An intracellular pH gradient in the anammox bacterium Kuenenia stuttgartiensis as evaluated by P-31 NMR

van der Star WRL, Dijkema C, de Waard P, Picioreanu C, Strous M, van Loosdrecht MCM (2010)
APPLIED MICROBIOLOGY AND BIOTECHNOLOGY 86(1): 311-317.

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DOI
Autor*in
van der Star, Wouter R. L.; Dijkema, Cor; de Waard, Pieter; Picioreanu, Cristian; Strous, MarcUniBi; van Loosdrecht, Mark C. M.
Einrichtung
Centrum für Biotechnologie > Arbeitsgruppe M. Strous
Fakultät für Biologie
Centrum für Biotechnologie > Institut für Genomforschung und Systembiologie
Abstract / Bemerkung
The cytoplasm of anaerobic ammonium oxidizing (anammox) bacteria consists of three compartments separated by membranes. It has been suggested that a proton motive force may be generated over the membrane of the innermost compartment, the "anammoxosome". P-31 nuclear magnetic resonance (NMR) spectroscopy was employed to investigate intracellular pH differences in the anammox bacterium Kuenenia stuttgartiensis. With in vivo NMR, spectra were recorded of active, highly concentrated suspensions of K. stuttgartiensis in a wide-bore NMR tube. At different external pH values, two stable and distinct phosphate peaks were apparent in the recorded spectra. These peaks were equivalent with pH values of 7.3 and 6.3 and suggested the presence of a proton motive force over an intracytoplasmic membrane in K. stuttgartiensis. This study provides for the second time-after discovery of acidocalcisome-like compartments in Agrobacterium tumefaciens-evidence for an intracytoplasmic pH gradient in a chemotrophic prokaryotic cell.
Stichworte
Internal pH; In vivo NMR; Nuclear; magnetic resonance spectroscopy; P-31 NMR; Anammox; Kuenenia stuttgartiensis
Erscheinungsjahr
2010
Zeitschriftentitel
APPLIED MICROBIOLOGY AND BIOTECHNOLOGY
Band
86
Ausgabe
1
Seite(n)
311-317
ISSN
0175-7598
eISSN
1432-0614
Page URI
https://pub.uni-bielefeld.de/record/1588560

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van der Star WRL, Dijkema C, de Waard P, Picioreanu C, Strous M, van Loosdrecht MCM. An intracellular pH gradient in the anammox bacterium Kuenenia stuttgartiensis as evaluated by P-31 NMR. APPLIED MICROBIOLOGY AND BIOTECHNOLOGY. 2010;86(1):311-317.
van der Star, W. R. L., Dijkema, C., de Waard, P., Picioreanu, C., Strous, M., & van Loosdrecht, M. C. M. (2010). An intracellular pH gradient in the anammox bacterium Kuenenia stuttgartiensis as evaluated by P-31 NMR. APPLIED MICROBIOLOGY AND BIOTECHNOLOGY, 86(1), 311-317. https://doi.org/10.1007/s00253-009-2309-9
van der Star, Wouter R. L., Dijkema, Cor, de Waard, Pieter, Picioreanu, Cristian, Strous, Marc, and van Loosdrecht, Mark C. M. 2010. “An intracellular pH gradient in the anammox bacterium Kuenenia stuttgartiensis as evaluated by P-31 NMR”. APPLIED MICROBIOLOGY AND BIOTECHNOLOGY 86 (1): 311-317.
van der Star, W. R. L., Dijkema, C., de Waard, P., Picioreanu, C., Strous, M., and van Loosdrecht, M. C. M. (2010). An intracellular pH gradient in the anammox bacterium Kuenenia stuttgartiensis as evaluated by P-31 NMR. APPLIED MICROBIOLOGY AND BIOTECHNOLOGY 86, 311-317.
van der Star, W.R.L., et al., 2010. An intracellular pH gradient in the anammox bacterium Kuenenia stuttgartiensis as evaluated by P-31 NMR. APPLIED MICROBIOLOGY AND BIOTECHNOLOGY, 86(1), p 311-317.
W.R.L. van der Star, et al., “An intracellular pH gradient in the anammox bacterium Kuenenia stuttgartiensis as evaluated by P-31 NMR”, APPLIED MICROBIOLOGY AND BIOTECHNOLOGY, vol. 86, 2010, pp. 311-317.
van der Star, W.R.L., Dijkema, C., de Waard, P., Picioreanu, C., Strous, M., van Loosdrecht, M.C.M.: An intracellular pH gradient in the anammox bacterium Kuenenia stuttgartiensis as evaluated by P-31 NMR. APPLIED MICROBIOLOGY AND BIOTECHNOLOGY. 86, 311-317 (2010).
van der Star, Wouter R. L., Dijkema, Cor, de Waard, Pieter, Picioreanu, Cristian, Strous, Marc, and van Loosdrecht, Mark C. M. “An intracellular pH gradient in the anammox bacterium Kuenenia stuttgartiensis as evaluated by P-31 NMR”. APPLIED MICROBIOLOGY AND BIOTECHNOLOGY 86.1 (2010): 311-317.

25 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

A 192-heme electron transfer network in the hydrazine dehydrogenase complex.
Akram M, Dietl A, Mersdorf U, Prinz S, Maalcke W, Keltjens J, Ferousi C, de Almeida NM, Reimann J, Kartal B, Jetten MSM, Parey K, Barends TRM., Sci Adv 5(4), 2019
PMID: 31001586
The pH dependency of N-converting enzymatic processes, pathways and microbes: effect on net N2 O production.
Blum JM, Su Q, Ma Y, Valverde-Pérez B, Domingo-Félez C, Jensen MM, Smets BF., Environ Microbiol 20(5), 2018
PMID: 29411510
Ladderane phospholipids form a densely packed membrane with normal hydrazine and anomalously low proton/hydroxide permeability.
Moss FR, Shuken SR, Mercer JAM, Cohen CM, Weiss TM, Boxer SG, Burns NZ., Proc Natl Acad Sci U S A 115(37), 2018
PMID: 30150407
Influence of temperature and pH on the anammox process: A review and meta-analysis.
Tomaszewski M, Cema G, Ziembińska-Buczyńska A., Chemosphere 182(), 2017
PMID: 28499181
Roles of EDTA washing and Ca²⁺ regulation on the restoration of anammox granules inhibited by copper(II).
Zhang ZZ, Cheng YF, Zhou YH, Buayi X, Jin RC., J Hazard Mater 301(), 2016
PMID: 26342580
Exogenous nitrate attenuates nitrite toxicity to anaerobic ammonium oxidizing (anammox) bacteria.
Li G, Vilcherrez D, Carvajal-Arroyo JM, Sierra-Alvarez R, Field JA., Chemosphere 144(), 2016
PMID: 26610295
Ecology and physiology of anaerobic ammonium oxidizing bacteria.
Oshiki M, Satoh H, Okabe S., Environ Microbiol 18(9), 2016
PMID: 26616750
Cytochromes c in Archaea: distribution, maturation, cell architecture, and the special case of Ignicoccus hospitalis.
Kletzin A, Heimerl T, Flechsler J, van Niftrik L, Rachel R, Klingl A., Front Microbiol 6(), 2015
PMID: 26029183
Stoichiometry and kinetics of the anaerobic ammonium oxidation (Anammox) with trace hydrazine addition.
Yao Z, Lu P, Zhang D, Wan X, Li Y, Peng S., Bioresour Technol 198(), 2015
PMID: 26364230
The inner workings of the hydrazine synthase multiprotein complex.
Dietl A, Ferousi C, Maalcke WJ, Menzel A, de Vries S, Keltjens JT, Jetten MS, Kartal B, Barends TR., Nature 527(7578), 2015
PMID: 26479033
Pre-exposure to nitrite in the absence of ammonium strongly inhibits anammox.
Carvajal-Arroyo JM, Puyol D, Li G, Lucero-Acuña A, Sierra-Álvarez R, Field JA., Water Res 48(), 2014
PMID: 24091185
Re-interpretation of the evidence for the PVC cell plan supports a Gram-negative origin.
Devos DP., Antonie Van Leeuwenhoek 105(2), 2014
PMID: 24292377
Reverse-transcriptional gene expression of anammox and ammonia-oxidizing archaea and bacteria in soybean and rice paddy soils of Northeast China.
Wang J, Dong H, Wang W, Gu JD., Appl Microbiol Biotechnol 98(6), 2014
PMID: 24077726
Subcellular localization of an ATPase in anammox bacteria using proteomics and immunogold electron microscopy.
Karlsson R, Karlsson A, Bäckman O, Johansson BR, Hulth S., FEMS Microbiol Lett 354(1), 2014
PMID: 24635406
The role of pH on the resistance of resting- and active anammox bacteria to NO2- inhibition.
Carvajal-Arroyo JM, Puyol D, Li G, Sierra-Álvarez R, Field JA., Biotechnol Bioeng 111(10), 2014
PMID: 24771200
High pH (and not free ammonia) is responsible for Anammox inhibition in mildly alkaline solutions with excess of ammonium.
Puyol D, Carvajal-Arroyo JM, Li GB, Dougless A, Fuentes-Velasco M, Sierra-Alvarez R, Field JA., Biotechnol Lett 36(10), 2014
PMID: 24930100
Starved anammox cells are less resistant to NO₂⁻ inhibition.
Carvajal-Arroyo JM, Puyol D, Li G, Swartwout A, Sierra-Álvarez R, Field JA., Water Res 65(), 2014
PMID: 25108528
Inhibition of anaerobic ammonium oxidizing (anammox) enrichment cultures by substrates, metabolites and common wastewater constituents.
Carvajal-Arroyo JM, Sun W, Sierra-Alvarez R, Field JA., Chemosphere 91(1), 2013
PMID: 23245574
How to make a living from anaerobic ammonium oxidation.
Kartal B, de Almeida NM, Maalcke WJ, Op den Camp HJ, Jetten MS, Keltjens JT., FEMS Microbiol Rev 37(3), 2013
PMID: 23210799
Multiple Rieske/cytb complexes in a single organism.
ten Brink F, Schoepp-Cothenet B, van Lis R, Nitschke W, Baymann F., Biochim Biophys Acta 1827(11-12), 2013
PMID: 23507620
Genomic analysis indicates the presence of an asymmetric bilayer outer membrane in planctomycetes and verrucomicrobia.
Speth DR, van Teeseling MC, Jetten MS., Front Microbiol 3(), 2012
PMID: 22934092
Anaerobic ammonium-oxidizing bacteria: unique microorganisms with exceptional properties.
van Niftrik L, Jetten MS., Microbiol Mol Biol Rev 76(3), 2012
PMID: 22933561
Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function.
Fuerst JA, Sagulenko E., Nat Rev Microbiol 9(6), 2011
PMID: 21572457
A predicted physicochemically distinct sub-proteome associated with the intracellular organelle of the anammox bacterium Kuenenia stuttgartiensis.
Medema MH, Zhou M, van Hijum SA, Gloerich J, Wessels HJ, Siezen RJ, Strous M., BMC Genomics 11(), 2010
PMID: 20459862
Intracellular localization of membrane-bound ATPases in the compartmentalized anammox bacterium 'Candidatus Kuenenia stuttgartiensis'.
van Niftrik L, van Helden M, Kirchen S, van Donselaar EG, Harhangi HR, Webb RI, Fuerst JA, Op den Camp HJ, Jetten MS, Strous M., Mol Microbiol 77(3), 2010
PMID: 20545867

31 References

Daten bereitgestellt von Europe PubMed Central.

Proton gradients in intact cyanobacteria.
Belkin S, Mehlhorn RJ, Packer L, Packer L., Plant Physiol. 84(), 1987
PMID: 11539679
Coupling between the sodium and proton gradients in respiring Escherichia coli cells measured by 23Na and 31P nuclear magnetic resonance.
Castle AM, Macnab RM, Shulman RG., J. Biol. Chem. 261(17), 1986
PMID: 3011799
Phosphorus-31 nuclear magnetic resonance studies of the effect of oxygen upon glycolysis in yeast.
den Hollander JA, Ugurbil K, Brown TR, Shulman RG., Biochemistry 20(20), 1981
PMID: 7028113
Enrichment and characterization of an anammox bacterium from a rotating biological contactor treating ammonium-rich leachate.
Egli K, Fanger U, Alvarez PJ, Siegrist H, van der Meer JR, Zehnder AJ., Arch. Microbiol. 175(3), 2001
PMID: 11357512
Intracellular compartmentation in planctomycetes.
Fuerst JA., Annu. Rev. Microbiol. 59(), 2005
PMID: 15910279
Measurement of intracellular (compartmental) pH by 31P NMR in Aspergillus niger.
Hesse SJ, Ruijter GJ, Dijkema C, Visser J., J. Biotechnol. 77(1), 2000
PMID: 10674210
Determination of the mitochondrial protonmotive force in isolated hepatocytes.
Hoek JB, Nicholls DG, Williamson JR., J. Biol. Chem. 255(4), 1980
PMID: 7354039
Biochemistry and molecular biology of anammox bacteria
Jetten MSM, Niftrik L, Strous M, Kartal B, Keltjens JT, Op HJM., 2009
Identification of key proteins involved in the anammox reaction.
Karlsson R, Karlsson A, Backman O, Johansson BR, Hulth S., FEMS Microbiol. Lett. 297(1), 2009
PMID: 19558586
Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell.
Lindsay MR, Webb RI, Strous M, Jetten MS, Butler MK, Forde RJ, Fuerst JA., Arch. Microbiol. 175(6), 2001
PMID: 11491082
Start-up and enrichment of a granular anammox SBR to treat high nitrogen load wastewaters
López H, Puig S, Ganigué R, Ruscalleda M, Balaguer MD, Colprim J., 2008
Phosphorus-31 nuclear magnetic resonance studies of intracellular pH, phosphate compartmentation and phosphate transport in yeasts
Nicolay K, Scheffers WA, Bruinenberg PM, Kaptein R., 1982
The relation between the internal phosphorylation potential and the proton motive force in mitochondria during ATP synthesis and hydrolysis.
Ogawa S, Lee TM., J. Biol. Chem. 259(16), 1984
PMID: 6469951
Ladderane lipid distribution in four genera of anammox bacteria.
Rattray JE, van de Vossenberg J, Hopmans EC, Kartal B, van Niftrik L, Rijpstra WI, Strous M, Jetten MS, Schouten S, Sinninghe Damste JS., Arch. Microbiol. 190(1), 2008
PMID: 18385981
Estimation of cytoplasmic and vacuolar pH in higher plant cells by phosphorus-31 NMR
Roberts JKM, Ray PM, Wade-Jardetzky N, Jardetzky O., 1980
Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation.
Schmid M, Twachtmann U, Klein M, Strous M, Juretschko S, Jetten M, Metzger JW, Schleifer KH, Wagner M., Syst. Appl. Microbiol. 23(1), 2000
PMID: 10879983
Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity.
Schmid MC, Risgaard-Petersen N, van de Vossenberg J, Kuypers MM, Lavik G, Petersen J, Hulth S, Thamdrup B, Canfield D, Dalsgaard T, Rysgaard S, Sejr MK, Strous M, den Camp HJ, Jetten MS., Environ. Microbiol. 9(6), 2007
PMID: 17504485
Stable carbon isotopic fractionations associated with inorganic carbon fixation by anaerobic ammonium-oxidizing bacteria.
Schouten S, Strous M, Kuypers MM, Rijpstra WI, Baas M, Schubert CJ, Jetten MS, Sinninghe Damste JS., Appl. Environ. Microbiol. 70(6), 2004
PMID: 15184193
Identification of organelles in bacteria similar to acidocalcisomes of unicellular eukaryotes.
Seufferheld M, Vieira MC, Ruiz FA, Rodrigues CO, Moreno SN, Docampo R., J. Biol. Chem. 278(32), 2003
PMID: 12783865
Linearly concatenated cyclobutane lipids form a dense bacterial membrane.
Sinninghe Damste JS, Strous M, Rijpstra WI, Hopmans EC, Geenevasen JA, van Duin AC, van Niftrik LA, Jetten MS., Nature 419(6908), 2002
PMID: 12384695
The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms
Strous M, Heijnen JJ, Kuenen JG, Jetten MSM., 1998
Missing lithotroph identified as new planctomycete.
Strous M, Fuerst JA, Kramer EH, Logemann S, Muyzer G, van de Pas-Schoonen KT, Webb R, Kuenen JG, Jetten MS., Nature 400(6743), 1999
PMID: 10440372
Deciphering the evolution and metabolism of an anammox bacterium from a community genome.
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, Medigue C, Collingro A, Snel B, Dutilh BE, Op den Camp HJ, 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, Frishman D, Huynen MA, Mewes HW, Weissenbach J, Jetten MS, Wagner M, Le Paslier D., Nature 440(7085), 2006
PMID: 16598256
The effect of hormones on proton compartmentation in hepatocytes.
Strzelecki T, Thomas JA, Koch CD, LaNoue KF., J. Biol. Chem. 259(7), 1984
PMID: 6323459
Quantification of anaerobic ammonium-oxidizing bacteria in enrichment cultures by real-time PCR.
Tsushima I, Kindaichi T, Okabe S., Water Res. 41(4), 2007
PMID: 17215016
Autotrophic growth of anaerobic ammonium-oxidizing microorganisms in a fluidized bed reactor
Graaf AA, Bruijn P, Robertson LA, Jetten MSM, Kuenen JG., 1996
Metabolic pathway of anaerobic ammonium oxidation on the basis of N studies in a fluidized bed reactor
Graaf AA, Bruijn P, Robertson LA, Jetten MSM, Kuenen JG., 1997
Startup of reactors for anoxic ammonium oxidation: experiences from the first full-scale anammox reactor in Rotterdam.
van der Star WR, Abma WR, Blommers D, Mulder JW, Tokutomi T, Strous M, Picioreanu C, van Loosdrecht MC., Water Res. 41(18), 2007
PMID: 17583763
The membrane bioreactor: a novel tool to grow anammox bacteria as free cells.
van der Star WR, Miclea AI, van Dongen UG, Muyzer G, Picioreanu C, van Loosdrecht MC., Biotechnol. Bioeng. 101(2), 2008
PMID: 18421799
The anammoxosome: an intracytoplasmic compartment in anammox bacteria.
van Niftrik LA, Fuerst JA, Sinninghe Damste JS, Kuenen JG, Jetten MS, Strous M., FEMS Microbiol. Lett. 233(1), 2004
PMID: 15098544
Linking ultrastructure and function in four genera of anaerobic ammonium-oxidizing bacteria: cell plan, glycogen storage, and localization of cytochrome C proteins.
van Niftrik L, Geerts WJ, van Donselaar EG, Humbel BM, Webb RI, Fuerst JA, Verkleij AJ, Jetten MS, Strous M., J. Bacteriol. 190(2), 2007
PMID: 17993524
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