A 3-Hydroxypropionate/4-Hydroxybutyrate Autotrophic Carbon Dioxide Assimilation Pathway in Archaea

Mikrobiologie, Fakultät Biologie, Universität Freiburg, Schänzlestrasse 1, D-79104 Freiburg, Germany.
Science (Impact Factor: 33.61). 07/2008; 318(5857):1782-6. DOI: 10.1126/science.1149976
Source: PubMed


The assimilation of carbon dioxide (CO2) into organic material is quantitatively the most important biosynthetic process. We discovered that an autotrophic member of the archaeal order Sulfolobales, Metallosphaera sedula, fixed CO2 with acetyl-coenzyme A (acetyl-CoA)/propionyl-CoA carboxylase as the key carboxylating enzyme. In this system, one acetyl-CoA and two bicarbonate molecules were reductively converted via 3-hydroxypropionate to succinyl-CoA. This intermediate was reduced to 4-hydroxybutyrate and converted into two acetyl-CoA molecules via 4-hydroxybutyryl-CoA dehydratase. The key genes of this pathway were found not only in Metallosphaera but also in Sulfolobus, Archaeoglobus, and Cenarchaeum species. Moreover, the Global Ocean Sampling database contains half as many 4-hydroxybutyryl-CoA dehydratase sequences as compared with those found for another key photosynthetic CO2-fixing enzyme, ribulose-1,5-bisphosphate carboxylase-oxygenase. This indicates the importance of this enzyme in global carbon cycling.

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    • "The MGI clade has been reported to dominate archaeal communities in the global ocean biosphere (Takai et al., 2006) and in the sea waters surrounding the cooler hydrothermal environments (Takai et al., 2004; Dick and Tebo, 2010; Roussel et al., 2011), which is in accordance with our results. The ammonia-oxidizing members of MGI, mostly represented by Candidatus Nitrosopumilus, presumably undergo the predominant type of chemolithoautotrophy in the dark ocean, via the 3-hydroxypropionate/4-hydroxybutyrate cycle (Berg et al., 2007). Other OTUs affiliated to anammox (anaerobic ammonium oxidation) bacteria from the Nitrosomonas and Nitrosococcus genera. "
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    ABSTRACT: Deep-sea hydrothermal sediments are known to support remarkably diverse microbial consortia. Culture-independent sequence-based technologies have extensively been used to disclose the associated microbial diversity as most of the microorganisms inhabiting these ecosystems remain uncultured. Here we provide the first description of the microbial community diversity found on sediments from Menez Gwen vent system. We compared hydrothermally influenced sediments, retrieved from an active vent chimney at 812 m depth, with non-hydrothermally influenced sediments, from a 1400 m depth bathyal plain. Considering the enriched methane and sulfur composition of Menez Gwen vent fluids, and the sediment physicochemical properties in each sampled area, we hypothesized that the site-associated microbes would be different. To address this question, taxonomic profiles of bacterial, archaeal and micro-eukaryotic representatives were studied by rRNA gene tag pyrosequencing. Communities were shown to be significantly different and segregated by sediment geographical area. Specific mesophilic, thermophilic and hyperthermophilic archaeal (e.g., Archaeoglobus, ANME-1) and bacterial (e.g., Caldithrix, Thermodesulfobacteria) taxa were highly abundant near the vent chimney. In contrast, bathyal-associated members affiliated to more ubiquitous phylogroups from deep-ocean sediments (e.g., Thaumarchaeota MGI, Gamma- and Alphaproteobacteria). This study provides a broader picture of the biological diversity and microbial biogeography, and represents a preliminary approach to the microbial ecology associated with the deep-sea sediments from the Menez Gwen hydrothermal vent field.
    Marine Genomics 09/2015; DOI:10.1016/j.margen.2015.09.001 · 1.79 Impact Factor
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    • "Nitrosoarchaeum limnia, revealed carbon fixation via a modified 3-hydroxypropionate/4-hydroxybutyrate cycle (3-HP/4-HB) (Berg et al., 2007; Walker et al., 2010; Blainey et al., 2011; Tourna et al., 2011). The use of this very cost-effective CO 2 fixation pathway by AOA (Könneke et al., 2014) distinguishes them from autotrophic ammonia-oxidizing bacteria, which use the Calvin- Benson-Basham cycle (e.g., Chain et al., 2003; Klotz et al., 2006). "
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    ABSTRACT: Ammonia-oxidizing archaea (AOA) are an important component of the planktonic community in aquatic habitats, linking nitrogen and carbon cycles through nitrification and carbon fixation. Therefore, measurements of these processes in culture-based experiments can provide insights into their contributions to energy conservation and biomass production by specific AOA. In this study, by enriching AOA from a brackish, oxygen-depleted water-column in the Landsort Deep, central Baltic Sea, we were able to investigate ammonium oxidation, chemoautotrophy, and growth in seawater batch experiments. The highly enriched culture consisted of up to 97% archaea, with maximal archaeal numbers of 2.9 × 107 cells mL−1. Phylogenetic analysis of the 16S rRNA and ammonia monooxygenase subunit A (amoA) gene sequences revealed an affiliation with assemblages from low-salinity and freshwater habitats, with Candidatus Nitrosoarchaeum limnia as the closest relative. Growth correlated significantly with nitrite production, ammonium consumption, and CO2 fixation, which occurred at a ratio of 10 atoms N oxidized per 1 atom C fixed. According to the carbon balance, AOA biomass production can be entirely explained by chemoautotrophy. The cellular carbon content was estimated to be 9 fg C per cell. Single-cell-based 13C and 15N labeling experiments and analysis by nano-scale secondary ion mass spectrometry provided further evidence that cellular carbon was derived from bicarbonate and that ammonium was taken up by the cells. Our study therefore revealed that growth by an AOA belonging to the genus Nitrosoarchaeum can be sustained largely by chemoautotrophy.
    Frontiers in Microbiology 01/2015; 5(786). DOI:10.3389/fmicb.2014.00786 · 3.99 Impact Factor
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    • "This assimilation process occurs through various complex biochemical pathways [3]. The distribution of carbon fixation strategies are widespread among prokaryotes and depends on the individual autotrophic organism and is also determined by different habitat characteristics, such as the energy demand, the availability of inorganic compounds (sulphide, elemental sulphur, thiosulphate and sometimes ferrous iron and hydrogen), usage of coenzymes and the oxygen sensitivity of enzymes [4]. "
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    ABSTRACT: Bacterial autotrophy contributes significantly to the overall carbon balance, which stabilises atmospheric CO2 concentration and decelerates global warming. Little attention has been paid to different modes of carbon/sulphur metabolism mediated by autotrophic bacterial communities in terrestrial soil ecosystems. We studied these pathways by analysing the distribution and abundance of the diagnostic metabolic marker genes cbbM, apsA and soxB, which encode for ribulose-1,5-bisphosphate carboxylase/oxygenase, adenosine phosphosulphate reductase and sulphate thiohydrolase, respectively, among different contrasting soil types. Additionally, the abundance of community members was assessed by quantifying the gene copy numbers for 16S rRNA, cbbL, cbbM, apsA and soxB. Distinct compositional differences were observed among the clone libraries, which revealed a dominance of phylotypes associated with carbon and sulphur cycling, such as Gammaproteobacteria (Thiohalomonas, Allochromatium, Chromatium, Thiomicrospira) and Alphaproteobacteria (Rhodopseudomonas, Rhodovulum, Paracoccus). The rhizosphere soil was devoid of sulphur metabolism, as the soxB and apsA genes were not observed in the rhizosphere metagenome, which suggests the absence or inadequate representation of sulphur-oxidising bacteria. We hypothesise that the novel Gammaproteobacteria sulphur oxidisers might be actively involved in sulphur oxidation and inorganic carbon fixation, particularly in barren saline soil ecosystems, suggesting their significant putative ecological role and contribution to the soil carbon pool.
    PLoS ONE 09/2014; 9(9):e107025.. DOI:10.1371/journal.pone.0107025 · 3.23 Impact Factor
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