Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea

Abstract

Ammonia-oxidizing archaea are ubiquitous in marine and terrestrial environments and now thought to be significant contributors to carbon and nitrogen cycling. The isolation of Candidatus "Nitrosopumilus maritimus" strain SCM1 provided the opportunity for linking its chemolithotrophic physiology with a genomic inventory of the globally distributed archaea. Here we report the 1,645,259-bp closed genome of strain SCM1, revealing highly copper-dependent systems for ammonia oxidation and electron transport that are distinctly different from known ammonia-oxidizing bacteria. Consistent with in situ isotopic studies of marine archaea, the genome sequence indicates N. maritimus grows autotrophically using a variant of the 3-hydroxypropionate/4-hydroxybutryrate pathway for carbon assimilation, while maintaining limited capacity for assimilation of organic carbon. This unique instance of archaeal biosynthesis of the osmoprotectant ectoine and an unprecedented enrichment of multicopper oxidases, thioredoxin-like proteins, and transcriptional regulators points to an organism responsive to environmental cues and adapted to handling reactive copper and nitrogen species that likely derive from its distinctive biochemistry. The conservation of N. maritimus gene content and organization within marine metagenomes indicates that the unique physiology of these specialized oligophiles may play a significant role in the biogeochemical cycles of carbon and nitrogen.

Fig. 1.

Proposed AOA respiratory pathway. Text indicates the described possible hydroxylamine (blue text and arrows) and nitroxyl (green) pathways. Red arrows indicate electron flow not involved in ammonia oxidation. Blue shading denotes blue copper-containing proteins. Pink box indicates possible alternative respiratory electron sink. Hexagons containing Q and QH2 represent the oxidized and reduced quinone pools, respectively.

Fig. 2.

Synteny plots comparing the N. maritimus genome with (A) the Cenarchaeum symbiosum A type genome, (B) crenarchaeal genome fragments, and (C) Sargasso Sea fosmids. Vertical gray bar indicates location of ribosomal RNA operon.

Fig. 3.

Comparison of N. maritimus genome to metagenomic sequence reads from GOS. (A) Percentage of reads from each GOS site that align to the N. maritimus genome by protein sequence similarity. (B) Number of GOS reads homologous to each N. maritimus protein-coding gene. Counts of 40 are mostly due to highly conserved proteins that include contaminants from other clades.