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Ecophysiology of ammonia-oxidizing Archaea

Background

The isolation of a marine mesophilic crenarchaeote that grows chemolithoautotrophically by aerobically oxidizing ammonia to nitrite (Könneke et al. 2005) was lately described. The strain, named candidatus Nitrosopumilus maritimus, represents the first nitrifier within the domain Archaea. This study also correlated for the first time the presence of archaeal ammonia-monooxygenase (AMO)-encoding genes with the biological conversion of ammonia to nitrite. The archaeal amoA gene was subsequently used as molecular target to demonstrate the ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean (Francis et al. 2005). Analysis of this gene also indicated that archaeal ammonia oxidizers are more abundant in soil than their well-known bacterial counterparts (Leininger et al. 2006). Similar findings were recently obtained from natural water samples of the North Sea and the Atlantic Ocean where archaeal amoA genes were detected in copy numbers up to three orders of magnitudes higher than those of bacterial amoA genes (Wuchter et al. 2006). Estimates based on biomass production confirmed the hypothesis that Crenarchaeota might be the most abundant nitrifiers in the ocean (Ingalls et al. 2006). Nitrification is a central biological process in the global nitrogen cycles. The complete oxidation of ammonia, has been thought so far, involves only two physiological distinct groups of microorganisms, the ammonia-oxidizing bacteria (AOB) and the nitrite-oxidizing bacteria (NOB) (Bock and Wagner, 2000. All cultured nitrifiers are chemolithoautotrophs and obligate aerobes. Most of the AOB and NOB fix inorganic carbon by the Calvin-Benson pathway. Only a few fix CO2 by the phosphoenolpyruvate carboxylase (Harms et al. 1981, Takahashi et al 1993). Based on tracer studies it is suggested that the oxidation of ammonia to nitrite is the rate-limiting step of nitrification in nature (Bock and Wagner, 2000). The discovery of archaeal ammonia-oxidation in N. maritimus might now challenge the current perspective on biological nitrification and the impact of AOB on the nitrogen cycle (Nicol and Schleper, 2006). Nitrogen is a limiting factor in many ecosystems, and the abundant crenarchaeal nitrifiers represent key players in the competition for ammonia or other reduced nitrogen compounds. Furthermore, The global crenarchaeal inorganic carbon fixation in the ocean was estimated between 3.3 and 6.5 · 1013 mol carbon per year, accounting for approximately one percent of the annual marine primary production (Herndl et al. 2005, Ingalls et al. 2006, Wuchter et al. 2006).


Goals

The main goal of our research is to understand the ecophysiology of ammonia-oxidizing archaea. We aim to discover biochemical pathways involved in the chemolithoautotrophic lifestyle of the only existing pure culture. The studies are being performed in close collaboration with David Stahl and colleagues at the University of Washington and are facilitated by the ongoing whole genome analysis at the Joint Genome Institute. Biochemical and classical microbiological analysis are being applied to investigate the mechanisms mechanisms of carbon metabolism and to approve hypothetical pathways.


The phylogenetic diversity of archaeal amoA and 16S rRNA-genes suggests the existence of various physiotypes. A current project in our lab deals with the isolation of further AOA strains from aquatic and terrestrial environments where the corresponding biomarkers have prevoiusly been detected. The new strains will be characterized physiologically and will help to understand the suggested high impact on the biogeochemical nitrogen and carbon cycles.

Investigators

Collaboration
  • University of Washington, Seattle, USA (David A. Stahl, José de la Torre,
    Willm Martens Habbena, Chris Walker)
  • IFM-GEOMAR, Kiel (Michael Hügler)
  • WHOI, Woods Hole, USA (Stefan Sievert)
  • NIOZ, Den Burg, The Netherlands (Jaap Sinninghe Damsté, Stefan Schouten)
  • Radboud University, Nijmegen, The Netherlands (Huub Obdencamp, Suzanne Haaijer)

Publications and presentations on this topic

De la Torre JR, Walker CB, Ingalls AE, Könneke M, Stahl D (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10:810–818

Könneke M (2008) New Crenarchaeota - the organismic link in the nitrogen cycle. In: Amann R, Goebel W, Reinhold-Hurek B, Schink B, Widdel F; (Eds.) Life strategies of microorganisms in the environment and in host organisms, Nova Acta Leopoldina NF 96, Nr. 356, ISBN: 978--3-8047-2499-0, Suppl. 3-8

Schouten S, Hopmans EC, Baas M, Boumann H, Standfest S, Könneke M, Stahl DA, Damste JSS (2008) Intact membrane lipids of "Candidatus Nitrosopumilus maritimus", a cultivated representative of the cosmopolitan mesophilic group I Crenarchaeota. Appl Environ Microbiol 74:2433-2440

Könneke M., Bernhard, A. E., de la Torré, J. R., Walker, C. B., Waterbury, J. B., Stahl, D. A. (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437: 543-546

Martin Könneke (Oral presentation, Leopoldina Symposium: Life strategies of microorganisms in the environment and in host organisms, 2006) New Crenarchaeota - The organismic link in the nitrogen cycle

Sonja Standfest, Heribert Cypionka and Martin Könneke (Poster, VAAM Annual-meeting 2007) Determination of growth characteristics of the ammonia-oxidizing crenarchaeon candidatus "Nitrosopumilus maritimus"

Martin Könneke (Oral presentation, ASM General meeting 2007) Nitrifying archaea.

Ellen C. HOPMANS, Stefan SCHOUTEN, Marianne BAAS, Henry BOUMANN, Sonja STANDFEST, Martin Könneke, David A. STAHL, and Jaap S. SINNINGHE DAMSTÉ (Poster, IMOG 2007)Membrane lipids of Candidatus "Nitrosopumilus maritimus", a cultivated isolate from the ubiquitous marine Crenarchaeota

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