Pathways of Carbon Assimilation and Ammonia Oxidation Suggested by Environmental Genomic Analyses of Marine Crenarchaeota

By S. Hallam, T. Mincer, C. Schleper, C. Preston, Katie Roberts, Paul Richardson, E. Delong. PLoS Biology, 2006

617 citations recorded by the source corpus.

Marine Crenarchaeota represent an abundant component of oceanic microbiota with potential to significantly influence biogeochemical cycling in marine ecosystems. Prior studies using specific archaeal lipid biomarkers and isotopic analyses indicated that planktonic Crenarchaeota have the capacity for autotrophic growth, and more recent cultivation studies support an ammonia-based chemolithoautotrophic energy metabolism. We report here analysis of fosmid sequences derived from the uncultivated marine crenarchaeote, Cenarchaeum symbiosum, focused on the reconstruction of carbon and energy metabolism. Genes predicted to encode multiple components of a modified 3-hydroxypropionate cycle of autotrophic carbon assimilation were identified, consistent with utilization of carbon dioxide as a carbon source. Additionally, genes predicted to encode a near complete oxidative tricarboxylic acid cycle were also identified, consistent with the consumption of organic carbon and in the production of intermediates for amino acid and cofactor biosynthesis. Therefore, C. symbiosum has the potential to function either as a strict autotroph, or as a mixotroph utilizing both carbon dioxide and organic material as carbon sources. From the standpoint of energy metabolism, genes predicted to encode ammonia monooxygenase subunits, ammonia permease, urease, and urea transporters were identified, consistent with the use of reduced nitrogen compounds as energy sources fueling autotrophic metabolism. Homologues of these genes, recovered from ocean waters worldwide, demonstrate the conservation and ubiquity of crenarchaeal pathways for carbon assimilation and ammonia oxidation. These findings further substantiate the likely global metabolic importance of Crenarchaeota with respect to key steps in the biogeochemical transformation of carbon and nitrogen in marine ecosystems.

Subfields: Ecology, Environmental Chemistry, Oceanography

View Paper: https://www.semanticscholar.org/paper/42933dc793412bc698db2f8863eb1ab4f1109667

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Citations in the corpus

Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. (2009, background): “Genes predicting a modified 3-hydroxypropionate cycle, known in thermophilic archaea, Sulfolobales, metabolizing sulfur, pyrite or hydrogen, were also retrieved from the C. symbiosum genome (Hallam et al., 2006b).”
Distribution and activity of Bacteria and Archaea in the deep water masses of the North Atlantic (2006, background): “Very recently, Crenarchaeota, including the only isolated nonthermophilic archaeon (Nitrosopumilus maritimus gen. et sp. nov.; Könneke et al. 2005) was found to be an ammonia oxidizer, as revealed by the presence of the amoA gene (Hallam et al. 2006).”
Crenarchaeol tracks winter blooms of ammonia‐oxidizing Thaumarchaeota in the coastal North Sea (2011, methodology): “The GDGTs were analyzed by HPLC-MS with atmospheric pressure chemical ionization (APCI) using conditions modified from Hopmans et al. (2000). Analyses were performed using an HP (PaloAlto) 1100 series HPLC-MS equipped with an auto-injector and Chemstation chromatography manager software.”
Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils (2011, background): “Recent progress in ammonia-oxidizing archaea (AOA) studies (Venter et al., 2004; Könneke et al., 2005; Hallam et al., 2006) greatly suggested their putative contributions to the global nitrogen cycle by possessing the potential capacity to oxidize ammonia (Nicol and Schleper, 2006), and phylogenetic”
Nickel Utilization in Phytoplankton Assemblages From Contrasting Oceanic Regimes (2010, result): “Ni uptake outside of the euphotic zone may be linked to urea decomposition (Cho and Azam, 1995) and is consistent with the observation of genes for a Ni-containing urease and a Ni transporter in the genomes of both Bacterial and Archaeal NH4 +-oxidizers (Hallam et al., 2006; Klotz et al., 2007).”
Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil (2011, positive): “…is also suggested by the identi ﬁ cation of genes in the draft genome of N. viennensis encoding key enzymes of the potential carbon ﬁ xation pathway of AOA (the 3-hydroxypropionate/4-hydroxybutyrate cycle) that are present in all thaumarchaeotal genomes (33, 39), as well as in metagenomes (40).”
Examining the global distribution of dominant archaeal populations in soil (2011, background): “…of the Cenarchaeum symbiosum and Nitrosopumilus maritimus genomes, however, suggests these organisms may also be capable of some level of mixotrophy (Hallam et al., 2006; Walker et al., 2010), and additional research will be required in this area before these dynamics can be more fully resolved.”
Opinion: Adaptations to energy stress dictate the ecology and evolution of the Archaea (2007, background): “In the case of nitrifiers there seems to be direct competition involving similar catabolic strategies, the details of which are still emergin”
New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation (2007, background): “For example, AOA, AOB, anammox bacteria and denitrifiers all appear to possess nitrite reductase (nirK/S) genes (Casciotti and Ward, 2001; Treusch et al., 2005; Strous et al., 2006; Hallam et al., 2006b; Cantera and Stein, 2007).”
Community structure of marine bacterioplankton: patterns, networks, and relationships to function (2008, positive): “Further confirmation of this capability, together with other valuable information about autotrophic and mixotrophic functionalities , has come from the metagenomic analysis of Cenarchaeum symbiosum, an uncultivated marine archaeon that lives symbiotically within a sponge (Hallam et al. 2006).”
The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. (2008, background): “The inclusion of marine and soil reference taxa [including those sequences from soil fosmid clone 54d9 (Treusch et al., 2005), C. symbiosum (Hallam et al., 2006) and N. maritimus (Könneke et al., 2005)] provided anchors for inferring congruence.”