A survey of the Desulfuromonadia "cytochromome" provides a glimpse of the unexplored diversity of multiheme cytochromes in nature.
Desulfuromonadia
Heme-binding motifs
Multiheme cytochromes
Nanowire
Pangenome
Protein diversity
Protein structure prediction
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
20 Oct 2024
20 Oct 2024
Historique:
received:
30
01
2024
accepted:
07
10
2024
medline:
21
10
2024
pubmed:
21
10
2024
entrez:
20
10
2024
Statut:
epublish
Résumé
Multiheme cytochromes c (MHC) provide prokaryotes with a broad metabolic versatility that contributes to their role in the biogeochemical cycling of the elements and in energy production in bioelectrochemical systems. However, MHC have only been isolated and studied in detail from a limited number of species. Among these, Desulfuromonadia spp. are particularly MHC-rich. To obtain a broad view of the diversity of MHC, we employed bioinformatic tools to study the cytochromome encoded in the genomes of the Desulfuromonadia class. We found that the distribution of the MHC families follows a different pattern between the two orders of the Desulfuromonadia class and that there is great diversity in the number of heme-binding motifs in MHC. However, the vast majority of MHC have up to 12 heme-binding motifs. MHC predicted to be extracellular are the least conserved and show high diversity, whereas inner membrane MHC are well conserved and show lower diversity. Although the most prevalent MHC have homologues already characterized, nearly half of the MHC families in the Desulforomonadia class have no known characterized homologues. AlphaFold2 was employed to predict their 3D structures. This provides an atlas of novel MHC, including examples with high beta-sheet content and nanowire MHC with unprecedented high numbers of putative heme cofactors per polypeptide. This work illuminates for the first time the universe of experimentally uncharacterized cytochromes that are likely to contribute to the metabolic versatility and to the fitness of Desulfuromonadia in diverse environmental conditions and to drive biotechnological applications of these organisms.
Sections du résumé
BACKGROUND
BACKGROUND
Multiheme cytochromes c (MHC) provide prokaryotes with a broad metabolic versatility that contributes to their role in the biogeochemical cycling of the elements and in energy production in bioelectrochemical systems. However, MHC have only been isolated and studied in detail from a limited number of species. Among these, Desulfuromonadia spp. are particularly MHC-rich. To obtain a broad view of the diversity of MHC, we employed bioinformatic tools to study the cytochromome encoded in the genomes of the Desulfuromonadia class.
RESULTS
RESULTS
We found that the distribution of the MHC families follows a different pattern between the two orders of the Desulfuromonadia class and that there is great diversity in the number of heme-binding motifs in MHC. However, the vast majority of MHC have up to 12 heme-binding motifs. MHC predicted to be extracellular are the least conserved and show high diversity, whereas inner membrane MHC are well conserved and show lower diversity. Although the most prevalent MHC have homologues already characterized, nearly half of the MHC families in the Desulforomonadia class have no known characterized homologues. AlphaFold2 was employed to predict their 3D structures. This provides an atlas of novel MHC, including examples with high beta-sheet content and nanowire MHC with unprecedented high numbers of putative heme cofactors per polypeptide.
CONCLUSIONS
CONCLUSIONS
This work illuminates for the first time the universe of experimentally uncharacterized cytochromes that are likely to contribute to the metabolic versatility and to the fitness of Desulfuromonadia in diverse environmental conditions and to drive biotechnological applications of these organisms.
Identifiants
pubmed: 39428470
doi: 10.1186/s12864-024-10872-4
pii: 10.1186/s12864-024-10872-4
doi:
Substances chimiques
Heme
42VZT0U6YR
Cytochromes c
9007-43-6
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
982Subventions
Organisme : Fundação para a Ciência e a Tecnologia
ID : PTDC/BIA-BQM/4143/2021
Informations de copyright
© 2024. The Author(s).
Références
Bird LJ, Bonnefoy V, Newman DK. Bioenergetic challenges of microbial iron metabolisms. Trends Microbiol. 2011;19:330–40.
pubmed: 21664821
doi: 10.1016/j.tim.2011.05.001
Paquete CM, Rusconi G, Silva AV, Soares R, Louro RO. A brief survey of the cytochromome. Adv Microb Physiol. 2019;75:69–135.
pubmed: 31655743
doi: 10.1016/bs.ampbs.2019.07.005
Daltrop O, Allen JWA, Willis AC, Ferguson SJ. In vitro formation of a c-type cytochrome. Proc Natl Acad Sci U S A. 2002;99:7872–6.
pubmed: 12060734
pmcid: 122987
doi: 10.1073/pnas.132259099
Ferousi C, Lindhoud S, Baymann F, Hester ER, Reimann J, Kartal B. Discovery of a functional, contracted heme-binding motif within a multiheme cytochrome. J Biol Chem. 2019;294:16953–65.
pubmed: 31582564
pmcid: 6851341
doi: 10.1074/jbc.RA119.010568
Einsle O, Messerschmidt A, Stach P, Bourenkov GP, Bartunik HD, Huber R, et al. Structure of cytochrome c nitrite reductase. Nature. 1999;400:476–80.
pubmed: 10440380
doi: 10.1038/22802
Aragão D, Frazão C, Sieker L, Sheldrick GM, LeGall J, Carrondo MA. Structure of dimeric cytochrome c
pubmed: 12657783
doi: 10.1107/S090744490300194X
Czjzek M, Guerlesquin F, Bruschi M, Haser R. Crystal structure of a dimeric octaheme cytochrome c
pubmed: 8740362
doi: 10.1016/S0969-2126(96)00045-7
Hermann B, Kern M, La Pietra L, Simon J, Einsle O. The octahaem MccA is a haem c-copper sulfite reductase. Nature. 2015;520:706–9.
pubmed: 25642962
doi: 10.1038/nature14109
Soares R, Costa NL, Paquete CM, Andreini C, Louro RO. A new paradigm of Multiheme Cytochrome evolution by Grafting and pruning protein modules. Mol Biol Evol. 2022;39:msac139.
pubmed: 35714268
pmcid: 9250108
doi: 10.1093/molbev/msac139
Akram M, Dietl A, Mersdorf U, Prinz S, Maalcke W, Keltjens J, et al. A 192-heme electron transfer network in the hydrazine dehydrogenase complex. Sci Adv. 2019;5:eaav4310.
pubmed: 31001586
pmcid: 6469936
doi: 10.1126/sciadv.aav4310
Gu Y, Guberman-Pfeffer MJ, Srikanth V, Shen C, Giska F, Gupta K, et al. Structure of Geobacter cytochrome OmcZ identifies mechanism of nanowire assembly and conductivity. Nat Microbiol. 2023;8:284–98.
pubmed: 36732469
pmcid: 9999484
doi: 10.1038/s41564-022-01315-5
Wang F, Mustafa K, Suciu V, Joshi K, Chan CH, Choi S, et al. Cryo-EM structure of an extracellular Geobacter OmcE cytochrome filament reveals tetrahaem packing. Nat Microbiol. 2022;7:1291–300.
pubmed: 35798889
pmcid: 9357133
doi: 10.1038/s41564-022-01159-z
Wang F, Gu Y, O’Brien JP, Yi SM, Yalcin SE, Srikanth V, et al. Structure of Microbial Nanowires reveals stacked hemes that Transport Electrons over Micrometers. Cell. 2019;177:361–e36910.
pubmed: 30951668
pmcid: 6720112
doi: 10.1016/j.cell.2019.03.029
Baquero DP, Cvirkaite-Krupovic V, Hu SS, Fields JL, Liu X, Rensing C, et al. Extracellular cytochrome nanowires appear to be ubiquitous in prokaryotes. Cell. 2023;186:2853–e28648.
pubmed: 37290436
pmcid: 10330847
doi: 10.1016/j.cell.2023.05.012
Carpenter JM, Zhong F, Ragusa MJ, Louro RO, Hogan DA, Pletneva EV. Structure and redox properties of the diheme electron carrier cytochrome c
pubmed: 31707335
doi: 10.1016/j.jinorgbio.2019.110889
Matias PM, Coelho AV, Valente FMA, Plácido D, LeGall J, Xavier AV, et al. Sulfate respiration in Desulfovibrio vulgaris Hildenborough. Structure of the 16-heme cytochrome c HmcA AT 2.5-A resolution and a view of its role in transmembrane electron transfer. J Biol Chem. 2002;277:47907–16.
pubmed: 12356749
doi: 10.1074/jbc.M207465200
Leu AO, Cai C, McIlroy SJ, Southam G, Orphan VJ, Yuan Z, et al. Anaerobic methane oxidation coupled to manganese reduction by members of the Methanoperedenaceae. ISME J. 2020;14:1030–41.
pubmed: 31988473
pmcid: 7082337
doi: 10.1038/s41396-020-0590-x
Klotz MG, Schmid MC, Strous M, op den Camp HJM, Jetten MSM, Hooper AB. Evolution of an octahaem cytochrome c protein family that is key to aerobic and anaerobic ammonia oxidation by bacteria. Environ Microbiol. 2008;10:3150–63.
pubmed: 18761666
doi: 10.1111/j.1462-2920.2008.01733.x
Edwards MJ, White GF, Butt JN, Richardson DJ, Clarke TA. The Crystal structure of a Biological Insulated Transmembrane Molecular Wire. Cell. 2020;181:665–e67310.
pubmed: 32289252
pmcid: 7198977
doi: 10.1016/j.cell.2020.03.032
Costa NL, Hermann B, Fourmond V, Faustino MM, Teixeira M, Einsle O et al. How thermophilic gram-positive organisms perform Extracellular Electron transfer: characterization of the cell surface terminal reductase OcwA. mBio. 2019;10.
Sharma S, Cavallaro G, Rosato A. A systematic investigation of multiheme c-type cytochromes in prokaryotes. J Biol Inorg Chem. 2010;15:559–71.
pubmed: 20084531
doi: 10.1007/s00775-010-0623-4
Londer YY, Giuliani SE, Peppler T, Collart FR. Addressing Shewanella oneidensis cytochromome: the first step towards high-throughput expression of cytochromes c. Protein Expr Purif. 2008;62:128–37.
pubmed: 18657620
doi: 10.1016/j.pep.2008.06.014
Waite DW, Chuvochina M, Pelikan C, Parks DH, Yilmaz P, Wagner M, et al. Proposal to reclassify the proteobacterial classes Deltaproteobacteria and Oligoflexia, and the phylum Thermodesulfobacteria into four phyla reflecting major functional capabilities. Int J Syst Evol Microbiol. 2020;70:5972–6016.
pubmed: 33151140
doi: 10.1099/ijsem.0.004213
Badalamenti JP, Summers ZM, Chan CH, Gralnick JA, Bond DR. Isolation and genomic characterization of ‘Desulfuromonas Soudanensis WTL’, a metal- and electrode-respiring bacterium from Anoxic Deep Subsurface Brine. Front Microbiol. 2016;7:913.
pubmed: 27445996
pmcid: 4914508
doi: 10.3389/fmicb.2016.00913
Xie L, Yoshida N, Ishii S, Meng L. Isolation and polyphasic characterization of Desulfuromonas Versatilis sp. Nov., an Electrogenic Bacteria Capable of versatile metabolism isolated from a Graphene Oxide-reducing Enrichment Culture. Microorganisms. 2021;9:1953.
pubmed: 34576847
pmcid: 8465243
doi: 10.3390/microorganisms9091953
Roden EE, Lovley DR. Dissimilatory Fe(III) reduction by the Marine Microorganism Desulfuromonas acetoxidans. Appl Environ Microbiol. 1993;59:734–42.
pubmed: 16348888
pmcid: 202183
doi: 10.1128/aem.59.3.734-742.1993
Rossi R, Logan BE. Using an anion exchange membrane for effective hydroxide ion transport enables high power densities in microbial fuel cells. Chem Eng J. 2021;422:130150.
doi: 10.1016/j.cej.2021.130150
Fonseca B, Soares R, Paquete CM, Louro RO. Chapter 8: bacterial power: an Alternative Energy source. In: Moura JJG, Moura I, Maia LB, editors. Enzymes for solving Humankind’s problems. Springer International Publishing; 2020. pp. 1–32.
Huang L, Tang J, Chen M, Liu X, Zhou S. Two modes of riboflavin-mediated Extracellular Electron transfer in Geobacter uraniireducens. Front Microbiol. 2018;9:2886.
pubmed: 30538691
pmcid: 6277576
doi: 10.3389/fmicb.2018.02886
Portela PC, Fernandes TM, Dantas JM, Ferreira MR, Salgueiro CA. Biochemical and functional insights on the triheme cytochrome PpcA from Geobacter metallireducens. Arch Biochem Biophys. 2018;644:8–16.
pubmed: 29486160
doi: 10.1016/j.abb.2018.02.017
Rotaru A-E, Woodard TL, Nevin KP, Lovley DR. Link between capacity for current production and syntrophic growth in Geobacter species. Front Microbiol. 2015;6:744.
pubmed: 26284037
pmcid: 4523033
doi: 10.3389/fmicb.2015.00744
Czjzek M, Haser R, Shepard W. Structure of cytochrome c
doi: 10.1107/S0907444901003481
Correia IJ, Paquete CM, Louro RO, Catarino T, Turner DL, Xavier AV. Thermodynamic and kinetic characterization of trihaem cytochrome c
pubmed: 12423372
doi: 10.1046/j.1432-1033.2002.03286.x
Alves A, Ly HK, Hildebrandt P, Louro RO, Millo D. Nature of the surface-exposed cytochrome-electrode interactions in Electroactive biofilms of Desulfuromonas acetoxidans. J Phys Chem B. 2015;119:7968–74.
pubmed: 26039558
doi: 10.1021/acs.jpcb.5b03419
Carmona-Martínez AA, Pierra M, Trably E, Bernet N. High current density via direct electron transfer by the halophilic anode respiring bacterium Geoalkalibacter subterraneus. Phys Chem Chem Phys. 2013;15:19699–707.
pubmed: 24135891
doi: 10.1039/c3cp54045f
Yadav S, Singh R, Sundharam SS, Chaudhary S, Krishnamurthi S, Patil SA. Geoalkalibacter halelectricus SAP-1 sp. nov. possessing extracellular electron transfer and mineral-reducing capabilities from a haloalkaline environment. Environ Microbiol. 2022;24:5066–81.
pubmed: 36066180
doi: 10.1111/1462-2920.16200
Pokkuluri PR, Londer YY, Duke NEC, Pessanha M, Yang X, Orshonsky V, et al. Structure of a novel dodecaheme cytochrome c from Geobacter sulfurreducens reveals an extended 12 nm protein with interacting hemes. J Struct Biol. 2011;174:223–33.
pubmed: 21130881
doi: 10.1016/j.jsb.2010.11.022
Butler JE, Young ND, Lovley DR. Evolution from a respiratory ancestor to fill syntrophic and fermentative niches: comparative genomics of six Geobacteraceae species. BMC Genomics. 2009;10:103.
pubmed: 19284579
pmcid: 2669807
doi: 10.1186/1471-2164-10-103
Baesman SM, Sutton JM, Fierst JL, Akob DM, Oremland RS. Syntrophotalea acetylenivorans sp. nov., a diazotrophic, acetylenotrophic anaerobe isolated from intertidal sediments. Int J Syst Evol Microbiol. 2021;71:004698.
pmcid: 8375424
Dehning I, Schink B. Malonomonas rubra gen. nov. sp. nov., a microaerotolerant anaerobic bacterium growing by decarboxylation of malonate. Arch Microbiol. 1989;151:427–33.
doi: 10.1007/BF00416602
Schink B. Fermentation of 2,3-butanediol by Pelobacter carbinolicus sp. nov. and Pelobacter propionicus sp. nov., and evidence for propionate formation from C2 compounds. Arch Microbiol. 1984;137:33–41.
Sung Y, Fletcher KE, Ritalahti KM, Apkarian RP, Ramos-Hernández N, Sanford RA, et al. Geobacter lovleyi sp. nov. Strain SZ, a Novel reducingducintetrachloroetheneedechlorinatingnbacteriumterium. Appl Environ Microbiol. 2006;72:2775–82.
pubmed: 16597982
pmcid: 1448980
doi: 10.1128/AEM.72.4.2775-2782.2006
De Wever H, Cole JR, Fettig MR, Hogan DA, Tiedje JM. Reductive dehalogenation of trichloroacetic acid by Trichlorobacter thiogenes gen. nov., sp. nov. Appl Environ Microbiol. 2000;66:2297–301.
pubmed: 10831402
pmcid: 110515
doi: 10.1128/AEM.66.6.2297-2301.2000
Ohtsuka T, Yamaguchi N, Makino T, Sakurai K, Kimura K, Kudo K, et al. Arsenic Dissolution from Japanese Paddy Soil by a dissimilatory arsenate-reducing bacterium Geobacter sp. OR-1. Environ Sci Technol. 2013;47:6263–71.
pubmed: 23668621
doi: 10.1021/es400231x
Straub KL, Buchholz-Cleven BE. Geobacter bremensis sp. nov. and Geobacter pelophilus sp. nov., two dissimilatory ferric-iron-reducing bacteria. Int J Syst Evol Microbiol. 2001;51:1805–8.
pubmed: 11594612
doi: 10.1099/00207713-51-5-1805
Sousa JS, Calisto F, Langer JD, Mills DJ, Refojo PN, Teixeira M, et al. Structural basis for energy transduction by respiratory alternative complex III. Nat Commun. 2018;9:1728.
pubmed: 29712914
pmcid: 5928083
doi: 10.1038/s41467-018-04141-8
Joshi K, Chan CH, Bond DR. Geobacter sulfurreducens inner membrane cytochrome CbcBA controls electron transfer and growth yield near the energetic limit of respiration. Mol Microbiol. 2021;116:1124–39.
pubmed: 34423503
doi: 10.1111/mmi.14801
Antunes JMA, Silva MA, Salgueiro CA, Morgado L. Electron Flow from the inner membrane towards the Cell Exterior in Geobacter sulfurreducens: biochemical characterization of cytochrome CbcL. Front Microbiol. 2022;13.
Aklujkar M, Coppi MV, Leang C, Kim BC, Chavan MA, Perpetua LA, et al. Proteins involved in electron transfer to Fe(III) and mn(IV) oxides by Geobacter sulfurreducens and Geobacter uraniireducens. Microbiol (Reading). 2013;159:515–35.
doi: 10.1099/mic.0.064089-0
Rodrigues ML, Scott KA, Sansom MSP, Pereira IAC, Archer M. Quinol Oxidation by c-Type cytochromes: structural characterization of the Menaquinol binding site of NrfHA. J Mol Biol. 2008;381:341–50.
pubmed: 18597779
doi: 10.1016/j.jmb.2008.05.066
Pimenta AI, Paquete CM, Morgado L, Edwards MJ, Clarke TA, Salgueiro CA, et al. Characterization of the inner membrane cytochrome ImcH from Geobacter reveals its importance for extracellular electron transfer and energy conservation. Protein Sci. 2023;32:e4796.
pubmed: 37779214
doi: 10.1002/pro.4796
Rizzolo K, Cohen SE, Weitz AC, López Muñoz MM, Hendrich MP, Drennan CL, et al. A widely distributed diheme enzyme from Burkholderia that displays an atypically stable bis-Fe(IV) state. Nat Commun. 2019;10:1101.
pubmed: 30846684
pmcid: 6405878
doi: 10.1038/s41467-019-09020-4
Messias AC, Kastrau DH, Costa HS, LeGall J, Turner DL, Santos H, et al. Solution structure of Desulfovibrio vulgaris (Hildenborough) ferrocytochrome c
pubmed: 9710542
doi: 10.1006/jmbi.1998.1974
Assfalg M, Banci L, Bertini I, Bruschi M, Turano P. 800 MHz 1H NMR solution structure refinement of oxidized cytochrome c
pubmed: 9760163
doi: 10.1046/j.1432-1327.1998.2560261.x
Heitmann D, Einsle O. Structural and biochemical characterization of DHC2, a novel diheme cytochrome c from Geobacter sulfurreducens. Biochemistry. 2005;44:12411–9.
pubmed: 16156654
doi: 10.1021/bi0509999
Grein F, Venceslau SS, Schneider L, Hildebrandt P, Todorovic S, Pereira IAC, et al. DsrJ, an essential part of the DsrMKJOP Transmembrane Complex in the Purple Sulfur Bacterium Allochromatium vinosum, is an unusual triheme cytochrome c. Biochemistry. 2010;49:8290–9.
pubmed: 20726534
doi: 10.1021/bi1007673
Taylor P, Pealing SL, Reid GA, Chapman SK, Walkinshaw MD. Structural and mechanistic mapping of a unique fumarate reductase. Nat Struct Biol. 1999;6:1108–12.
pubmed: 10581550
doi: 10.1038/70045
Fernandes TM, Folgosa F, Teixeira M, Salgueiro CA, Morgado L. Structural and functional insights of GSU0105, a unique multiheme cytochrome from G. sulfurreducens. Biophys J. 2021;120:5395–407.
pubmed: 34688593
pmcid: 8715191
doi: 10.1016/j.bpj.2021.10.023
Shelobolina ES, Coppi MV, Korenevsky AA, DiDonato LN, Sullivan SA, Konishi H, et al. Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens. BMC Microbiol. 2007;7:16.
pubmed: 17346345
pmcid: 1829397
doi: 10.1186/1471-2180-7-16
Maalcke WJ, Dietl A, Marritt SJ, Butt JN, Jetten MSM, Keltjens JT, et al. Structural basis of biological NO generation by octaheme oxidoreductases. J Biol Chem. 2014;289:1228–42.
pubmed: 24302732
doi: 10.1074/jbc.M113.525147
Parey K, Fielding AJ, Sörgel M, Rachel R, Huber H, Ziegler C, et al. In meso crystal structure of a novel membrane-associated octaheme cytochrome c from the Crenarchaeon Ignicoccus hospitalis. FEBS J. 2016;283:3807–20.
pubmed: 27586496
doi: 10.1111/febs.13870
Mowat CG, Rothery E, Miles CS, McIver L, Doherty MK, Drewette K, et al. Octaheme tetrathionate reductase is a respiratory enzyme with novel heme ligation. Nat Struct Mol Biol. 2004;11:1023–4.
pubmed: 15361860
doi: 10.1038/nsmb827
Datta S, Ikeda T, Kano K, Mathews FS. Structure of the phenylhydrazine adduct of the quinohemoprotein amine dehydrogenase from Paracoccus denitrificans at 1.7 a resolution. Acta Crystallogr D Biol Crystallogr. 2003;59:1551–6.
pubmed: 12925784
doi: 10.1107/S090744490301429X
De March M, Di Rocco G, Hickey N, Geremia S. High-resolution crystal structure of the recombinant diheme cytochrome c from Shewanella baltica (OS155). J Biomol Struct Dyn. 2015;33:395–403.
pubmed: 24559494
doi: 10.1080/07391102.2014.880657
Abreu IA, Lourenço AI, Xavier AV, LeGall J, Coelho AV, Matias PM, et al. A novel iron centre in the split-soret cytochrome c from Desulfovibrio desulfuricans ATCC 27774. J Biol Inorg Chem. 2003;8:360–70.
pubmed: 12589573
doi: 10.1007/s00775-002-0426-3
Fonseca BM, Silva L, Trindade IB, Moe E, Matias PM, Louro RO et al. Optimizing Electroactive organisms: the Effect of Orthologous proteins. Front Energy Res. 2019;7.
Jiménez Otero F, Chan CH, Bond DR. Identification of different putative outer membrane Electron conduits necessary for Fe(III) citrate, Fe(III) Oxide, Mn(IV) Oxide, or Electrode Reduction by Geobacter sulfurreducens. J Bacteriol. 2018;200:e00347–18.
pubmed: 30038047
pmcid: 6148476
doi: 10.1128/JB.00347-18
Liu Y, Fredrickson JK, Zachara JM, Shi L. Direct involvement of ombB, omaB, and omcB genes in extracellular reduction of Fe(III) by Geobacter sulfurreducens PCA. Front Microbiol. 2015;6:1075.
pubmed: 26483786
pmcid: 4589669
doi: 10.3389/fmicb.2015.01075
Leang C, Coppi MV, Lovley DR. OmcB, a c-Type polyheme cytochrome, involved in Fe(III) reduction in Geobacter sulfurreducens. J Bacteriol. 2003;185:2096–103.
pubmed: 12644478
pmcid: 151516
doi: 10.1128/JB.185.7.2096-2103.2003
Kim B-C, Qian X, Leang C, Coppi MV, Lovley DR. Two putative c-type multiheme cytochromes required for the expression of OmcB, an outer membrane protein essential for optimal Fe(III) reduction in Geobacter sulfurreducens. J Bacteriol. 2006;188:3138–42.
pubmed: 16585776
pmcid: 1447008
doi: 10.1128/JB.188.8.3138-3142.2006
Fernandes TM, Silva MA, Morgado L, Salgueiro CA. Hemes on a string: insights on the functional mechanisms of PgcA from Geobacter sulfurreducens. J Biol Chem. 2023;299.
Ding Y-HR, Hixson KK, Aklujkar MA, Lipton MS, Smith RD, Lovley DR, et al. Proteome of Geobacter sulfurreducens grown with Fe(III) oxide or fe(III) citrate as the electron acceptor. Biochim et Biophys Acta (BBA) - Proteins Proteom. 2008;1784:1935–41.
doi: 10.1016/j.bbapap.2008.06.011
Morgado L, Bruix M, Pessanha M, Londer YY, Salgueiro CA. Thermodynamic characterization of a Triheme Cytochrome Family from Geobacter sulfurreducens reveals mechanistic and functional diversity. Biophys J. 2010;99:293–301.
pubmed: 20655858
pmcid: 2895378
doi: 10.1016/j.bpj.2010.04.017
Richardson DJ, Butt JN, Fredrickson JK, Zachara JM, Shi L, Edwards MJ, et al. The porin-cytochrome model for microbe-to-mineral electron transfer. Mol Microbiol. 2012;85:201–12.
pubmed: 22646977
doi: 10.1111/j.1365-2958.2012.08088.x
Locher KP. Mechanistic diversity in ATP-binding cassette (ABC) transporters. Nat Struct Mol Biol. 2016;23:487–93.
pubmed: 27273632
doi: 10.1038/nsmb.3216
Zhong C, Han M, Yu S, Yang P, Li H, Ning K. Pan-genome analyses of 24 Shewanella strains re-emphasize the diversification of their functions yet evolutionary dynamics of metal-reducing pathway. Biotechnol Biofuels. 2018;11:193.
pubmed: 30026808
pmcid: 6048853
doi: 10.1186/s13068-018-1201-1
Butler JE, Young ND, Lovley DR. Evolution of electron transfer out of the cell: comparative genomics of six Geobacter genomes. BMC Genomics. 2010;11:40.
pubmed: 20078895
pmcid: 2825233
doi: 10.1186/1471-2164-11-40
Butler JE, Young ND, Aklujkar M, Lovley DR. Comparative genomic analysis of Geobacter sulfurreducens KN400, a strain with enhanced capacity for extracellular electron transfer and electricity production. BMC Genomics. 2012;13:471.
pubmed: 22967216
pmcid: 3495685
doi: 10.1186/1471-2164-13-471
Fonseca BM, Paquete CM, Neto SE, Pacheco I, Soares CM, Louro RO. Mind the gap: cytochrome interactions reveal electron pathways across the periplasm of Shewanella oneidensis MR-1. Biochem J. 2013;449:101–8.
pubmed: 23067389
doi: 10.1042/BJ20121467
Howley E, Krajmalnik-Brown R, Torres CI. Cytochrome gene expression shifts in Geobacter sulfurreducens to maximize energy conservation in response to changes in redox conditions. Biosens Bioelectron. 2023;237:115524.
pubmed: 37459687
doi: 10.1016/j.bios.2023.115524
Levar CE, Hoffman CL, Dunshee AJ, Toner BM, Bond DR. Redox potential as a master variable controlling pathways of metal reduction by Geobacter sulfurreducens. ISME J. 2017;11:741–52.
pubmed: 28045456
pmcid: 5322298
doi: 10.1038/ismej.2016.146
Deng X, Dohmae N, Nealson KH, Hashimoto K, Okamoto A. Multi-heme cytochromes provide a pathway for survival in energy-limited environments. Sci Adv. 2018;4.
Firer-Sherwood MA, Bewley KD, Mock J-Y, Elliott SJ. Tools for resolving complexity in the electron transfer networks of multiheme cytochromes c. Metallomics. 2011;3:344–8.
pubmed: 21327265
doi: 10.1039/c0mt00097c
Schuetz B, Schicklberger M, Kuermann J, Spormann AM, Gescher J. Periplasmic electron transfer via the c-type cytochromes MtrA and FccA of Shewanella oneidensis MR-1. Appl Environ Microbiol. 2009;75:7789–96.
pubmed: 19837833
pmcid: 2794085
doi: 10.1128/AEM.01834-09
Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;596:583–9.
pubmed: 34265844
pmcid: 8371605
doi: 10.1038/s41586-021-03819-2
Page CC, Moser CC, Dutton PL. Mechanism for electron transfer within and between proteins. Curr Opin Chem Biol. 2003;7:551–6.
pubmed: 14580557
doi: 10.1016/j.cbpa.2003.08.005
Seltmann G, Holst O. Periplasmic Space and rigid layer. In: Seltmann G, Holst O, editors. The bacterial cell wall. Berlin, Heidelberg: Springer; 2002. pp. 103–32.
doi: 10.1007/978-3-662-04878-8_3
Morgado L, Fernandes AP, Londer YY, Pokkuluri PR, Schiffer M, Salgueiro CA. Thermodynamic characterization of the redox centres in a representative domain of a novel c-type multihaem cytochrome. Biochem J. 2009;420:485–92.
pubmed: 19351328
doi: 10.1042/BJ20082428
Dohnalkova AC, Marshall MJ, Arey BW, Williams KH, Buck EC, Fredrickson JK. Imaging Hydrated Microbial Extracellular polymers: comparative analysis by Electron Microscopy. Appl Environ Microbiol. 2011;77:1254–62.
pubmed: 21169451
doi: 10.1128/AEM.02001-10
Lower BH, Lins RD, Oestreicher Z, Straatsma TP, Hochella MF, Shi L, et al. In vitro evolution of a peptide with a hematite binding motif that may constitute a natural metal-oxide binding archetype. Environ Sci Technol. 2008;42:3821–7.
pubmed: 18546729
doi: 10.1021/es702688c
Edwards MJ, Baiden NA, Johs A, Tomanicek SJ, Liang L, Shi L, et al. The X-ray crystal structure of Shewanella oneidensis OmcA reveals new insight at the microbe–mineral interface. FEBS Lett. 2014;588:1886–90.
pubmed: 24747425
doi: 10.1016/j.febslet.2014.04.013
Myers JM, Myers CR. Isolation and sequence of omcA, a gene encoding a decaheme outer membrane cytochrome c of Shewanella putrefaciens MR-1, and detection of omcA homologs in other strains of S. putrefaciens. Biochim Biophys Acta. 1998;1373:237–51.
pubmed: 9733973
doi: 10.1016/S0005-2736(98)00111-4
Baker IR, Conley BE, Gralnick JA, Girguis PR. Evidence for Horizontal and Vertical transmission of mtr-mediated Extracellular Electron transfer among the Bacteria. mBio. 2022;:e0290421.
Nakahara Y, Kimura K, Inokuchi H, Yagi T. Electrical conductivity of an anhydrous cytochrome c
doi: 10.1016/0009-2614(80)85195-5
Wu L, Liu H, Xu Y, Nie Y. Entering an era of protein structuromics. Biochemistry. 2023;62:3167–9.
pubmed: 37950690
doi: 10.1021/acs.biochem.3c00547
Illergård K, Ardell DH, Elofsson A. Structure is three to ten times more conserved than sequence–a study of structural response in protein cores. Proteins. 2009;77:499–508.
pubmed: 19507241
doi: 10.1002/prot.22458
Ingles-Prieto A, Ibarra-Molero B, Delgado-Delgado A, Perez-Jimenez R, Fernandez JM, Gaucher EA, et al. Conservation of protein structure over four billion years. Structure. 2013;21:1690–7.
pubmed: 23932589
pmcid: 3774310
doi: 10.1016/j.str.2013.06.020
Chothia C, Lesk AM. The relation between the divergence of sequence and structure in proteins. EMBO J. 1986;5:823–6.
pubmed: 3709526
pmcid: 1166865
doi: 10.1002/j.1460-2075.1986.tb04288.x
O’Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, McVeigh R, et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 2016;44:D733–745.
pubmed: 26553804
doi: 10.1093/nar/gkv1189
Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, et al. InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014;30:1236–40.
pubmed: 24451626
pmcid: 3998142
doi: 10.1093/bioinformatics/btu031
Spitzer M, Wildenhain J, Rappsilber J, Tyers M. BoxPlotR: a web tool for generation of box plots. Nat Methods. 2014;11:121–2.
pubmed: 24481215
pmcid: 3930876
doi: 10.1038/nmeth.2811
Yu NY, Wagner JR, Laird MR, Melli G, Rey S, Lo R, et al. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics. 2010;26:1608–15.
pubmed: 20472543
pmcid: 2887053
doi: 10.1093/bioinformatics/btq249
Walker JM, editor. The Proteomics protocols Handbook. Totowa, NJ: Humana; 2005.
Tatusova TA, Madden TL. BLAST 2 sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol Lett. 1999;174:247–50.
pubmed: 10339815
doi: 10.1111/j.1574-6968.1999.tb13575.x
Steinegger M, Söding J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat Biotechnol. 2017;35:1026–8.
pubmed: 29035372
doi: 10.1038/nbt.3988
Chung SY, Subbiah S. A structural explanation for the twilight zone of protein sequence homology. Structure. 1996;4:1123–7.
pubmed: 8939745
doi: 10.1016/S0969-2126(96)00119-0
Punetha A, Sarkar P, Nimkar S, Sharma H, KNR Y, Nagaraj S. Structural Bioinformatics: Life through the 3D glasses. In: Shanker A, editor. Bioinformatics: sequences, structures, phylogeny. Singapore: Springer; 2018. pp. 191–253.
doi: 10.1007/978-981-13-1562-6_10
Cianfrocco MA, Wong-Barnum M, Youn C, Wagner R, Leschziner A. COSMIC2: A Science Gateway for Cryo-Electron Microscopy Structure Determination. In: Proceedings of the Practice and Experience in Advanced Research Computing 2017 on Sustainability, Success and Impact. New York, NY, USA: Association for Computing Machinery; 2017. pp. 1–5.
Varadi M, Anyango S, Deshpande M, Nair S, Natassia C, Yordanova G, et al. AlphaFold protein structure database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res. 2022;50:D439–44.
pubmed: 34791371
doi: 10.1093/nar/gkab1061
Almagro Armenteros JJ, Tsirigos KD, Sønderby CK, Petersen TN, Winther O, Brunak S, et al. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol. 2019;37:420–3.
pubmed: 30778233
doi: 10.1038/s41587-019-0036-z
de Vries SJ, van Dijk M, Bonvin AMJJ. The HADDOCK web server for data-driven biomolecular docking. Nat Protoc. 2010;5:883–97.
pubmed: 20431534
doi: 10.1038/nprot.2010.32
van Zundert GCP, Rodrigues JPGLM, Trellet M, Schmitz C, Kastritis PL, Karaca E, et al. The HADDOCK2.2 web server: user-friendly integrative modeling of Biomolecular complexes. J Mol Biol. 2016;428:720–5.
pubmed: 26410586
doi: 10.1016/j.jmb.2015.09.014
Li Z, Jaroszewski L, Iyer M, Sedova M, Godzik A. FATCAT 2.0: towards a better understanding of the structural diversity of proteins. Nucleic Acids Res. 2020;48:W60–4.
pubmed: 32469061
pmcid: 7319568
doi: 10.1093/nar/gkaa443
van Kempen M, Kim SS, Tumescheit C, Mirdita M, Lee J, Gilchrist CLM, et al. Fast and accurate protein structure search with Foldseek. Nat Biotechnol. 2024;42:243–6.
pubmed: 37156916
doi: 10.1038/s41587-023-01773-0