Abstract
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.
Highlights
Crenarchaeota are abundant in the world’s oceans, comprising an estimated 20% of all planktonic prokaryotes [1,2]
Radiocarbon analyses of 14C in lipid biomarkers associated with marine plankton [14], and 13C-labeled bicarbonate tracer studies [15] suggest that marine Crenarchaeota are capable of light-independent autotrophic carbon assimilation into membrane lipid biomass, an hypothesis further strengthened by recent single cell phylogenetic identification and autoradiographic verification of carbon dioxide incorporation [16]
Eight C. symbiosum SSU rRNA genes were identified in the second library, representing approximately 0.38% of the total clone population [31]
Summary
Crenarchaeota are abundant in the world’s oceans, comprising an estimated 20% of all planktonic prokaryotes [1,2] They are distributed over a wide depth range, spanning both euphotic and aphotic zones [3,4,5], and at least one species, Cenarchaeum symbiosum, has a symbiotic association with the marine sponge Axinella mexicana [6]. Planktonic Archaea produce glycerol dialkyl glycerol tetraethers [9,10,11], including one unique structure crenarchaeol [7,12,13] often considered a diagnostic biomarker for planktonic archaeal species It remains unclear if this compound is unique to marine Crenarchaeota, or is found in both euryarchaeotal lineages, too. The direct incorporation of dissolved inorganic carbon by marine Crenarchaeota may be homologous to metabolic properties of more distantly related thermophilic Crenarchaeota that utilize a modified 3-hydroxypropionate [17,18,19,20,21] or reductive tricarboxylic acid [22,23,24] cycle for autotrophic carbon assimilation
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