Comparative genomic analysis of nickel homeostasis in cable bacteria.
Candidatus Electrothrix antwerpensis
Cable bacteria
Genomics
Nickel cofactor
Nickel homeostasis
RcnA
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
15 Jul 2024
15 Jul 2024
Historique:
received:
27
03
2024
accepted:
03
07
2024
medline:
16
7
2024
pubmed:
16
7
2024
entrez:
15
7
2024
Statut:
epublish
Résumé
Cable bacteria are filamentous members of the Desulfobulbaceae family that are capable of performing centimetre‑scale electron transport in marine and freshwater sediments. This long‑distance electron transport is mediated by a network of parallel conductive fibres embedded in the cell envelope. This fibre network efficiently transports electrical currents along the entire length of the centimetre‑long filament. Recent analyses show that these fibres consist of metalloproteins that harbour a novel nickel‑containing cofactor, which indicates that cable bacteria have evolved a unique form of biological electron transport. This nickel‑dependent conduction mechanism suggests that cable bacteria are strongly dependent on nickel as a biosynthetic resource. Here, we performed a comprehensive comparative genomic analysis of the genes linked to nickel homeostasis. We compared the genome‑encoded adaptation to nickel of cable bacteria to related members of the Desulfobulbaceae family and other members of the Desulfobulbales order. Presently, four closed genomes are available for the monophyletic cable bacteria clade that consists of the genera Candidatus Electrothrix and Candidatus Electronema. To increase the phylogenomic coverage, we additionally generated two closed genomes of cable bacteria: Candidatus Electrothrix gigas strain HY10‑6 and Candidatus Electrothrix antwerpensis strain GW3‑4, which are the first closed genomes of their respective species. Nickel homeostasis genes were identified in a database of 38 cable bacteria genomes (including 6 closed genomes). Gene prevalence was compared to 19 genomes of related strains, residing within the Desulfobulbales order but outside of the cable bacteria clade, revealing several genome‑encoded adaptations to nickel homeostasis in cable bacteria. Phylogenetic analysis indicates that nickel importers, nickel‑binding enzymes and nickel chaperones of cable bacteria are affiliated to organisms outside the Desulfobulbaceae family, with several proteins showing affiliation to organisms outside of the Desulfobacterota phylum. Conspicuously, cable bacteria encode a unique periplasmic nickel export protein RcnA, which possesses a putative cytoplasmic histidine‑rich loop that has been largely expanded compared to RcnA homologs in other organisms. Cable bacteria genomes show a clear genetic adaptation for nickel utilization when compared to closely related genera. This fully aligns with the nickel‑dependent conduction mechanism that is uniquely found in cable bacteria.
Sections du résumé
BACKGROUND
BACKGROUND
Cable bacteria are filamentous members of the Desulfobulbaceae family that are capable of performing centimetre‑scale electron transport in marine and freshwater sediments. This long‑distance electron transport is mediated by a network of parallel conductive fibres embedded in the cell envelope. This fibre network efficiently transports electrical currents along the entire length of the centimetre‑long filament. Recent analyses show that these fibres consist of metalloproteins that harbour a novel nickel‑containing cofactor, which indicates that cable bacteria have evolved a unique form of biological electron transport. This nickel‑dependent conduction mechanism suggests that cable bacteria are strongly dependent on nickel as a biosynthetic resource. Here, we performed a comprehensive comparative genomic analysis of the genes linked to nickel homeostasis. We compared the genome‑encoded adaptation to nickel of cable bacteria to related members of the Desulfobulbaceae family and other members of the Desulfobulbales order.
RESULTS
RESULTS
Presently, four closed genomes are available for the monophyletic cable bacteria clade that consists of the genera Candidatus Electrothrix and Candidatus Electronema. To increase the phylogenomic coverage, we additionally generated two closed genomes of cable bacteria: Candidatus Electrothrix gigas strain HY10‑6 and Candidatus Electrothrix antwerpensis strain GW3‑4, which are the first closed genomes of their respective species. Nickel homeostasis genes were identified in a database of 38 cable bacteria genomes (including 6 closed genomes). Gene prevalence was compared to 19 genomes of related strains, residing within the Desulfobulbales order but outside of the cable bacteria clade, revealing several genome‑encoded adaptations to nickel homeostasis in cable bacteria. Phylogenetic analysis indicates that nickel importers, nickel‑binding enzymes and nickel chaperones of cable bacteria are affiliated to organisms outside the Desulfobulbaceae family, with several proteins showing affiliation to organisms outside of the Desulfobacterota phylum. Conspicuously, cable bacteria encode a unique periplasmic nickel export protein RcnA, which possesses a putative cytoplasmic histidine‑rich loop that has been largely expanded compared to RcnA homologs in other organisms.
CONCLUSION
CONCLUSIONS
Cable bacteria genomes show a clear genetic adaptation for nickel utilization when compared to closely related genera. This fully aligns with the nickel‑dependent conduction mechanism that is uniquely found in cable bacteria.
Identifiants
pubmed: 39009997
doi: 10.1186/s12864-024-10594-7
pii: 10.1186/s12864-024-10594-7
doi:
Substances chimiques
Nickel
7OV03QG267
Bacterial Proteins
0
Types de publication
Journal Article
Comparative Study
Langues
eng
Sous-ensembles de citation
IM
Pagination
692Informations de copyright
© 2024. The Author(s).
Références
Risgaard-Petersen N, Kristiansen M, Frederiksen RB, Dittmer AL, Bjerg JT, Trojan D, et al. Cable bacteria in freshwater sediments. Appl Environ Microbiol. 2015;81(17):6003–11.
pubmed: 26116678
pmcid: 4551263
doi: 10.1128/AEM.01064-15
Malkin SY, Rao AMF, Seitaj D, Vasquez-Cardenas D, Zetsche EM, Hidalgo-Martinez S, et al. Natural occurrence of microbial sulphur oxidation by long-range electron transport in the seafloor. ISME J. 2014;8(9):1843–54.
pubmed: 24671086
pmcid: 4139731
doi: 10.1038/ismej.2014.41
Burdorf LDW, Tramper A, Seitaj D, Meire L, Hidalgo-Martinez S, Zetsche EM, et al. Long-distance electron transport occurs globally in marine sediments. Biogeosciences. 2017;14(3):683–701.
doi: 10.5194/bg-14-683-2017
Pfeffer C, Larsen S, Song J, Dong M, Besenbacher F, Meyer RL, et al. Filamentous bacteria transport electrons over centimetre distances. Nature. 2012;491(7423):218–21.
pubmed: 23103872
doi: 10.1038/nature11586
Cornelissen R, Bøggild A, Thiruvallur Eachambadi R, Koning RI, Kremer A, Hidalgo-Martinez S, et al. The cell envelope structure of cable bacteria. Front Microbiol. 2018;9(3044):1–13.
Meysman FJR, Cornelissen R, Trashin S, Bonné R, Martinez SH, van der Veen J, et al. A highly conductive fibre network enables centimetre-scale electron transport in multicellular cable bacteria. Nat Commun. 2019;10(1):4120.
pubmed: 31511526
pmcid: 6739318
doi: 10.1038/s41467-019-12115-7
Thiruvallur Eachambadi R, Bonné R, Cornelissen R, Hidalgo-Martinez S, Vangronsveld J, Meysman FJR, et al. Cable bacteria: an ordered and fail-safe electrical network in cable bacteria. Adv Biosyst. 2020;4(7):e2000006.
pubmed: 32449305
doi: 10.1002/adbi.202000006
Bjerg JT, Boschker HTS, Larsen S, Berry D, Schmid M, Millo D, et al. Long-distance electron transport in individual, living cable bacteria. Proc Natl Acad Sci. 2018;115(22):5786–91.
pubmed: 29735671
pmcid: 5984516
doi: 10.1073/pnas.1800367115
Geerlings NMJ, Karman C, Trashin S, As KS, Kienhuis MVM, Hidalgo-Martinez S, et al. Division of labor and growth during electrical cooperation in multicellular cable bacteria. Proc Natl Acad Sci. 2020;117(10):5478–85.
pubmed: 32094191
pmcid: 7071850
doi: 10.1073/pnas.1916244117
Smets B, Boschker HTS, Wetherington MT, Lelong G, Hidalgo-Martinez S, Polerecky L, et al. Multi-wavelength Raman microscopy of nickel-based electron transport in cable bacteria. Front Microbiol. 2024;8:15.
Boschker HTS, Cook PLM, Polerecky L, Eachambadi RT, Lozano H, Hidalgo-Martinez S, et al. Efficient long-range conduction in cable bacteria through nickel protein wires. Nat Commun. 2021;12(1):3996.
pubmed: 34183682
pmcid: 8238962
doi: 10.1038/s41467-021-24312-4
Pankratov D, Hidalgo Martinez S, Karman C, Gherzik A, Gomila G, Trashin S, et al. The organo-metal-like nature of long-range conduction in cable bacteria. Bioelectrochemistry. 2024;157:108675.
pubmed: 38422765
doi: 10.1016/j.bioelechem.2024.108675
van der Veen JR, Valianti S, van der Zant HSJ, Blanter YM, Meysman FJR. A model analysis of centimeter-long electron transport in cable bacteria. Phys Chem Chem Phys. 2024;26(4):3139–51.
pubmed: 38189548
doi: 10.1039/D3CP04466A
Alfano M, Cavazza C. Structure, function, and biosynthesis of nickel-dependent enzymes. Protein Sci. 2020;29(5):1071–89.
pubmed: 32022353
pmcid: 7184782
doi: 10.1002/pro.3836
Fontecilla-Camps JC. Nickel and the origin and early evolution of life. Metallomics. 2022;14(4):mfa016.
doi: 10.1093/mtomcs/mfac016
Liu J, Chakraborty S, Hosseinzadeh P, Yu Y, Tian S, Petrik I, et al. Metalloproteins containing cytochrome, iron-sulfur, or copper redox centers. Chem Rev. 2014;114(8):4366–469.
pubmed: 24758379
pmcid: 4002152
doi: 10.1021/cr400479b
Trojan D, Schreiber L, Bjerg JT, Bøggild A, Yang T, Kjeldsen KU, et al. A taxonomic framework for cable bacteria and proposal of the candidate genera Electrothrix and Electronema. Syst Appl Microbiol. 2016;39(5):297–306.
pubmed: 27324572
pmcid: 4958695
doi: 10.1016/j.syapm.2016.05.006
Kjeldsen KU, Schreiber L, Thorup CA, Boesen T, Bjerg JT, Yang T. On the evolution and physiology of cable bacteria. PNAS. 2019;116(38):19116–25.
pubmed: 31427514
pmcid: 6754541
doi: 10.1073/pnas.1903514116
Sereika M, Petriglieri F, Jensen TBN, Sannikov A, Hoppe M, Nielsen PH, et al. Closed genomes uncover a saltwater species of Candidatus Electronema and shed new light on the boundary between marine and freshwater cable bacteria. ISME J. 2023;17(4):561–9.
pubmed: 36697964
pmcid: 10030654
doi: 10.1038/s41396-023-01372-6
Geelhoed JS, van de Velde SJ, Meysman FJR. Quantification of cable bacteria in marine sediments via qPCR. Front Microbiol. 2020;3:11.
Moeck GS, Coulton JW. TonB-dependent iron acquisition: mechanisms of siderophore-mediated active transport
pubmed: 9643536
doi: 10.1046/j.1365-2958.1998.00817.x
Silale A, van den Berg B. TonB-dependent transport across the bacterial outer membrane. Annu Rev Microbiol. 2023;77(1):67–88.
pubmed: 36944260
doi: 10.1146/annurev-micro-032421-111116
Lhospice S, Gomez NO, Ouerdane L, Brutesco C, Ghssein G, Hajjar C, et al. Pseudomonas aeruginosa zinc uptake in chelating environment is primarily mediated by the metallophore pseudopaline. Sci Rep. 2017;7(1):17132.
pubmed: 29214991
pmcid: 5719457
doi: 10.1038/s41598-017-16765-9
Noinaj N, Guillier M, Barnard TJ, Buchanan SK. TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol. 2010;64(1):43–60.
pubmed: 20420522
pmcid: 3108441
doi: 10.1146/annurev.micro.112408.134247
Eitinger T, Suhr J, Moore L, Smith JAC. Secondary transporters for nickel and cobalt ions: theme and variations. Biometals. 2005;18(4):399–405.
pubmed: 16158232
doi: 10.1007/s10534-005-3714-x
Mulrooney SB, Hausinger RP. Nickel uptake and utilization by microorganisms. FEMS Microbiol Rev. 2003;27(2–3):239–61.
pubmed: 12829270
doi: 10.1016/S0168-6445(03)00042-1
Zeer-Wanklyn CJ, Zamble DB. Microbial nickel: cellular uptake and delivery to enzyme centers. Curr Opin Chem Biol. 2017;37:80–8.
pubmed: 28213182
doi: 10.1016/j.cbpa.2017.01.014
Macomber L, Hausinger RP. Mechanisms of nickel toxicity in microorganisms. Metallomics. 2011;3(11):1153.
pubmed: 21799955
doi: 10.1039/c1mt00063b
Sydor AM, Zamble DB. Nickel metallomics: general themes guiding nickel homeostasis. 2013. p. 375–416.
Li Y, Zamble DB. Nickel homeostasis and nickel regulation: an overview. Chem Rev. 2009;109(10):4617–43.
pubmed: 19711977
doi: 10.1021/cr900010n
Hiralal A, Geelhoed JS, Hidalgo-Martinez S, Smets B, van Dijk JR, Meysman FJR. Closing the genome of unculturable cable bacteria using a combined metagenomic assembly of long and short sequencing reads. Microb Genom. 2024;10(2):001197.
pubmed: 38376381
pmcid: 10926707
Thorup C, Petro C, Bøggild A, Ebsen TS, Brokjær S, Nielsen LP, et al. How to grow your cable bacteria: establishment of a stable single-strain culture in sediment and proposal of Candidatus electronema aureum GS. Syst Appl Microbiol. 2021;44(5):126236.
pubmed: 34332367
doi: 10.1016/j.syapm.2021.126236
Nečas D, Klapetek P. Gwyddion: an open-source software for SPM data analysis. Open Phys. 2012;10(1):181–8.
doi: 10.2478/s11534-011-0096-2
Ewels P, Magnusson M, Lundin S, Käller M. MultiQC: Summarize analysis results for multiple tools and samples in a single report. Bioinformatics. 2016;32(19):3047–8.
pubmed: 27312411
pmcid: 5039924
doi: 10.1093/bioinformatics/btw354
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics. 2014;30(15):2114–20.
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Lanfear R, Schalamun M, Kainer D, Wang W, Schwessinger B. MinIONQC: Fast and simple quality control for MinION sequencing data. Bioinformatics. 2019;35(3):523–5.
pubmed: 30052755
doi: 10.1093/bioinformatics/bty654
Kolmogorov M, Yuan J, Lin Y, Pevzner PA. Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol. 2019;37(5):540–6.
pubmed: 30936562
doi: 10.1038/s41587-019-0072-8
Kolmogorov M, Bickhart DM, Behsaz B, Gurevich A, Rayko M, Shin SB, et al. metaFlye: scalable long-read metagenome assembly using repeat graphs. Nat Methods. 2020;17(11):1103–10.
pubmed: 33020656
pmcid: 10699202
doi: 10.1038/s41592-020-00971-x
Milne I, Bayer M, Cardle L, Shaw P, Stephen G, Wright F, et al. Tablet-next generation sequence assembly visualization. Bioinformatics. 2009;26(3):401–2.
pubmed: 19965881
pmcid: 2815658
doi: 10.1093/bioinformatics/btp666
Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk v2: memory friendly classification with the genome taxonomy database. Bioinformatics. 2022;38(23):5315–6.
pubmed: 36218463
pmcid: 9710552
doi: 10.1093/bioinformatics/btac672
Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE. 2014;9(11):e112963.
pubmed: 25409509
pmcid: 4237348
doi: 10.1371/journal.pone.0112963
Geelhoed JS, Thorup CA, Bjerg JJ, Schreiber L, Nielsen LP, Schramm A, et al. Indications for a genetic basis for big bacteria and description of the giant cable bacterium Candidatus Electrothrix gigas sp. nov. Microbiol Spectr. 2023;11(5):e00538–23.
Li H. Minimap2: Pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34(18):3094–100.
pubmed: 29750242
pmcid: 6137996
doi: 10.1093/bioinformatics/bty191
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25(16):2078–9.
pubmed: 19505943
pmcid: 2723002
doi: 10.1093/bioinformatics/btp352
Fang Y, Liu J, Yang J, Wu G, Hua Z, Dong H, et al. Compositional and metabolic responses of autotrophic microbial community to salinity in lacustrine environments. mSystems. 2022;7(4):e0033522.
pubmed: 35862818
doi: 10.1128/msystems.00335-22
Plum-Jensen LE, Schramm A, Marshall IPG. First single-strain enrichments of electrothrix cable bacteria, description of E. aestuarii sp. nov. and E. rattekaaiensis sp. nov., and proposal of a cable bacteria taxonomy following the rules of the SeqCode. Syst Appl Microbiol. 2024;47(1):126487.
pubmed: 38295603
doi: 10.1016/j.syapm.2024.126487
Bowers RM, Kyrpides NC, Stepanauskas R, Harmon-Smith M, Doud D, Reddy TBK, et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat Biotechnol. 2017;35(8):725–31.
pubmed: 28787424
pmcid: 6436528
doi: 10.1038/nbt.3893
Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol. 2018;35(2):518–22.
pubmed: 29077904
doi: 10.1093/molbev/msx281
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14(6):587–9.
pubmed: 28481363
pmcid: 5453245
doi: 10.1038/nmeth.4285
Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–74.
pubmed: 25371430
doi: 10.1093/molbev/msu300
Pritchard L, Glover RH, Humphris S, Elphinstone JG, Toth IK. Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Anal Methods. 2016;8(1):12–24.
doi: 10.1039/C5AY02550H
Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 2016;44(14):6614–24.
pubmed: 27342282
pmcid: 5001611
doi: 10.1093/nar/gkw569
Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics. 2010;11(1):1–11.
doi: 10.1186/1471-2105-11-119
Seemann T. Prokka: Rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068–9.
pubmed: 24642063
doi: 10.1093/bioinformatics/btu153
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.
pubmed: 2231712
doi: 10.1016/S0022-2836(05)80360-2
Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using clustal omega. Mol Syst Biol. 2011;7:539.
pubmed: 21988835
pmcid: 3261699
doi: 10.1038/msb.2011.75
Eddy SR. Accelerated Profile HMM Searches. PLoS Comput Biol. 2011;7(10):e1002195.
pubmed: 22039361
pmcid: 3197634
doi: 10.1371/journal.pcbi.1002195
Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, et al. InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014;30(9):1236–40.
pubmed: 24451626
pmcid: 3998142
doi: 10.1093/bioinformatics/btu031
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(4):420–3.
pubmed: 30778233
doi: 10.1038/s41587-019-0036-z
Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. J Mol Biol. 2001;305(3):567–80.
pubmed: 11152613
doi: 10.1006/jmbi.2000.4315
Søndergaard D, Pedersen CNS, Greening C. HydDB: A web tool for hydrogenase classification and analysis. Sci Rep. 2016;6(1):34212.
pubmed: 27670643
pmcid: 5037454
doi: 10.1038/srep34212
Pirovano W, Feenstra KA, Heringa J. PRALINE™: a strategy for improved multiple alignment of transmembrane proteins. Bioinformatics. 2008;24(4):492–7.
pubmed: 18174178
doi: 10.1093/bioinformatics/btm636
Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun. 2018;9(1):5114.
pubmed: 30504855
pmcid: 6269478
doi: 10.1038/s41467-018-07641-9
Lücker S, Steger D, Kjeldsen KU, MacGregor BJ, Wagner M, Loy A. Improved 16S rRNA-targeted probe set for analysis of sulfate-reducing bacteria by fluorescence in situ hybridization. J Microbiol Methods. 2007;69(3):523–8.
pubmed: 17408790
doi: 10.1016/j.mimet.2007.02.009
Loy A, Lehner A, Lee N, Adamczyk J, Meier H, Ernst J, et al. Oligonucleotide microarray for 16S rRNA gene-based detection of all recognized lineages of sulfate-reducing prokaryotes in the environment. Appl Environ Microbiol. 2002;68(10):5064–81.
pubmed: 12324358
pmcid: 126405
doi: 10.1128/AEM.68.10.5064-5081.2002
Thorup C, Schramm A, Findlay AJ, Finster KW, Schreiber L. Disguised as a sulfate reducer: growth of the deltaproteobacterium Desulfurivibrio alkaliphilus by sulfide oxidation with nitrate. mBio. 2017;8(4):e00671–17.
pubmed: 28720728
pmcid: 5516251
doi: 10.1128/mBio.00671-17
Vasquez-Cardenas D, Van De Vossenberg J, Polerecky L, Malkin SY, Schauer R, Hidalgo-Martinez S, et al. Microbial carbon metabolism associated with electrogenic sulphur oxidation in coastal sediments. ISME J. 2015;9(9):1966–78.
pubmed: 25679534
pmcid: 4542026
doi: 10.1038/ismej.2015.10
Ramel F, Amrani A, Pieulle L, Lamrabet O, Voordouw G, Seddiki N, et al. Membrane-bound oxygen reductases of the anaerobic sulfate-reducing Desulfovibrio vulgaris Hildenborough: roles in oxygen defence and electron link with periplasmic hydrogen oxidation. Microbiology. 2013;159(Pt_12):2663–73.
Marzocchi U, Thorup C, Dam AS, Schramm A, Risgaard-Petersen N. Dissimilatory nitrate reduction by a freshwater cable bacterium. ISME J. 2022;16(1):50–7.
pubmed: 34215856
doi: 10.1038/s41396-021-01048-z
Hebbeln P, Eitinger T. Heterologous production and characterization of bacterial nickel/cobalt permeases. FEMS Microbiol Lett. 2004;230(1):129–35.
pubmed: 14734175
doi: 10.1016/S0378-1097(03)00885-1
Degen O, Eitinger T. Substrate specificity of nickel/cobalt permeases: insights from mutants altered in transmembrane domains I and II. J Bacteriol. 2002;184(13):3569–77.
pubmed: 12057951
pmcid: 135128
doi: 10.1128/JB.184.13.3569-3577.2002
Degen O, Kobayashi M, Shimizu S, Eitinger T. Selective transport of divalent cations by transition metal permeases: the Alcaligenes eutrophus HoxN and the Rhodococcus rhodochrous NhlF. Arch Microbiol. 1999;171(3):139–45.
pubmed: 10201093
doi: 10.1007/s002030050691
Wolfram L, Friedrich B, Eitinger T. The Alcaligenes eutrophus protein HoxN mediates nickel transport in Escherichia coli. J Bacteriol. 1995;177(7):1840–3.
pubmed: 7896709
pmcid: 176814
doi: 10.1128/jb.177.7.1840-1843.1995
Mobley HLT, Garner RM, Bauerfeind P. Helicobacter pylori nickel-transport gene nixA : synthesis of catalytically active urease in Escherichia coli independent of growth conditions. Mol Microbiol. 1995;16(1):97–109.
pubmed: 7651142
doi: 10.1111/j.1365-2958.1995.tb02395.x
Fu C, Javedan S, Moshiri F, Maier RJ. Bacterial genes involved in incorporation of nickel into a hydrogenase enzyme. Proc Natl Acad Sci. 1994;91(11):5099–103.
pubmed: 8197192
pmcid: 43939
doi: 10.1073/pnas.91.11.5099
Navarro C, Wu L, Mandrand-Berthelot M. The nik operon of Escherichia coli encodes a periplasmic binding-protein-dependent transport system for nickel. Mol Microbiol. 1993;9(6):1181–91.
pubmed: 7934931
doi: 10.1111/j.1365-2958.1993.tb01247.x
Heddle J, Scott DJ, Unzai S, Park SY, Tame JRH. Crystal structures of the liganded and unliganded nickel-binding protein NikA from Escherichia coli. J Biol Chem. 2003;278(50):50322–9.
pubmed: 12960164
doi: 10.1074/jbc.M307941200
Rowe JL, Starnes GL, Chivers PT. Complex transcriptional control links NikABCDE-dependent nickel transport with hydrogenase expression in Escherichia coli. J Bacteriol. 2005;187(18):6317–23.
pubmed: 16159764
pmcid: 1236639
doi: 10.1128/JB.187.18.6317-6323.2005
Chivers PT, Benanti EL, Heil-Chapdelaine V, Iwig JS, Rowe JL. Identification of Ni-(l-His)2 as a substrate for NikABCDE-dependent nickel uptake in Escherichia coli. Metallomics. 2012;4(10):1043.
pubmed: 22885853
doi: 10.1039/c2mt20139a
Lebrette H, Iannello M, Fontecilla-Camps JC, Cavazza C. The binding mode of Ni-(L-His)2 in NikA revealed by X-ray crystallography. J Inorg Biochem. 2013;121:16–8.
pubmed: 23314594
doi: 10.1016/j.jinorgbio.2012.12.010
Rodionov DA, Hebbeln P, Gelfand MS, Eitinger T. Comparative and functional genomic analysis of prokaryotic nickel and cobalt uptake transporters: evidence for a novel group of ATP-binding cassette transporters. J Bacteriol. 2006;188(1):317–27.
pubmed: 16352848
pmcid: 1317602
doi: 10.1128/JB.188.1.317-327.2006
Hollenstein K, Dawson RJ, Locher KP. Structure and mechanism of ABC transporter proteins. Curr Opin Struct Biol. 2007;17(4):412–8.
pubmed: 17723295
doi: 10.1016/j.sbi.2007.07.003
Cherrier MV, Cavazza C, Bochot C, Lemaire D, Fontecilla-Camps JC. Structural characterization of a putative endogenous metal chelator in the periplasmic nickel transporter NikA. Biochemistry. 2008;47(38):9937–43.
pubmed: 18759453
doi: 10.1021/bi801051y
Remy L, Carrière M, Derré-Bobillot A, Martini C, Sanguinetti M, Borezée-Durant E. The Staphylococcus aureus Opp1 ABC transporter imports nickel and cobalt in zinc-depleted conditions and contributes to virulence. Mol Microbiol. 2013;87(4):730–43.
pubmed: 23279021
doi: 10.1111/mmi.12126
Cui J, Davidson AL. ABC solute importers in bacteria. Essays Biochem. 2011;7(50):85–99.
Ernst FD, Stoof J, Horrevoets WM, Kuipers EJ, Kusters JG, van Vliet AHM. NikR Mediates nickel-responsive transcriptional repression of the Helicobacter pylori outer membrane proteins FecA3 (HP1400) and FrpB4 (HP1512). Infect Immun. 2006;74(12):6821–8.
pubmed: 17015456
pmcid: 1698083
doi: 10.1128/IAI.01196-06
Stoof J, Kuipers EJ, Klaver G, van Vliet AHM. An ABC transporter and a TonB ortholog contribute to Helicobacter mustelae nickel and cobalt acquisition. Infect Immun. 2010;78(10):4261–7.
pubmed: 20643857
pmcid: 2950367
doi: 10.1128/IAI.00365-10
Schauer K, Gouget B, Carrière M, Labigne A, De Reuse H. Novel nickel transport mechanism across the bacterial outer membrane energized by the TonB/ExbB/ExbD machinery. Mol Microbiol. 2007;63(4):1054–68.
pubmed: 17238922
doi: 10.1111/j.1365-2958.2006.05578.x
Davis GS, Flannery EL, Mobley HLT. Helicobacter pylori HP1512 Is a nickel-responsive NikR-regulated outer membrane protein. Infect Immun. 2006;74(12):6811–20.
pubmed: 17030579
pmcid: 1698071
doi: 10.1128/IAI.01188-06
Ogata H, Lubitz W, Higuchi Y. Structure and function of [NiFe] hydrogenases. J Biochem. 2016;160(5):251–8.
pubmed: 27493211
doi: 10.1093/jb/mvw048
Vignais PM, Billoud B, Meyer J. Classification and phylogeny of hydrogenases. FEMS Microbiol Rev. 2001;25(4):455–501.
pubmed: 11524134
doi: 10.1016/S0168-6445(01)00063-8
Peters JW, Schut GJ, Boyd ES, Mulder DW, Shepard EM, Broderick JB, et al. [FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation. Biochim Biophy Acta (BBA) - Mol Cell Res. 2015;1853(6):1350–69.
doi: 10.1016/j.bbamcr.2014.11.021
Leach MR, Zhang JW, Zamble DB. The role of complex formation between the Escherichia coli hydrogenase accessory factors HypB and SlyD. J Biol Chem. 2007;282(22):16177–86.
pubmed: 17426034
doi: 10.1074/jbc.M610834200
Chan Chung KC, Zamble DB. Protein interactions and localization of the Escherichia coli accessory protein HypA during nickel insertion to [NiFe] hydrogenase. J Biol Chem. 2011;286(50):43081–90.
pubmed: 22016389
pmcid: 3234881
doi: 10.1074/jbc.M111.290726
Kaluarachchi H, Sutherland DEK, Young A, Pickering IJ, Stillman MJ, Zamble DB. The Ni(II)-binding properties of the Metallochaperone SlyD. J Am Chem Soc. 2009;131(51):18489–500.
pubmed: 19947632
doi: 10.1021/ja9081765
Kunkle DE, Skaar EP. Moving metals: How microbes deliver metal cofactors to metalloproteins. Mol Microbiol. 2023;120(4):547–54.
pubmed: 37408317
doi: 10.1111/mmi.15117
Wülfing C, Plückthun A. Protein folding in the periplasm of Escherichia coli. Mol Microbiol. 1994;12(5):685–92.
pubmed: 8052121
doi: 10.1111/j.1365-2958.1994.tb01056.x
Lacasse MJ, Zamble DB. [NiFe]-Hydrogenase maturation. Biochemistry. 2016;55(12):1689–701.
pubmed: 26919691
doi: 10.1021/acs.biochem.5b01328
Lacasse MJ, Douglas CD, Zamble DB. Mechanism of selective nickel transfer from HypB to HypA, Escherichia coli [NiFe]-hydrogenase accessory proteins. Biochemistry. 2016;55(49):6821–31.
pubmed: 27951644
doi: 10.1021/acs.biochem.6b00706
Leach MR, Sandal S, Sun H, Zamble DB. Metal binding activity of the Escherichia coli hydrogenase maturation factor HypB. Biochemistry. 2005;44(36):12229–38.
pubmed: 16142921
doi: 10.1021/bi050993j
Can M, Armstrong FA, Ragsdale SW. Structure, function, and mechanism of the nickel metalloenzymes, CO dehydrogenase, and acetyl-CoA synthase. Chem Rev. 2014;114(8):4149–74.
pubmed: 24521136
pmcid: 4002135
doi: 10.1021/cr400461p
Oelgeschläger E, Rother M. Carbon monoxide-dependent energy metabolism in anaerobic bacteria and archaea. Arch Microbiol. 2008;190(3):257–69.
pubmed: 18575848
doi: 10.1007/s00203-008-0382-6
Lindahl PA. The Ni-containing carbon monoxide dehydrogenase family: light at the end of the tunnel? Biochemistry. 2002;41(7):2097–105.
pubmed: 11841199
doi: 10.1021/bi015932+
Svetlitchnaia T, Svetlitchnyi V, Meyer O, Dobbek H. Structural insights into methyltransfer reactions of a corrinoid iron–sulfur protein involved in acetyl-CoA synthesis. Proc Natl Acad Sci. 2006;103(39):14331–6.
pubmed: 16983091
pmcid: 1599964
doi: 10.1073/pnas.0601420103
Doukov TI, Blasiak LC, Seravalli J, Ragsdale SW, Drennan CL. Xenon in and at the end of the tunnel of bifunctional carbon monoxide dehydrogenase/acetyl-CoA synthase. Biochemistry. 2008;47(11):3474–83.
pubmed: 18293927
doi: 10.1021/bi702386t
Doukov TI, Iverson TM, Seravalli J, Ragsdale SW, Drennan CL. A Ni-Fe-Cu center in a bifunctional carbon monoxide dehydrogenase/acetyl-CoA synthase. Science (1979). 2002;298(5593):567–72.
Diender M, Stams AJM, Sousa DZ. Pathways and bioenergetics of anaerobic carbon monoxide fermentation. Front Microbiol. 2015;19:6.
Adam PS, Borrel G, Gribaldo S. Evolutionary history of carbon monoxide dehydrogenase/acetyl-CoA synthase, one of the oldest enzymatic complexes. Proc Natl Acad Sci. 2018;115(6):E1166–73.
pubmed: 29358391
pmcid: 5819426
doi: 10.1073/pnas.1716667115
Dobbek H, Svetlitchnyi V, Gremer L, Huber R, Meyer O. Crystal structure of a carbon monoxide dehydrogenase reveals a [Ni-4Fe-5S] cluster. Science (1979). 2001;293(5533):1281–5.
Domnik L, Merrouch M, Goetzl S, Jeoung J, Léger C, Dementin S, et al. CODH-IV: a high-efficiency CO-scavenging CO dehydrogenase with resistance to O
doi: 10.1002/anie.201709261
Drennan CL, Heo J, Sintchak MD, Schreiter E, Ludden PW. Life on carbon monoxide: X-ray structure of Rhodospirillum rubrum Ni-Fe-S carbon monoxide dehydrogenase. Proc Natl Acad Sci. 2001;98(21):11973–8.
pubmed: 11593006
pmcid: 59822
doi: 10.1073/pnas.211429998
Geelhoed JS, Henstra AM, Stams AJM. Carboxydotrophic growth of Geobacter sulfurreducens. Appl Microbiol Biotechnol. 2016;100(2):997–1007.
pubmed: 26481622
doi: 10.1007/s00253-015-7033-z
Liesegang H, Lemke K, Siddiqui RA, Schlegel HG. Characterization of the inducible nickel and cobalt resistance determinant cnr from pMOL28 of Alcaligenes eutrophus CH34. J Bacteriol. 1993;175(3):767–78.
pubmed: 8380802
pmcid: 196216
doi: 10.1128/jb.175.3.767-778.1993
Grass G, Fricke B, Nies DH. Control of expression of a periplasmic nickel efflux pump by periplasmic nickel concentrations. Biometals. 2005;18(4):437–48.
pubmed: 16158236
doi: 10.1007/s10534-005-3718-6
Cavet JS, Meng W, Pennella MA, Appelhoff RJ, Giedroc DP, Robinson NJ. A nickel-cobalt-sensing ArsR-SmtB family repressor. J Biol Chem. 2002;277(41):38441–8.
pubmed: 12163508
doi: 10.1074/jbc.M207677200
Munkelt D, Grass G, Nies DH. The chromosomally encoded cation diffusion facilitator proteins DmeF and FieF from Wautersia metallidurans CH34 Are transporters of broad metal specificity. J Bacteriol. 2004;186(23):8036–43.
pubmed: 15547276
pmcid: 529076
doi: 10.1128/JB.186.23.8036-8043.2004
Rodrigue A, Effantin G, Mandrand-Berthelot MA. Identification of rcnA ( yohM ), a nickel and cobalt resistance gene in Escherichia coli. J Bacteriol. 2005;187(8):2912–6.
pubmed: 15805538
pmcid: 1070376
doi: 10.1128/JB.187.8.2912-2916.2005
Iwig JS, Rowe JL, Chivers PT. Nickel homeostasis in Escherichia coli – the rcnR-rcnA efflux pathway and its linkage to NikR function. Mol Microbiol. 2006;62(1):252–62.
pubmed: 16956381
doi: 10.1111/j.1365-2958.2006.05369.x
Kim HM, Ahn BE, Lee JH, Roe JH. Regulation of a nickel–cobalt efflux system and nickel homeostasis in a soil actinobacterium Streptomyces coelicolor. Metallomics. 2015;7(4):702–9.
pubmed: 25697558
doi: 10.1039/C4MT00318G
Hallgren J, Tsirigos KD, Pedersen MD, Almagro Armenteros JJ, Marcatili P, Nielsen H, et al. DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks. BioRxiv. 2022;2022–04. https://www.biorxiv.org/content/10.1101/2022.04.08.487609v1.abstract .
Bryant P, Pozzati G, Elofsson A. Improved prediction of protein-protein interactions using AlphaFold2. Nat Commun. 2022;13(1):1265.
pubmed: 35273146
pmcid: 8913741
doi: 10.1038/s41467-022-28865-w
Digel L, Mierzwa M, Bonné R, Zieger SE, Pavel I, Ferapontova E, et al. Cable bacteria skeletons as catalytically active electrodes. Angew Chem Int Ed. 2024;63(6):e202312647.
van de Velde S, Callebaut I, Gao Y, Meysman FJR. Impact of electrogenic sulfur oxidation on trace metal cycling in a coastal sediment. Chem Geol. 2017;452:9–23.
doi: 10.1016/j.chemgeo.2017.01.028
Nikaido H. Porins and specific channels of bacterial outer membranes. Mol Microbiol. 1992;6(4):435–42.
pubmed: 1373213
doi: 10.1111/j.1365-2958.1992.tb01487.x
Buhrke T, Lenz O, Krauss N, Friedrich B. Oxygen tolerance of the H2-sensing [NiFe] hydrogenase from Ralstonia eutropha H16 Is based on limited access of oxygen to the active site. J Biol Chem. 2005;280(25):23791–6.
pubmed: 15849358
doi: 10.1074/jbc.M503260200
van der Linden E, Faber BW, Bleijlevens B, Burgdorf T, Bernhard M, Friedrich B, et al. Selective release and function of one of the two FMN groups in the cytoplasmic NAD
pubmed: 14764097
doi: 10.1111/j.1432-1033.2004.03984.x
Burgdorf T, Lenz O, Buhrke T, van der Linden E, Jones AK, Albracht SPJ, et al. [NiFe]-hydrogenases of Ralstonia eutropha; H16: modular enzymes for oxygen-tolerant biological hydrogen oxidation. Microb Physiol. 2005;10(2–4):181–96.
doi: 10.1159/000091564
Vieira S, Luckner M, Wanner G, Overmann J. Luteitalea pratensis gen. nov., sp. nov. a new member of subdivision 6 acidobacteria isolated from temperate grassland soil. Int J Syst Evol Microbiol. 2017;67(5):1408–14.
pubmed: 28141504
doi: 10.1099/ijsem.0.001827
Scilipoti S, Koren K, Risgaard-Petersen N, Schramm A, Nielsen LP. Oxygen consumption of individual cable bacteria. Sci Adv. 2021;7(7):eabe1870.
pubmed: 33568484
pmcid: 7875522
doi: 10.1126/sciadv.abe1870
Kerby RL, Youn H, Roberts GP. RcoM: a new single-component transcriptional regulator of CO metabolism in bacteria. J Bacteriol. 2008;190(9):3336–43.
pubmed: 18326575
pmcid: 2347395
doi: 10.1128/JB.00033-08
Nies DH. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev. 2003;27(2–3):313–39.
pubmed: 12829273
doi: 10.1016/S0168-6445(03)00048-2
Siunova TV, Siunov AV, Kochetkov VV, Boronin AM. The cnr-like operon in strain Comamonas sp. encoding resistance to cobalt and nickel. Russ J Genet. 2009;45(3):292–7.
doi: 10.1134/S1022795409030053