Abstract

High representation by ammonia-oxidizing archaea (AOA) in marine systems is consistent with their high affinity for ammonia, efficient carbon fixation, and copper (Cu)-centric respiratory system. However, little is known about their response to nutrient stress. We therefore used global transcriptional and proteomic analyses to characterize the response of a model AOA, Nitrosopumilus maritimus SCM1, to ammonia starvation, Cu limitation and Cu excess. Most predicted protein-coding genes were transcribed in exponentially growing cells, and of ~74% detected in the proteome, ~6% were modified by N-terminal acetylation. The general response to ammonia starvation and Cu stress was downregulation of genes for energy generation and biosynthesis. Cells rapidly depleted transcripts for the A and B subunits of ammonia monooxygenase (AMO) in response to ammonia starvation, yet retained relatively high levels of transcripts for the C subunit. Thus, similar to ammonia-oxidizing bacteria, selective retention of amoC transcripts during starvation appears important for subsequent recovery, and also suggests that AMO subunit transcript ratios could be used to assess the physiological status of marine populations. Unexpectedly, cobalamin biosynthesis was upregulated in response to both ammonia starvation and Cu stress, indicating the importance of this cofactor in retaining functional integrity during times of stress.

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Acknowledgements

This study was supported by National Science Foundation Grants MCB-0604448 and MCB-0920741 (to DAS), Dimensions of Biodiversity Program OCE-1046017 (to DAS, AEI, EVA, AHD and JWM), Swiss National Science Foundation (P2EZP2_155522 to RAL), and NSF GRFP (to KRH). Supplementary Information is available at ISME Journal’s website.

Author information

Affiliations

  1. Department of Civil and Environmental Engineering, University of Washington, Seattle, WA, USA

    • Wei Qin
    •  & David A Stahl
  2. Department of Biology, New York University Abu Dhabi, Abu Dhabi, UAE

    • Shady A Amin
  3. School of Oceanography, University of Washington, Seattle, WA, USA

    • Rachel A Lundeen
    • , Katherine R Heal
    • , Allan H Devol
    • , E Virginia Armbrust
    •  & Anitra E Ingalls
  4. Department of Microbiology and Cell Science & Fort Lauderdale Research and Education Center, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL, USA

    • Willm Martens-Habbena
  5. Institute for Systems Biology, Seattle, WA, USA

    • Serdar Turkarslan
    •  & Nitin S Baliga
  6. Department of Marine and Ecological Sciences, Florida Gulf Coast University, Fort Myers, FL, USA

    • Hidetoshi Urakawa
  7. Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA

    • Kyle C Costa
  8. Department of Chemical Engineering and Center for Microbial Proteomics, University of Washington, Seattle, WA, USA

    • Erik L Hendrickson
    • , Tony Wang
    • , Fred Taub
    •  & Murray Hackett
  9. Department of Chemical Engineering and eScience Institute, University of Washington, Seattle, WA, USA

    • David AC Beck
  10. Department of Natural Sciences, University of Michigan, Dearborn, MI, USA

    • Sonia M Tiquia-Arashiro
  11. Department of Biomolecular Engineering, University of California Santa Cruz, Santa Cruz, CA, USA

    • Andrew D Holmes
    •  & Todd M Lowe
  12. Botany and Plant Pathology, Oregon State University, Corvallis, OR, USA

    • Neeraja Vajrala
    • , Daniel J Arp
    •  & Luis A Sayavedra-Soto
  13. Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA

    • Paul M Berube
  14. Departments of Biological Sciences and Earth Sciences and Civil and Environmental Engineering, University of Southern California, Los Angeles, CA, USA

    • James W Moffett
  15. Department of Microbiology, University of Washington, Seattle, WA, USA

    • Nitin S Baliga

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DOI

https://doi.org/10.1038/ismej.2017.186

Supplementary Information accompanies this paper on The ISME Journal website (http://www.nature.com/ismej)