Carbon dioxide fixation in ‘Archaeoglobus lithotrophicus’: are there multiple autotrophic pathways?

Abstract

Several representatives of the euryarchaeal class Archaeoglobi are able to grow facultative autotrophically using the reductive acetyl-CoA pathway, with 'Archaeoglobus lithotrophicus' being an obligate autotroph. However, genome sequencing revealed that some species harbor genes for key enzymes of other autotrophic pathways, i.e. 4-hydroxybutyryl-CoA dehydratase of the dicarboxylate/hydroxybutyrate cycle and the hydroxypropionate/hydroxybutyrate cycle and ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) of the Calvin-Benson cycle. This raised the question of whether only one or multiple autotrophic pathways are operating in these species. We searched for the presence of enzyme activities specific for the dicarboxylate/hydroxybutyrate or the hydroxypropionate/hydroxybutyrate cycles in 'A. lithotrophicus', but such enzymes could not be detected. Low Rubisco activity was detected that could not account for the carbon dioxide (CO(2)) fixation rate; in addition, phosphoribulokinase activity was not found. The generation of ribulose 1,5-bisphosphate from 5-phospho-D-ribose 1-pyrophosphate was observed, but not from AMP; these sources for ribulose 1,5-bisphosphate have been proposed before. Our data indicate that the reductive acetyl-CoA pathway is the only functioning CO(2) fixation pathway in 'A. lithotrophicus'.

Identification of key components in the energy metabolism of the hyperthermophilic sulfate-reducing archaeon Archaeoglobus fulgidus by transcriptome analyses

“…Carboxylase activity has been verified in A. fulgidus (Watson et al, 1999). However, the role of RuBisCo in anaerobic Archaea may relate to ribulose 1,5-bisphosphate recycling, or AMP metabolism, rather than a carbon assimilation mechanism (Sato et al, 2007; Estelmann et al, 2011). …”

“…The differential transcriptional expression of 4hcd (Msed1321) in M. sedula was related to autotrophic vs. heterotrophic growth and resulted in a more than 7 fold up-regulation (Auernik and Kelly, 2010). The presence of a 3HP/4HB cycle was refuted by Estelmann et al (2011) by a subsequent study on the obligate autotroph “ A. litotrophicus ,” where enzyme activity of key processes could not be detected. The presence of 5 homologs of A. fulgidus 4hcd in the genome of Desulfatibacillum alkenivorans suggest that this enzyme is involved in alkene degradation in these species (Estelmann et al, 2011).…”

“…The genes related to fatty acid biosynthesis also encode enzymes in the 3-hydroxypropionate/4-hydroxybutyrate (3HP/4HB) cycle identified in Metallosphaera sedula , and could potentially represent a secondary carbon fixation pathway in A. fulgidus (Berg et al, 2007; Estelmann et al, 2011). The genome of A. fulgidus includes 3 homologs of the 4-hydroxybutyryl-CoA dehydratase ( 4hcd ), (AF0333, AF0885 and AF1027, Table S1c), which is a key enzyme of the 4-hydroxybutyrate carbon dioxide assimilation pathway (Figure 7) (Berg et al, 2007).…”

“…In addition, A. fulgidus grows carboxydotrophically on CO/CO 2 and as a chemoorganoheterotroph utilizing a wide range of substrates including fatty acids, alkenes, complex peptides, and specific amino acids (Stetter et al, 1987; Stetter, 1988; Hartzell and Reed, 2006; Henstra et al, 2007; Khelifi et al, 2010; Parthasarathy et al, 2013). For the complete oxidation of organic substrates to CO 2 , A. fulgidus uses a modified acetyl-CoA pathway with similar enzymes and cofactors as in the methanogens (Möller-Zinkhan et al, 1989; Möller-Zinkhan and Thauer, 1990; Vorholt et al, 1995; Estelmann et al, 2011). Reduction of sulfate (SO 2− 4 ) to sulfide (S 2− ) in A. fulgidus proceeds via the highly conserved dissimilatory sulfate reduction pathway of the SRP (Peck, 1962; Klenk et al, 1997; Pereira et al, 2011).…”

A Post-Genomic View of the Ecophysiology, Catabolism and Biotechnological Relevance of Sulphate-Reducing Prokaryotes

“…In recent years, several novel CO 2 -fixation pathways have been discovered, e.g., the hydroxypropionate/hydroxybutyrate cycle (for overview, see Fuchs, 2011;. In Archaeoglobus lithotrophicus, previously demonstrated to employ the Wood-Ljungdahl pathway for autotrophic CO 2 fixation (Vorholt, Kunow, Stetter, & Thauer, 1995), enzymatic studies could not demonstrate the activities of the dicarboxylate/hydroxybutyrate or the hydroxypropionate/hydroxybutyrate cycle (Estelmann et al, 2011).…”