Deciphering the evolution and metabolism of an anammox bacterium from a community genome

Marc Strous; Eric Pelletier; Sophie Mangenot; Thomas Rattei; Angelika Lehner; Michael W. Taylor; Matthias Horn; Holger Daims; Delphine Bartol-Mavel; Patrick Wincker; Valérie Barbe; Nuria Fonknechten; David Vallenet; Béatrice Segurens; Chantal Schenowitz-Truong; Claudine Médigue; Astrid Collingro; Berend Snel; Bas E. Dutilh; Huub J.M. Op Den Camp; Chris Van Der Drift; Irina Cirpus; Katinka T. Van De Pas-Schoonen; Harry R. Harhangi; Laura Van Niftrik; Markus Schmid; Jan Keltjens; Jack Van De Vossenberg; Boran Kartal; Harald Meier; Dmitrij Frishman; Martijn A. Huynen; Hans Werner Mewes; Jean Weissenbach; Mike S.M. Jetten; Michael Wagner; Denis Le Paslier

doi:10.1038/nature04647

Deciphering the evolution and metabolism of an anammox bacterium from a community genome

Marc Strous, Eric Pelletier, Sophie Mangenot, Thomas Rattei, Angelika Lehner, Michael W. Taylor, Matthias Horn, Holger Daims, Delphine Bartol-Mavel, Patrick Wincker, Valérie Barbe, Nuria Fonknechten, David Vallenet, Béatrice Segurens, Chantal Schenowitz-Truong, Claudine Médigue, Astrid Collingro, Berend Snel, Bas E. Dutilh, Huub J.M. Op Den CampChris Van Der Drift, Irina Cirpus, Katinka T. Van De Pas-Schoonen, Harry R. Harhangi, Laura Van Niftrik, Markus Schmid, Jan Keltjens, Jack Van De Vossenberg, Boran Kartal, Harald Meier, Dmitrij Frishman, Martijn A. Huynen, Hans Werner Mewes, Jean Weissenbach, Mike S.M. Jetten, Michael Wagner, Denis Le Paslier

Life Sciences

Research output: Contribution to journal › Article › peer-review

1169 Scopus citations

Abstract

Anaerobic ammonium oxidation (anammox) has become a main focus in oceanography and wastewater treatment^1,2. It is also the nitrogen cycle's major remaining biochemical enigma. Among its features, the occurrence of hydrazine as a free intermediate of catabolism^3,4, the biosynthesis of ladderane lipids^5,6 and the role of cytoplasm differentiation⁷ are unique in biology. Here we use environmental genomics^8,9 - the reconstruction of genomic data directly from the environment - to assemble the genome of the uncultured anammox bacterium Kuenenia stuttgartiensis¹⁰ from a complex bioreactor community. The genome data illuminate the evolutionary history of the Planctomycetes and allow us to expose the genetic blueprint of the organism's special properties. Most significantly, we identified candidate genes responsible for ladderane biosynthesis and biological hydrazine metabolism, and discovered unexpected metabolic versatility.

Original language	English
Pages (from-to)	790-794
Number of pages	5
Journal	Nature
Volume	440
Issue number	7085
DOIs	https://doi.org/10.1038/nature04647
State	Published - 6 Apr 2006

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Strous, M., Pelletier, E., Mangenot, S., Rattei, T., Lehner, A., Taylor, M. W., 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, B. E., ... Le Paslier, D. (2006). Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature, 440(7085), 790-794. https://doi.org/10.1038/nature04647

@article{140aa723c5b541debd7a6faf9a956c18,

title = "Deciphering the evolution and metabolism of an anammox bacterium from a community genome",

abstract = "Anaerobic ammonium oxidation (anammox) has become a main focus in oceanography and wastewater treatment1,2. It is also the nitrogen cycle's major remaining biochemical enigma. Among its features, the occurrence of hydrazine as a free intermediate of catabolism3,4, the biosynthesis of ladderane lipids5,6 and the role of cytoplasm differentiation7 are unique in biology. Here we use environmental genomics8,9 - the reconstruction of genomic data directly from the environment - to assemble the genome of the uncultured anammox bacterium Kuenenia stuttgartiensis10 from a complex bioreactor community. The genome data illuminate the evolutionary history of the Planctomycetes and allow us to expose the genetic blueprint of the organism's special properties. Most significantly, we identified candidate genes responsible for ladderane biosynthesis and biological hydrazine metabolism, and discovered unexpected metabolic versatility.",

author = "Marc Strous and Eric Pelletier and Sophie Mangenot and Thomas Rattei and Angelika Lehner and Taylor, {Michael W.} and Matthias Horn and Holger Daims and Delphine Bartol-Mavel and Patrick Wincker and Val{\'e}rie Barbe and Nuria Fonknechten and David Vallenet and B{\'e}atrice Segurens and Chantal Schenowitz-Truong and Claudine M{\'e}digue and Astrid Collingro and Berend Snel and Dutilh, {Bas E.} and {Op Den Camp}, {Huub J.M.} and {Van Der Drift}, Chris and Irina Cirpus and {Van De Pas-Schoonen}, {Katinka T.} and Harhangi, {Harry R.} and {Van Niftrik}, Laura and Markus Schmid and Jan Keltjens and {Van De Vossenberg}, Jack and Boran Kartal and Harald Meier and Dmitrij Frishman and Huynen, {Martijn A.} and Mewes, {Hans Werner} and Jean Weissenbach and Jetten, {Mike S.M.} and Michael Wagner and {Le Paslier}, Denis",

note = "Funding Information: Acknowledgements Preliminary sequence data from G. obscuriglobus was obtained from The Institute for Genomic Research through the website at http://www.tigr.org. Sequencing of G. obscuriglobus was accomplished with support from the United States Department of Energy. A. Cabezas is acknowledged for technical assistance. M.H., A.C. and M.W. were supported by the Austrian Ministry for Science and Education. M.T. was funded by the German Federal Ministry for Education and Research (Biolog II). H.D. was supported by the Wiener Wissenschafts-, Forschungs-und Technologiefonds (WWTF). We thank B. Anneser, F. Maixner, M. Leitner, A. Pol and B. Meijerink for help in the first round annotation and M. Ott for his effort in high performance phylogenetic treeing. The Dutch anammox research was supported by the Netherlands Science Foundation for Earth and Life Science (ALW), the Foundation for Applied Research (STW) and the European Union. The Radboud University and S. Wendelaar Bonga financially supported the initial phase of the project.",

year = "2006",

month = apr,

day = "6",

doi = "10.1038/nature04647",

language = "English",

volume = "440",

pages = "790--794",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Research",

number = "7085",

}

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, Frishman, D, Huynen, MA, Mewes, HW, Weissenbach, J, Jetten, MSM, Wagner, M & Le Paslier, D 2006, 'Deciphering the evolution and metabolism of an anammox bacterium from a community genome', Nature, vol. 440, no. 7085, pp. 790-794. https://doi.org/10.1038/nature04647

TY - JOUR

T1 - Deciphering the evolution and metabolism of an anammox bacterium from a community genome

AU - Strous, Marc

AU - Pelletier, Eric

AU - Mangenot, Sophie

AU - Rattei, Thomas

AU - Lehner, Angelika

AU - Taylor, Michael W.

AU - Horn, Matthias

AU - Daims, Holger

AU - Bartol-Mavel, Delphine

AU - Wincker, Patrick

AU - Barbe, Valérie

AU - Fonknechten, Nuria

AU - Vallenet, David

AU - Segurens, Béatrice

AU - Schenowitz-Truong, Chantal

AU - Médigue, Claudine

AU - Collingro, Astrid

AU - Snel, Berend

AU - Dutilh, Bas E.

AU - Op Den Camp, Huub J.M.

AU - Van Der Drift, Chris

AU - Cirpus, Irina

AU - Van De Pas-Schoonen, Katinka T.

AU - Harhangi, Harry R.

AU - Van Niftrik, Laura

AU - Schmid, Markus

AU - Keltjens, Jan

AU - Van De Vossenberg, Jack

AU - Kartal, Boran

AU - Meier, Harald

AU - Frishman, Dmitrij

AU - Huynen, Martijn A.

AU - Mewes, Hans Werner

AU - Weissenbach, Jean

AU - Jetten, Mike S.M.

AU - Wagner, Michael

AU - Le Paslier, Denis

N1 - Funding Information: Acknowledgements Preliminary sequence data from G. obscuriglobus was obtained from The Institute for Genomic Research through the website at http://www.tigr.org. Sequencing of G. obscuriglobus was accomplished with support from the United States Department of Energy. A. Cabezas is acknowledged for technical assistance. M.H., A.C. and M.W. were supported by the Austrian Ministry for Science and Education. M.T. was funded by the German Federal Ministry for Education and Research (Biolog II). H.D. was supported by the Wiener Wissenschafts-, Forschungs-und Technologiefonds (WWTF). We thank B. Anneser, F. Maixner, M. Leitner, A. Pol and B. Meijerink for help in the first round annotation and M. Ott for his effort in high performance phylogenetic treeing. The Dutch anammox research was supported by the Netherlands Science Foundation for Earth and Life Science (ALW), the Foundation for Applied Research (STW) and the European Union. The Radboud University and S. Wendelaar Bonga financially supported the initial phase of the project.

PY - 2006/4/6

Y1 - 2006/4/6

N2 - Anaerobic ammonium oxidation (anammox) has become a main focus in oceanography and wastewater treatment1,2. It is also the nitrogen cycle's major remaining biochemical enigma. Among its features, the occurrence of hydrazine as a free intermediate of catabolism3,4, the biosynthesis of ladderane lipids5,6 and the role of cytoplasm differentiation7 are unique in biology. Here we use environmental genomics8,9 - the reconstruction of genomic data directly from the environment - to assemble the genome of the uncultured anammox bacterium Kuenenia stuttgartiensis10 from a complex bioreactor community. The genome data illuminate the evolutionary history of the Planctomycetes and allow us to expose the genetic blueprint of the organism's special properties. Most significantly, we identified candidate genes responsible for ladderane biosynthesis and biological hydrazine metabolism, and discovered unexpected metabolic versatility.

AB - Anaerobic ammonium oxidation (anammox) has become a main focus in oceanography and wastewater treatment1,2. It is also the nitrogen cycle's major remaining biochemical enigma. Among its features, the occurrence of hydrazine as a free intermediate of catabolism3,4, the biosynthesis of ladderane lipids5,6 and the role of cytoplasm differentiation7 are unique in biology. Here we use environmental genomics8,9 - the reconstruction of genomic data directly from the environment - to assemble the genome of the uncultured anammox bacterium Kuenenia stuttgartiensis10 from a complex bioreactor community. The genome data illuminate the evolutionary history of the Planctomycetes and allow us to expose the genetic blueprint of the organism's special properties. Most significantly, we identified candidate genes responsible for ladderane biosynthesis and biological hydrazine metabolism, and discovered unexpected metabolic versatility.

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U2 - 10.1038/nature04647

DO - 10.1038/nature04647

M3 - Article

C2 - 16598256

AN - SCOPUS:33645741019

SN - 0028-0836

VL - 440

SP - 790

EP - 794

JO - Nature

JF - Nature

IS - 7085

ER -

Deciphering the evolution and metabolism of an anammox bacterium from a community genome

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