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Insights into the Autotrophic CO₂ Fixation Pathway of the Archaeon Ignicoccus hospitalis: Comprehensive Analysis of the Central Carbon Metabolism

Ulrike Jahn,¹ Harald Huber,^1* Wolfgang Eisenreich,² Michael Hügler,^3, and Georg Fuchs^3*

Lehrstuhl Mikrobiologie und Archaeenzentrum, Universität Regensburg, Universitätsstr. 31, D-93053 Regensburg, Germany,¹ Lehrstuhl für Organische Chemie und Biochemie, Technische Universität München, Lichtenbergstr. 4, D-85748 Garching, Germany,² Mikrobiologie, Fakultät Biologie, Universität Freiburg, Schänzlestr. 1, D-79104 Freiburg, Germany³

Received 10 January 2007/ Accepted 19 March 2007

Ignicoccus hospitalis is an autotrophic hyperthermophilic archaeon that serves as a host for another parasitic/symbiotic archaeon, Nanoarchaeum equitans. In this study, the biosynthetic pathways of I. hospitalis were investigated by in vitro enzymatic analyses, in vivo ¹³C-labeling experiments, and genomic analyses. Our results suggest the operation of a so far unknown pathway of autotrophic CO₂ fixation that starts from acetyl-coenzyme A (CoA). The cyclic regeneration of acetyl-CoA, the primary CO₂ acceptor molecule, has not been clarified yet. In essence, acetyl-CoA is converted into pyruvate via reductive carboxylation by pyruvate-ferredoxin oxidoreductase. Pyruvate-water dikinase converts pyruvate into phosphoenolpyruvate (PEP), which is carboxylated to oxaloacetate by PEP carboxylase. An incomplete citric acid cycle is operating: citrate is synthesized from oxaloacetate and acetyl-CoA by a (re)-specific citrate synthase, whereas a 2-oxoglutarate-oxidizing enzyme is lacking. Further investigations revealed that several special biosynthetic pathways that have recently been described for various archaea are operating. Isoleucine is synthesized via the uncommon citramalate pathway and lysine via the -aminoadipate pathway. Gluconeogenesis is achieved via a reverse Embden-Meyerhof pathway using a novel type of fructose 1,6-bisphosphate aldolase. Pentosephosphates are formed from hexosephosphates via the suggested ribulose-monophosphate pathway, whereby formaldehyde is released from C-1 of hexose. The organism may not contain any sugar-metabolizing pathway. This comprehensive analysis of the central carbon metabolism of I. hospitalis revealed further evidence for the unexpected and unexplored diversity of metabolic pathways within the (hyperthermophilic) archaea.

Published ahead of print on 30 March 2007.

Present address: Leibniz-Institut für Meereswissenschaften, IFM-GEOMAR, Kiel, Germany.

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