Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea
Edited by David Karl, University of Hawaii, Honolulu, HI, and approved April 2, 2010 (received for review December 6, 2009)
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.
Data Availability
Data deposition: The sequence reported in this paper has been deposited in the NCBI database (accession no. NC_010085).
Acknowledgments
The authors thank David Bruce and Paul Richardson from the Joint Genome Institute for facilitating genome sequencing. This work was supported by the Department of Energy Microbial Genome Program, by National Science Foundation Microbial Interactions and Processes Grant MCB-0604448 (to D.A.S. and J.R.d.l.T.), by National Science Foundation Molecular and Cellular Biosciences Grant MCB-0920741 (to D.A.S.), by National Science Foundation Biological Oceanography Grants OCE-0623174 (to D.A.S.) and OCE-0623908 (to S.M.S.), by National Science Foundation Grant EF-0412129 (to M.G.K.), by incentive funds from the University of Louisville VP Research office (to M.G.K.), by the Deutsche Forschungsgemeinschaft (M.K.), by US Department of Agriculture Grant 2010-65115-20380 (to A.C.R.), and by a Salk Institute Innovation Grant (to G.M.).
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Information & Authors
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Published in
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Data Availability
Data deposition: The sequence reported in this paper has been deposited in the NCBI database (accession no. NC_010085).
Submission history
Published online: April 26, 2010
Published in issue: May 11, 2010
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Acknowledgments
The authors thank David Bruce and Paul Richardson from the Joint Genome Institute for facilitating genome sequencing. This work was supported by the Department of Energy Microbial Genome Program, by National Science Foundation Microbial Interactions and Processes Grant MCB-0604448 (to D.A.S. and J.R.d.l.T.), by National Science Foundation Molecular and Cellular Biosciences Grant MCB-0920741 (to D.A.S.), by National Science Foundation Biological Oceanography Grants OCE-0623174 (to D.A.S.) and OCE-0623908 (to S.M.S.), by National Science Foundation Grant EF-0412129 (to M.G.K.), by incentive funds from the University of Louisville VP Research office (to M.G.K.), by the Deutsche Forschungsgemeinschaft (M.K.), by US Department of Agriculture Grant 2010-65115-20380 (to A.C.R.), and by a Salk Institute Innovation Grant (to G.M.).
Notes
This article is a PNAS Direct Submission.
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The authors declare no conflict of interest.
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Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea, Proc. Natl. Acad. Sci. U.S.A.
107 (19) 8818-8823,
https://doi.org/10.1073/pnas.0913533107
(2010).
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