Genomic and proteomic characterization of “ Candidatus Nitrosopelagicus brevis”: An ammonia-oxidizing archaeon from the open ocean

Abstract

Thaumarchaeota are among the most abundant microbial cells in the ocean, but difficulty in cultivating marine Thaumarchaeota has hindered investigation into the physiological and evolutionary basis of their success. We report here a closed genome assembled from a highly enriched culture of the ammonia-oxidizing pelagic thaumarchaeon CN25, originating from the open ocean. The CN25 genome exhibits strong evidence of genome streamlining, including a 1.23-Mbp genome, a high coding density, and a low number of paralogous genes. Proteomic analysis recovered nearly 70% of the predicted proteins encoded by the genome, demonstrating that a high fraction of the genome is translated. In contrast to other minimal marine microbes that acquire, rather than synthesize, cofactors, CN25 encodes and expresses near-complete biosynthetic pathways for multiple vitamins. Metagenomic fragment recruitment indicated the presence of DNA sequences >90% identical to the CN25 genome throughout the oligotrophic ocean. We propose the provisional name "Candidatus Nitrosopelagicus brevis" str. CN25 for this minimalist marine thaumarchaeon and suggest it as a potential model system for understanding archaeal adaptation to the open ocean.nitrification | marine metagenomics | genome streamlining | archaea

Influence of ammonia oxidation rate on thaumarchaeal lipid composition and the TEX 86 temperature proxy

“…This idea is consistent with studies that show a low half-saturation constant (K m ; NH 3 + NH 4 + ) of 98-132 nM for ammonia oxidation by N. maritimus (49,50), and it suggests adaptation to growth under conditions of constantly low energy flux, as typically found in open ocean waters. N. maritimus (as well as all recently characterized Thaumarchaeota) fixes inorganic carbon using an energyefficient hydroxypropionate/hydroxybutyrate (HP/HB) pathway that minimizes input of chemical energy from ATP and yields the products acetate (HP/HB full cycle) and succinate (HP half cycle) (43,51). The results of our chemostat experiments are consistent with this view of broad metabolic adaptation to energy stress in Thaumarchaeota.…”

“…Cell-specific ammonia oxidation rates in the chemostat (1.6-7.1 fmol cell −1 ·d −1 ), as well as those estimated for previous batch cultures (22,35), fall well within activities of natural assemblages in pelagic and coastal settings (0.2-15 and 10 fmol cell −1 ·d −1 , respectively) (8, 10). The slow ammonia oxidation rate additionally resembled the pelagic AOA enrichment, Candidatus Nitrosopelagicus brevis (2 fmol NO 2 − cell −1 ·d −1 ; Td, 98 h) (42,43), as well as North Sea enrichments (2-4 fmol NO 2 − cell −1 ·d −1 ) (44). To examine the relationship between TEX 86 ratios and ammonia oxidation rates in the environment, we measured GDGTs, NO 2 − concentrations, in situ temperatures, and nitrification rates for the upper water column of two locations in the South Atlantic Ocean (Fig.…”

Ammonium and nitrite oxidation at nanomolar oxygen concentrations in oxygen minimum zone waters

“…We used small subunit (SSU) ribosomal rRNA gene pyrosequencing with primers encompassing both Bacteria and Archaea to describe microbial population diversity at 50 m. Between 53% and 58% of all sequences were affiliated with four monophyletic clades within the phylum Thaumarchaeota ( Fig. S1): Nitrosopumilus, Nitrosopelagicus water column A, unaffiliated water column B, and marine benthic group B (38)(39)(40). The most abundant thaumarchaeal phylotype observed was affiliated with the Nitrosopumilus cluster, a group that contains cultivated, ammonium-oxidizing representatives (39) and has been observed in a wide array of marine environments (41,42).…”

Two distinct pools of B12analogs reveal community interdependencies in the ocean

“…Like Prochlorococcus, marine Thaumarchaeota have maintained several genes committed to the biosynthesis of cobalamin in their small genomes. Detection of MCM, NrdJ, BluB, and cobalamin biosynthesis proteins in the proteome of an oceanic thaumarchaeote with a highly streamlined genome, "Candidatus Nitrosopelagicus brevis," implies that cobalamin is actively produced and used in these microbes (45). In Thaumarchaeota, the cobalamin-dependent MCM catalyzes a key step in their exceptionally energy-efficient pathway for carbon fixation (46)(47)(48).…”