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

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.

Patterns of thaumarchaeal gene expression in culture and diverse marine environments

“…Similar to the N. maritimus transcriptome and environmental metatranscriptomes (Hollibaugh et al ., ; Williams et al ., ; Qin et al ., ), ferredoxins were among the most highly expressed genes in N. brevis (Fig. ).…”

“…Nutrient stress has been shown to induce the expression of molecular chaperone proteins in ammonia‐oxidizing archaea, ammonia‐oxidizing bacteria and oligotrophic marine heterotrophs. For example, in N. maritimus , two copies of Hsp20 were differentially expressed during copper stress and recovery, but not during ammonia starvation (Qin et al ., ). Similar to our findings regarding Hsp20, Nitrosomonas europaea expressed peptides for the molecular chaperone GroEL in both energy starved and energy replete conditions, but at significantly greater levels under energy starvation (Pellitteri‐Hahn et al ., ).…”

“…In both models, NirK and two membrane‐anchored cupredoxins (T478_1362 and T478_0895) act in concert to oxidize NH 2 OH to in two steps: a three‐electron oxidation of NH 2 OH to NO, followed by a one‐electron oxidation of NO to (Supporting Information Figure 3). The involvement of T478_0895 orthologs in electron transfer with NirK, is consistent with previous predictions based on gene expression data for N. maritimus (Qin et al ., ). Both proposed pathways are also consistent with the observed coexpression and high abundance of these transcripts across distinct environmental conditions (Figs ) (Hollibaugh et al ., ; Baker et al ., ; Stewart et al ., ; Gifford et al ., ).…”

“…, Supporting Information Table 2). The downregulation of amoA , amoB and nirK in ammonia‐limiting conditions was recently shown for the ammonia‐oxidizing thaumarchaeon Nitrosopumilus maritimus using DNA microarrays (Qin et al ., ), suggesting that one adaptation of ammonia‐oxidizing archaea to ammonia limitation is to reduce the relative expression of energy generation machinery.…”

“…In contrast to the finding that only two genes were more abundant in ammonia-limited stationary phase for Ca. N. brevis, over 200 genes were upregulated in ammonialimited stationary phase for N. maritimus (Qin et al, 2018). One explanation for this observation is that Ca.…”