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

C. B. Walker, J. R. De La Torre, M. G. Klotz, H. Urakawa, N. Pinel, D. J. Arp, C. Brochier-Armanet, P. S.G. Chain, P. P. Chan, A. Gollabgir, J. Hemp, M. Hügler, E. A. Karr, M. Könneke, M. Shin, T. J. Lawton, T. Lowe, W. Martens-Habbena, L. A. Sayavedra-Soto, D. LangS. M. Sievert, A. C. Rosenzweig, G. Manning, D. A. Stahl

Research output: Contribution to journalArticle

559 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)8818-8823
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume107
Issue number19
DOIs
StatePublished - May 11 2010

Keywords

  • Ammonia oxidation
  • Archaea
  • Marine microbiology
  • Nitroxyl

ASJC Scopus subject areas

  • General

Fingerprint Dive into the research topics of 'Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea'. Together they form a unique fingerprint.

  • Cite this

    Walker, C. B., De La Torre, J. R., Klotz, M. G., Urakawa, H., Pinel, N., Arp, D. J., Brochier-Armanet, C., Chain, P. S. G., Chan, P. P., Gollabgir, A., Hemp, J., Hügler, M., Karr, E. A., Könneke, M., Shin, M., Lawton, T. J., Lowe, T., Martens-Habbena, W., Sayavedra-Soto, L. A., ... Stahl, D. A. (2010). Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proceedings of the National Academy of Sciences of the United States of America, 107(19), 8818-8823. https://doi.org/10.1073/pnas.0913533107