Stress response of a marine ammonia-oxidizing archaeon informs physiological status of environmental populations

Wei Qin, Shady A. Amin, Rachel A. Lundeen, Katherine R. Heal, Willm Martens-Habbena, Serdar Turkarslan, Hidetoshi Urakawa, Kyle C. Costa, Erik L. Hendrickson, Tony Wang, David Ac Beck, Sonia M. Tiquia-Arashiro, Fred Taub, Andrew D. Holmes, Neeraja Vajrala, Paul M. Berube, Todd M. Lowe, James W. Moffett, Allan H. Devol, Nitin S. BaligaDaniel J. Arp, Luis A. Sayavedra-Soto, Murray Hackett, E. Virginia Armbrust, Anitra E. Ingalls, David A. Stahl

Research output: Contribution to journalArticlepeer-review

30 Scopus citations


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.

Original languageEnglish (US)
Pages (from-to)508-519
Number of pages12
JournalISME Journal
Issue number2
StatePublished - Feb 1 2018
Externally publishedYes

Bibliographical note

Funding Information:
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.

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