Identification of the type II cytochrome c maturation pathway in anammox bacteria by comparative genomics

BMC Microbiology

Mike SM Jetten²  Jan TM Keltjens²  James WA Allen¹  Huub JM Op den Camp²  Joachim Reimann²  Daan R Speth²  Christina Ferousi² 

[1] Department of Biochemistry, University of Oxford, South Parks Road, OX13QU Oxford, UK;Department of Microbiology, Institute for Water and Wetland Research, Radboud University Nijmegen, Heyendaalseweg 135, 6525, AJ, Nijmegen, the Netherlands

关键词: CcdA;    DsbD;    CcsX;    CcsB;    CcsA;    ccs;    Anaerobic ammonium oxidizing bacteria;    Cytochrome c biogenesis;   

Others  :  1142607
DOI  :  10.1186/1471-2180-13-265

 received in 2013-06-26, accepted in 2013-11-18,  发布年份 2013

【 摘 要 】

Background

Anaerobic ammonium oxidizing (anammox) bacteria may contribute up to 50% to the global nitrogen production, and are, thus, key players of the global nitrogen cycle. The molecular mechanism of anammox was recently elucidated and is suggested to proceed through a branched respiratory chain. This chain involves an exceptionally high number of c-type cytochrome proteins which are localized within the anammoxosome, a unique subcellular organelle. During transport into the organelle the c-type cytochrome apoproteins need to be post-translationally processed so that heme groups become covalently attached to them, resulting in mature c-type cytochrome proteins.

Results

In this study, a comparative genome analysis was performed to identify the cytochrome c maturation system employed by anammox bacteria. Our results show that all available anammox genome assemblies contain a complete type II cytochrome c maturation system.

Conclusions

Our working model suggests that this machinery is localized at the anammoxosome membrane which is assumed to be the locus of anammox catabolism. These findings will stimulate further studies in dissecting the molecular and cellular basis of cytochrome c biogenesis in anammox bacteria.

【 授权许可】

   
2013 Ferousi et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Lindsay MR, Webb RI, Strous M, Jetten MS, Butler MK, Forde RJ, Fuerst JA: Cell compartmentalisation in Planctomycetes: novel types of structural organisation for the bacterial cell. Arch Microbiol 2001, 175:413-429.
• [2]Jetten MSM, Niftrik LV, Strous M, Kartal B, Keltjens JT, Op den Camp HJM: Biochemistry and molecular biology of anammox bacteria. Critic Rev Biochem Mol Biol 2009, 44:65-84.
• [3]van Niftrik L, van Helden M, Kirchen S, van Donselaar EG, Harhangi HR, Webb RI, Fuerst J, Op den Camp HJM, Jetten MSM, Strous M: Intracellular localization of membrane-bound ATPases in the compartmentalized anammox bacterium 'Candidatus Kuenenia stuttgartiensis’. Mol Microbiol 2010, 77:701-715.
• [4]van Niftrik L, Geerts WJC, van Donselaar EG, Humbel BM, Webb RI, Fuerst J, Verkleij AJ, Jetten MSM, Strous M: Linking ultrastructure and function in four genera of anaerobic ammonium-oxidizing bacteria: cell plan, glycogen storage, and localization of cytochrome c proteins. J Bacteriol 2008, 190:708-717.
• [5]Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor MW, Horn M, Daims H, Bartol-Mavel D, Wincker P, Barbe V, Fonknechten N, Vallenet D, Segurens B, Schenowitz-Truong C, Médigue C, Collingro A, Snel B, Dutilh BE, Op den Camp HJM, van der Drift C, Cirpus I, van de Pas-Schoonen KT, Harhangi HR, van Niftrik L, Schmid M, Keltjens J, van de Vossenberg J, Kartal B, Meier H, et al.: Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 2006, 440:790-794.
• [6]van de Vossenberg J, Woebken D, Maalcke WJ, Wessels HJ, Dutilh BE, Kartal B, Janssen-Megens EM, Roeselers G, Yan J, Speth D, Gloerich J, Geerts W, van der Biezen E, Pluk W, Francoijs KJ, Russ L, Lam P, Malfatti SA, Tringe SG, Haaijer SC, Op den Camp HJ, Stunnenberg HG, Amann R, Kuypers MM, Jetten MS: The metagenome of the marine anammox bacterium 'Candidatus Scalindua profunda’ illustrates the versatility of this globally important nitrogen cycle bacterium. Environ Microbiol 2013, 15(5):1275-1289.
• [7]Hira D, Toh H, Migita CT, Okubo H, Nishiyama T, Hattori M, Furukawa K, Fujii T: Anammox organism KSU-1 expresses a NirK-type copper-containing nitrite reductase instead of a NirS-type with cytochrome cd1. FEBS Lett 2012, 586:1658-1663.
• [8]Hamel P, Corvest V, Giege P, Bonnard G: Biochemical requirements for the maturation of mitochondrial c-type cytochromes. Biochim Biophys Acta 2009, 1793:125-138.
• [9]Allen J, Ginger M, Ferguson S: Complexity and diversity in c-type cytochrome biogenesis systems. Biochem Soc Trans 2005, 33:145-146.
• [10]Jetten MSM, Op den Camp HJM, Kuenen JG, Strous M: Description of the order Brocadiales. In Bergey’s manual of systematic bacteriology. Volume 4. Edited by Krieg NR, Staley JT, Brown DR, Hedlund BP, Paster BJ, Ward NL, Ludwig W, Whitman WB. Heidelberg, Germany: Springer; 2010:596-603.
• [11]Soding J, Biegert A, Lupas AN: The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 2005, 33:W244-W248.
• [12]Finn RD, Clements J, Eddy SR: HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 2011, 39:W29-W37.
• [13]Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy SR, Sonnhammer EL, Bateman A: Pfam: clans, web tools and services. Nucleic Acids Res 2006, 34:D247-D251.
• [14]Sonnhammer E, Von Heijne G, Krogh A: A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 1998, 6:175-182.
• [15]Petersen TN, Brunak S, von Heijne G, Nielsen H: SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011, 8:785-786.
• [16]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
• [17]Frawley ER, Kranz RG: CcsBA is a cytochrome c synthetase that also functions in heme transport. Proc Natl Acad Sci U S A 2009, 106:10201-10206.
• [18]Beckett CS, Loughman JA, Karberg KA, Donato GM, Goldman WE, Kranz RG: Four genes are required for the system II cytochrome c biogenesis pathway in Bordetella pertussis, a unique bacterial model. Mol Microbiol 2000, 38:465-481.
• [19]Kranz RG, Richard-Fogal C, Taylor JS, Frawley ER: Cytochrome c biogenesis: mechanisms for covalent modifications and trafficking of heme and for heme-iron redox control. Microbiol Mol Biol Rev 2009, 73:510-528.
• [20]Kartal B, Maalcke WJ, de Almeida NM, Cirpus I, Gloerich J, Geerts W, Op den Camp HJ, Harhangi HR, Janssen-Megens EM, Francoijs KJ, Stunnenberg HG, Keltjens JT, Jetten MS, Strous M: Molecular mechanism of anaerobic ammonium oxidation. Nature 2011, 479:127-130.
• [21]Jones DT, Taylor WR, Thornton JM: The rapid generation of mutation data matrices from protein sequences. Comp Appl Biosci: CABIOS 1992, 8:275-282.
• [22]Stewart EJ, Katzen F, Beckwith J: Six conserved cysteines of the membrane protein DsbD are required for the transfer of electrons from the cytoplasm to the periplasm of Escherichia coli. EMBO J 1999, 18:5963-5971.
• [23]Porat A, Cho SH, Beckwith J: The unusual transmembrane electron transporter DsbD and its homologues: a bacterial family of disulfide reductases. Res Microbiol 2004, 155:617-622.
• [24]Ito K, Inaba K: The disulfide bond formation (Dsb) system. Curr Opin Struct Biol 2008, 18:450-458.