<i>Nitrosopumilus maritimus</i> genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea

TLDR

Ammonia‑oxidizing archaea are widespread in marine and terrestrial habitats and are important drivers of global carbon and nitrogen cycling. The isolation of strain SCM1 enabled linking its chemolithotrophic physiology to its genome, revealing the genetic basis of its global distribution. The 1.65‑Mb closed genome of SCM1 shows copper‑dependent ammonia oxidation and electron transport systems distinct from bacteria, an autotrophic 3‑hydroxypropionate/4‑hydroxybutyrate carbon‑assimilation pathway, limited organic carbon uptake, ectoine biosynthesis, and an enrichment of multicopper oxidases, thioredoxin‑like proteins, and transcriptional regulators, underscoring its adaptive response to copper and nitrogen species and its potential role in marine carbon and nitrogen cycles.

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.