):2006–2019. https://doi.org/10.1016/j.ijheatmasstransfer.2007.06.027
Beese-Vasbender PF, Nayak S, Erbe A, Stratmann M, Mayrhofer KJJ (2015) Electrochemical characterization of direct electron uptake in electrical microbially influenced corrosion of iron by the lithoautotrophic SRB Desulfopila corrodens strain IS4. Electrochimica Acta 167:321–329. https://doi.org/10.1016/j.electacta.2015.03.184
Canstein HV, Ogawa J, Shimizu S, Lloyd JR (2008) Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl Environ Microb 74(3):615–623. https://doi.org/10.1128/AEM.01387-07
Carbajosa S, Malki M, Caillard R, Lopez MF, Palomares FJ, Martín-Gago JA, Rodríguez N, Amils R, Fernández VM, De Lacey AL (2010) Electrochemical growth of Acidithiobacillus ferrooxidans on a graphite electrode for obtaining a biocathode for direct electrocatalytic reduction of oxygen. Biosens and Bioelectron 26(2):877–880. https://doi.org/10.1016/j.bios.2010.07.037
Chen M, He M, Liu M, Dong F, Nie X (2019a) Synergistic effects of electron shuttle AQS and Alcaligenes faecalis on photocatalytic removal of U(VI). J Radioanal Nuclear Ch 322(2):731–742. https://doi.org/10.1007/s10967-019-06753-w
Chen M, Zhou XF, Yu YQ, Liu X, Raymond JX (2019b) Light-driven nitrous oxide production via autotrophic denitrification by self-photosensitized Thiobacillus denitrificans. Environ Int 127:353–360. https://doi.org/10.1016/j.envint.2019b.03.045
de Campos Rodrigues T, Rosenbaum MA (2014) Microbial electroreduction: screening for new cathodic biocatalysts. Chem Electro Chem 1(11):1916–1922. https://doi.org/10.1002/celc.201402239
Deng X, Dohmae N, Kaksonen AH, Okamoto A (2020) Biogenic iron sulfide nanoparticles to enable extracellular electron uptake in sulfate-reducing bacteria. Angewandte Chemie 132(15):5995–5999. https://doi.org/10.1002/anie.201915196
Deng X, Saito J, Kaksone NA, Okamoto A (2020) Enhancement of cell growth by uncoupling extracellular electron uptake and oxidative stress production in sediment sulfate-reducing bacteria. Ennviron Int 144:106006. https://doi.org/10.1016/j.envint.2020b.106006
FöRster AH, Beblawy S, Golitsch F, Gescher J (2017) Electrode-assisted acetoin production in a metabolically engineered Escherichia coli strain. Biotechnol Biofuels 10(1):65. https://doi.org/10.1186/s13068-017-0745-9
Feng H, Liang Y, Guo K, Li N, Shen D, Cong Y, Zhou Y, Wang Y, Wang M, Long Y (2016) Hybridization of photoanode and bioanode to enhance the current production of bioelectrochemical systems. Water Res 102:428–435. https://doi.org/10.1016/j.watres.2016.06.061
Feng J, Jiang M, Li K, Lu Q, Ouyang P (2020) Direct electron uptake from a cathode using the inward Mtr pathway in Escherichia coli. Bioelectrochemistry 134:107498. https://doi.org/10.1016/j.bioelechem.2020.107498
Guzman MS, Rengasamy K, Binkley MM, Jones C, Ranaivoarisoa TO, Singh R, Fike DA, Meacham JM, Bose A (2019) Phototrophic extracellular electron uptake is linked to carbon dioxide fixation in the bacterium Rhodopseudomonas palustris. Nat Commun 10(1):1–13. https://doi.org/10.1038/s41467-019-09377-6
Huang G, Qu L, Ding Y (2019) Birnessite modified graphite cathode toward efficient autotrophic denitrification of Thiobacillus denitrificans in bioelectrochemical system. Desalin Water Treat 150:367–373. https://doi.org/10.5004/dwt.2019.23750
Liu PC, Ma XL, Li TT, Yan F, Xiao X (2020) Elucidation of photodegradation of p-chlorophenol in a biophotoelectric reductive degradation system by density functional theory calculations. Int Biodeter Biodegr 151:104969. https://doi.org/10.1016/j.ibiod.2020.104969
Lu A, Li Y, Jin S (2012) Interactions between semiconducting minerals and bacteria under light. Elements 8(2):125–130. https://doi.org/10.2113/gselements.8.2.125
Lu A, Li Y, Jin S, Wang X, Wu XL, Zeng C, Ding H, Hao R, Lv M, Wang C (2012) Growth of non-phototrophic microorganisms using solar energy through mineral photocatalysis. Nat Commun 3(1):1–8. https://doi.org/10.1038/ncomms1768
Lu A, Li Y, Lv M, Wang C, Yang L, Liu J, Wang Y, Wong KH, Wong PK (2007) Photocatalytic oxidation of methyl orange by natural V-bearing rutile under visible light. Sol Energ Mat and Sol C 91(19):1849–1855. https://doi.org/10.1016/j.solmat.2007.06.015
Lu A, Li Y, Wang X, Ding H, Zeng C, Yang X, Hao R, Wang C, Santosh M (2013) Photoelectrons from minerals and microbial world: a perspective on life evolution in the early Earth. Precambrian Res 231:401–408. https://doi.org/10.1016/j.precamres.2013.04.004
Meng F, Dong F, Liu M, Wang P (2018) Effects of photoelectron and photogenerated hole on the metabolites of Alcaligenes faecalis. Acta Microbiologica Sinica 58(4):538–545. https://0001-6209(2018)58:4<538:GDZHGS>2.0.TX;2-R
Mevers E, Su L, Pishchany G, Baruch M, Cornejo J, Hobert E, Dimise E, Ajo-Franklin CM, Clardy J (2019) An elusive electron shuttle from a facultative anaerobe. Elife 8:e48054. https://doi.org/10.7554/eLife.48054
Min D, Cheng L, Liu DF, Li WW, Yu HQ (2020) Electron transfer via the non-Mtr respiratory pathway from Shewanella putrefaciens CN-32 for methyl orange bioreduction. Prpcess Biochem 95(3):108–114. https://doi.org/10.1016/j.procbio.2020.05.015
Mohamed A, Yu L, Fang Y, Ashry N, Riahi Y, Uddin I, Dai K, Huang Q (2020) Iron mineral-humic acid complex enhanced Cr (VI) reduction by Shewanella oneidensis MR-1. Chemosphere 247:125902. https://doi.org/10.1016/j.chemosphere.2020.125902
Rowe AR, Rajeev P, Jain A, Pirbadian S, Okamoto A, Gralnick JA, El-Naggar MY, Nealson KH (2018) Tracking electron uptake from a cathode into Shewanella cells: implications for energy acquisition from solid-substrate electron donors. MBio 9(1):e02203-17. https://doi.org/10.1128/mBio.02203-17
Sakimoto KK, Wong AB, Yang P (2016) Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science 351(6268):62–68. https://doi.org/10.1126/science.aad3317
Satoshi K, Tetsuya Y, Akio U, Mcglynn SE, Takehiro S, Naoshi D, Takashi Y, Yoshihiko S, Nobuhiro M, Kazuhito H (2018) Anodic and cathodic extracellular electron transfer by the filamentous bacterium Ardenticatena maritima 110S. Front Microbiol 9:68–72. https://doi.org/10.3389/fmicb.2018.00068
Summers ZM, Gralnick JA, Bond DR (2013) Cultivation of an obligate Fe (II)-oxidizing lithoautotrophic bacterium using electrodes. MBio 4(1):e00420-12. https://doi.org/10.1128/mBio.00420-12
Wu Y, Li F, Liu T, Han R, Luo X (2016) pH dependence of quinone-mediated extracellular electron transfer in a bioelectrochemical system. Electrochimica Acta 213:408–415. https://doi.org/10.1016/j.electacta.2016.07.122
Zheng S, Liu F, Li M, Xiao L, Wang O (2018) Comparative transcriptomic insights into the mechanisms of electron transfer in Geobacter co-cultures with activated carbon and magnetite. Sci China Life Sci 61(7):787–798. https://doi.org/10.1007/s11427-017-9177-1
Zhu W, Liu X, Tan L, Cui Z, Wu S (2019) AgBr nanoparticles in-situ growth on 2D MoS2 nanosheets for rapid bacteria-killing and photo-disinfection. ACS Appl Mater & Inter 11(37):34364–34375. https://doi.org/10.1021/acsami.9b12629
Author information
Authors and Affiliations
Contributions
LB and JYW participated and performed the research, analyzed the data, and wrote the paper. YLW participated in the experiment. YQW and YY participated in modification. DZC and MZ conceived of or designed study. All the authors read and approved the manuscript.
Corresponding authors
Ethics declarations
Ethics approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Bai, L., Wang, J., Wang, Y. et al. Photocatalytic performance of an α-Fe2O3 electrode and its effects on the growth and metabolism of Citrobacter freundii. Appl Microbiol Biotechnol 106, 6253–6262 (2022). https://doi.org/10.1007/s00253-022-12120-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-022-12120-9