Expression of filaments of the Geobacter extracellular cytochrome OmcS in Shewanella oneidensis.
Geobacter
OmcS filaments
Shewanella oneidensis
extracellular electron transfer
outer surface cytochromes
Journal
Biotechnology and bioengineering
ISSN: 1097-0290
Titre abrégé: Biotechnol Bioeng
Pays: United States
ID NLM: 7502021
Informations de publication
Date de publication:
30 Mar 2024
30 Mar 2024
Historique:
revised:
01
03
2024
received:
09
10
2023
accepted:
11
03
2024
medline:
31
3
2024
pubmed:
31
3
2024
entrez:
30
3
2024
Statut:
aheadofprint
Résumé
The physiological role of Geobacter sulfurreducens extracellular cytochrome filaments is a matter of debate and the development of proposed electronic device applications of cytochrome filaments awaits methods for large-scale cytochrome nanowire production. Functional studies in G. sulfurreducens are stymied by the broad diversity of redox-active proteins on the outer cell surface and the redundancy and plasticity of extracellular electron transport routes. G. sulfurreducens is a poor chassis for producing cytochrome nanowires for electronics because of its slow, low-yield, anaerobic growth. Here we report that filaments of the G. sulfurreducens cytochrome OmcS can be heterologously expressed in Shewanella oneidensis. Multiple lines of evidence demonstrated that a strain of S. oneidensis, expressing the G. sulfurreducens OmcS gene on a plasmid, localized OmcS on the outer cell surface. Atomic force microscopy revealed filaments with the unique morphology of OmcS filaments emanating from cells. Electron transfer to OmcS appeared to require a functional outer-membrane porin-cytochrome conduit. The results suggest that S. oneidensis, which grows rapidly to high culture densities under aerobic conditions, may be suitable for the development of a chassis for producing cytochrome nanowires for electronics applications and may also be a good model microbe for elucidating cytochrome filament function in anaerobic extracellular electron transfer.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : The National Key Research and Development Program of China
ID : 2018YFA0901300
Organisme : The National Natural Science Foundation of China
ID : NSFC 22378305
Organisme : The National Natural Science Foundation of China
ID : 32071411
Organisme : The National Natural Science Foundation of China
ID : 21621004
Organisme : The Natural Science Foundation of Hebei Province
ID : B2020408005
Organisme : The Science and Technology Project of Hebei Education Department
ID : QN2021125
Informations de copyright
© 2024 Wiley Periodicals LLC.
Références
Aebersold, R., & Mann, M. (2003). Mass spectrometry‐based proteomics. Nature, 422, 198–207.
Aklujkar, M., Coppi, M. V., Leang, C., Kim, B. C., Chavan, M. A., Perpetua, L. A., Giloteaux, L., Liu, A., & Holmes, D. E. (2013). Proteins involved in electron transfer to Fe(III) and Mn(IV) oxides by Geobacter sulfurreducens and Geobacter uraniireducens. Microbiology, 159, 515–535.
Atkinson, J. T., Chavez, M. S., Niman, C. M., & El‐Naggar, M. Y. (2023). Living electronics: A catalogue of engineered living electronic components. Microbial Biotechnology, 16, 507–533.
Baron, D., LaBelle, E., Coursolle, D., Gralnick, J. A., & Bond, D. R. (2009). Electrochemical measurement of electron transfer kinetics by shewanella oneidensis MR‐1. Journal of Biological Chemistry, 284, 28865–28873.
Bouhenni, R. A., Vora, G. J., Biffinger, J. C., Shirodkar, S., Brockman, K., Ray, R., Wu, P., Johnson, B. J., Biddle, E. M., Marshall, M. J., Fitzgerald, L. A., Little, B. J., Fredrickson, J. K., Beliaev, A. S., Ringeisen, B. R., & Saffarini, D. A. (2010). The role of Shewanella oneidensis MR‐1 outer surface structures in extracellular electron transfer. Electroanalysis, 22, 856–864.
Bretschger, O., Obraztsova, A., Sturm, C. A., Chang, I. S., Gorby, Y. A., Reed, S. B., Culley, D. E., Reardon, C. L., Barua, S., Romine, M. F., Zhou, J., Beliaev, A. S., Bouhenni, R., Saffarini, D., Mansfeld, F., Kim, B. H., Fredrickson, J. K., & Nealson, K. H. (2007). Current production and metal oxide reduction by Shewanella oneidensis MR‐1 wild type and mutants. Applied and Environmental Microbiology, 73, 7003–7012.
Clarke, T. A. (2022). Plugging into bacterial nanowires: A comparison of model electrogenic organisms. Current Opinion in Microbiology, 66, 56–62.
Delgado, V. P., Paquete, C. M., Sturm, G., & Gescher, J. (2019). Improvement of the electron transfer rate in Shewanella oneidensis MR‐1 using a tailored periplasmic protein composition. Bioelectrochemistry, 129, 18–25.
Dong, F., Lee, Y. S., Gaffney, E. M., Liou, W., & Minteer, S. D. (2021). Engineering cyanobacterium with transmembrane electron transfer ability for bioelectrochemical nitrogen fixation. ACS Catalysis, 11, 13169–13179.
Filman, D. J., Marino, S. F., Ward, J. E., Yang, L., Mester, Z., Bullitt, E., Lovley, D. R., & Strauss, M. (2019). Cryo‐EM reveals the structural basis of long‐range electron transport in a cytochrome‐based bacterial nanowire. Communications Biology, 2, 219.
Flanagan, K. A., Leang, C., Ward, J. E., & Lovley, D. R. (2017). Improper localization of the OmcS cytochrome may explain the inability of the xapD‐deficient mutant of Geobacter sulfurreducens to reduce Fe(III) oxide. bioRxiv, 114900. https://doi.org/10.1101/114900
Foster, L. J., & Mann, M. (2006). Protein identification and sequencing by mass spectrometry. In J. E. Celis (Ed.), Cell biology (Vol. 4, pp. 363–369). Elsevier.
Fu, T., Liu, X., Fu, S., Woodard, T., Gao, H., Lovley, D. R., & Yao, J. (2021). Self‐sustained green neuromorphic interfaces. Nature Communications, 12, 3351.
Fu, T., Liu, X., Gao, H., Ward, J. E., Liu, X., Yin, B., Wang, Z., Zhuo, Y., Walker, D. J. F., Joshua Yang, J., Chen, J., Lovley, D. R., & Yao, J. (2020). Bioinspired bio‐voltage memristors. Nature Communications, 11, 1861.
Gralnick, J. A., & Bond, D. R. (2023). Electron transfer beyond the outer membrane: Putting electrons to rest. Annual Review of Microbiology, 77, 517–539.
Grote, A., Hiller, K., Scheer, M., Munch, R., Nortemann, B., Hempel, D. C., & Jahn, D. (2005). JCat: A novel tool to adapt codon usage of a target gene to its potential expression host. Nucleic Acids Research, 33, W526–W531.
Gstaiger, M., & Aebersold, R. (2009). Applying mass spectrometry‐based proteomics to genetics, genomics and network biology. Nature Reviews Genetics, 10, 617–627.
Guberman‐Pfeffer, M. J., Dorval Courchesne, N.‐M., & Lovley, D. R. (2024). Microbial nanowires for sustainable electronics. Nature Reviews Bioengineering, 2, (in press).
Gundry, R. L., White, M. Y., Murray, C. I., Kane, L. A., Fu, Q., Stanley, B. A., & Van Eyk, J. E. (2010). Preparation of proteins and peptides for mass spectrometry analysis in a bottom‐up proteomics workflow. Current protocols in molecular biology, 90(1).
Heukeshoven, J., & Dernick, R. (1985). Simplified method for silver staining of proteins in polyacrylamide gels and the mechanism of silver staining. Electrophoresis, 6, 103–112.
Izallalen, M., Glaven, R. H., Mester, T., Nevin, K. P., Franks, A. E., & Lovley, D. R. (2008). Going wireless? Additional phenotypes of a pilin‐deficient mutant weaken the genetic evidence for the role of microbial nanowires in extracellular electron transfer. In: Abstracts of the 108th Annual Meeting of the American Society for Microbiology (Boston, MA).
Kanehisa, M. (2000). KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Research, 28(1), 27–30.
Leang, C., Adams, L. A., Chin, K.‐J., Nevin, K. P., Methé, B. A., Webster, J., Sharma, M. L., & Lovley, D. R. (2005). Adaptation to disruption of the electron transfer pathway for Fe(III) reduction in Geobacter sulfurreducens. Journal of Bacteriology, 187(17), 5918–5926.
Leang, C., Coppi, M. V., & Lovley, D. R. (2003). OmcB, a c‐type polyheme cytochrome, involved in Fe(III) reduction in Geobacter sulfurreducens. Journal of Bacteriology, 185, 2096–2103.
Lekbach, Y., Ueki, T., Liu, X., Woodard, T., Yao, J., & Lovley, D. R. (2023). Microbial nanowires with genetically modified peptide ligands to sustainably fabricate electronic sensing devices. Biosensors and Bioelectronics, 226, 115147.
Liu, X., Fu, T., Ward, J., Gao, H., Yin, B., Woodard, T., Lovley, D. R., & Yao, J. (2020). Multifunctional protein nanowire humidity sensors for Green wearable electronics. Advanced Electronic Materials, 6, 2000721.
Liu, X., Gao, H., Ward, J. E., Liu, X., Yin, B., Fu, T., Chen, J., Lovley, D. R., & Yao, J. (2020). Power generation from ambient humidity using protein nanowires. Nature, 578, 550–554.
Liu, X., Holmes, D. E., Walker, D. J. F., Li, Y., Meier, D., Pinches, S., Woodard, T. L., & Smith, J. A. (2022). Cytochrome OmcS is not essential for extracellular electron transport via conductive pili in Geobacter sulfurreducens strain KN400. Applied and Environmental Microbiology, 88, e01622–01621.
Liu, X., Ueki, T., Gao, H., Woodard, T. L., Nevin, K. P., Fu, T., Fu, S., Sun, L., Lovley, D. R., & Yao, J. (2022). Microbial biofilms for electricity generation from water evaporation and power to wearables. Nature Communications, 13, 4369.
Liu, X., Walker, D. J. F., Nonnenmann, S. S., Sun, D., & Lovley, D. R. (2021). Direct observation of electrically conductive pili emanating from Geobacter sulfurreducens. mBio, 12, e02209–e02221.
Logan, B. E., Rossi, R., Ragab, A., & Saikaly, P. E. (2019). Electroactive microorganisms in bioelectrochemical systems. Nature Reviews Microbiology, 17, 307–319.
Lovley, D. R., & Holmes, D. E. (2022). Electromicrobiology: The ecophysiology of phylogenetically diverse electroactive microorganisms. Nature Reviews Microbiology, 20, 5–19.
Lovley, D. R., Ueki, T., Zhang, T., Malvankar, N. S., Shrestha, P. M., Flanagan, K., & Nevin, K. P. (2011). Geobacter: The microbe electric's physiology, ecology, and practical applications. Advances in Microbial Physiology, 59, 1–100.
Lovley, D. R., & Yao, J. (2021). Intrinsically conductive microbial nanowires for ‘Green’ electronics with novel functions. Trends in Biotechnology, 39, 940–952.
Ludwig, K. R., Schroll, M. M., & Hummon, A. B. (2018). Comparison of in‐solution, fasp, and s‐trap based digestion methods for bottom‐up proteomic studies. Journal of Proteome Research, 17, 2480–2490.
Malvankar, N. S., Tuominen, M. T., & Lovley, D. R. (2012). Lack of cytochrome involvement in long‐range electron transport through conductive biofilms and nanowires of Geobacter sulfurreducens. Energy & Environmental Science, 5, 8651–8659.
Mehta, T., Childers, S. E., Glaven, R., Lovley, D. R., & Mester, T. (2006). A putative multicopper protein secreted by an atypical type II secretion system involved in the reduction of insoluble electron acceptors in Geobacter sulfurreducens. Microbiology, 152, 2257–2264.
Mehta, T., Coppi, M. V., Childers, S. E., & Lovley, D. R. (2005). Outer membrane c‐type cytochromes required for Fe(III) and Mn(IV) oxide reduction in Geobacter sulfurreducens. Applied and Environmental Microbiology, 71, 8634–8641.
Nevin, K. P., Kim, B.‐C., Glaven, R. H., Johnson, J. P., Woodard, T. L., Methé, B. A., & Lovley, D. R. (2009). Anode biofilm transcriptomics reveals outer surface components essential for high current power production in Geobacter sulfurreducens fuel cells. PLoS One, 5(4), e5628.
Qian, X., Mester, T., Morgado, L., Arakawa, T., Sharma, M. L., Inoue, K., Joseph, C., Salgueiro, C. A., Maroney, M. J., & Lovley, D. R. (2011). Biochemical characterization of purified OmcS, a c‐type cytochrome required for insoluble Fe(III) reduction in Geobacter sulfurreducens. Biochimica et Biophysica Acta (BBA) ‐ Bioenergetics, 1807, 404–412.
Qian, X., Reguera, G., Mester, T., & Lovley, D. R. (2007). Evidence that OmcB and OmpB of Geobacter sulfurreducens are outer membrane surface proteins. FEMS Microbiology Letters, 277, 21–27.
Reguera, G., & Kashefi, K. (2019). The electrifying physiology of geobacter bacteria, 30 years on. Advances in Microbial Physiology, 74, 1–95.
Reguera, G., McCarthy, K. D., Mehta, T., Nicoll, J. S., Tuominen, M. T., & Lovley, D. R. (2005). Extracellular electron transfer via microbial nanowires. Nature, 435, 1098–1101.
Saltikov, C. W., & Newman, D. K. (2003). Genetic identification of a respiratory arsenate reductase. Proceedings of the National Academy of Sciences, 100, 10983–10988.
Schwarz, I. A., Alsaqri, B., Lekbach, Y., Henry, K., Gorman, S., Woodard, T. L., & Lovley, D. R. (2024). Lack of physiological evidence for cytochrome filaments functioning as conduits for extracellular electron transfer. mBio, 15, e00690–24.
Sekar, N., Jain, R., Yan, Y., & Ramasamy, R. P. (2016). Enhanced photo‐bioelectrochemical energy conversion by genetically engineered Cyanobacteria. Biotechnology and Bioengineering, 113, 675–679.
Shi, L., Dong, H., Reguera, G., Beyenal, H., Lu, A., Liu, J., Yu, H. Q., & Fredrickson, J. K. (2016). Extracellular electron transfer mechanisms between microorganisms and minerals. Nature Reviews Microbiology, 14, 651–662.
Smith, A. F., Liu, X., Woodard, T. L., Fu, T., Emrick, T., Jiménez, J. M., Lovley, D. R., & Yao, J. (2020). Bioelectronic protein nanowire sensors for ammonia detection. Nano Research, 13, 1479–1484.
Smith, J. A., Holmes, D. E., Woodard, T. L., Li, Y., Liu, X., Wang, L.‐Y., Meier, D., Schwarz, I. A., & Lovley, D. R. (2023). Detrimental impact of the Geobacter metallireducens type VI secretion system on direct interspecies electron transfer. Microbiology Spectrum, 11, e00941–00923.
Smith, J. A., Tremblay, P.‐L., Shrestha, P. M., Snoeyenbos‐West, O. L., Franks, A. E., Nevin, K. P., & Lovley, D. R. (2014). Going wireless: Fe(III) oxide reduction without pili by Geobacter sulfurreducens strain JS‐1. Applied and Environmental Microbiology, 80, 4331–4340.
Steidl, R. J., Lampa‐Pastirk, S., & Reguera, G. (2016). Mechanistic stratification in electroactive biofilms of Geobacter sulfurreducens mediated by pilus nanowires. Nature Communications, 7, 12217.
Szmuc, E., Walker, D. J. F., Kireev, D., Akinwande, D., Lovley, D. R., Keitz, B., & Ellington, A. (2023). Engineering geobacter pili to produce metal: Organic filaments. Biosensors and Bioelectronics, 222, 114993.
Thomas, P. E., Ryan, D., & Levin, W. (1976). An improved staining procedure for the detection of the peroxidase activity of cytochrome P‐450 on sodium dodecyl sulfate polyacrylamide gels. Analytical Biochemistry, 75, 168–176.
Tremblay, P.‐L., Summers, Z. M., Glaven, R. H., Nevin, K. P., Zengler, K., Barrett, C. L., Qiu, Y., Palsson, B. O., & Lovley, D. R. (2011). A c‐type cytochrome and a transcriptional regulator responsible for enhanced extracellular electron transfer in Geobacter sulfurreducens revealed by adaptive evolution. Environmental Microbiology, 13, 13–23.
Ueki, T., Walker, D. J. F., Woodard, T. L., Nevin, K. P., Nonnenmann, S. S., & Lovley, D. R. (2020). An Escherichia coli chassis for production of electrically conductive protein nanowires. ACS Synthetic Biology, 9, 647–654.
Vargas, M., Malvankar, N. S., Tremblay, P.‐L., Leang, C., Smith, J. A., Patel, P., Snoeyenbos‐West, O., Nevin, K. P., & Lovley, D. R. (2013). Aromatic amino acids required for pili conductivity and long‐range extracellular electron transport in Geobacter sulfurreducens. mBio, 4, e00105–e00113.
Wang, F., Chan, C. H., Suciu, V., Mustafa, K., Ammend, M., Si, D., Hochbaum, A. I., Egelman, E. H., & Bond, D. R. (2022). Structure of geobacter OmcZ filaments suggests extracellular cytochrome polymers evolved independently multiple times. eLife, 11, e8155.
Wang, F., Gu, Y., O'Brien, J. P., Yi, S. M., Yalcin, S. E., Srikanth, V., Shen, C., Vu, D., Ing, N. L., Hochbaum, A. I., Egelman, E. H., & Malvankar, N. S. (2019). Structure of microbial nanowires reveals stacked hemes that transport electrons over micrometers. Cell, 177, 361–369.e10.
Wang, F., Mustafa, K., Suciu, V., Joshi, K., Chan, C. H., Choi, S., Su, Z., Si, D., Hochbaum, A. I., Egelman, E. H., & Bond, D. R. (2022). Cryo‐EM structure of an extracellular geobacter OmcE cytochrome filament reveals tetrahaem packing. Nature Microbiology, 7, 1291–1300.
Yalcin, S. E., O'Brien, J. P., Gu, Y., Reiss, K., Yi, S. M., Jain, R., Srikanth, V., Dahl, P. J., Huynh, W., Vu, D., Acharya, A., Chaudhuri, S., Varga, T., Batista, V. S., & Malvankar, N. S. (2020). Electric field stimulates production of highly conductive microbial OmcZ nanowires. Nature Chemical Biology, 16, 1136–1142.
Yang, Y., Ding, Y., Hu, Y., Cao, B., Rice, S. A., Kjelleberg, S., & Song, H. (2015). Enhancing bidirectional electron transfer of shewanella oneidensis by a synthetic flavin pathway. ACS Synthetic Biology, 4, 815–823.