Patterns of thaumarchaeal gene expression in culture and diverse marine environments

Abstract

Thaumarchaea are ubiquitous in marine habitats where they participate in carbon and nitrogen cycling. Although metatranscriptomes suggest thaumarchaea are active microbes in marine waters, we understand little about how thaumarchaeal gene expression patterns relate to substrate utilization and activity. Here, we report the global transcriptional response of the marine ammonia-oxidizing thaumarchaeon 'Candidatus Nitrosopelagicus brevis' str. CN25 to ammonia limitation using RNA-Seq. We further describe the genome and transcriptome of Ca. N. brevis str. U25, a new strain capable of urea utilization. Ammonia limitation in CN25 resulted in reduced expression of transcripts coding for ammonia oxidation proteins, and increased expression of a gene coding an Hsp20-like chaperone. Despite significantly different transcript abundances across treatments, two ammonia monooxygenase subunits (amoAB), a nitrite reductase (nirK) and both ammonium transporter genes were always among the most abundant transcripts, regardless of growth state. Ca. N. brevis str. U25 cells expressed a urea transporter 139-fold more than the urease catalytic subunit ureC. Gene coexpression networks derived from culture transcriptomes and 10 thaumarchaea-enriched metatranscriptomes revealed a high degree of correlated gene expression across disparate environmental conditions and identified a module of coexpressed genes, including amoABC and nirK, that we hypothesize to represent the core ammonia oxidation machinery.

Characterization of a thaumarchaeal symbiont that drives incomplete nitrification in the tropical spongeIanthella basta

“…C. symbiosum), Ca. N. ianthellae encodes the putative NO-forming nitrite reductase (nirK; found to be highly expressed as protein; Supporting Information - Table S3) that has been suggested to play an important role for archaeal ammonia oxidation (Kozlowski et al, 2016;Carini et al, 2018) a hypothesis that nicely explains the inhibitory effect of the NO scavenger PTIO used in our incubation experiments described below. Interestingly however, the purple cupredoxin Nmar_1307 from Nitrosopumilus maritimus that is capable of oxidizing NO to NO 2 − (Hosseinzadeh et al, 2016) is absent in Ca.…”

Depth distributions of nitrite reductase (nirK) gene variants reveal spatial dynamics of thaumarchaeal ecotype populations in coastal Monterey Bay

“…Another functional gene that has been proposed as an alternative molecular marker for Thaumarchaeota is the copper-containing nitrite reductase gene (nirK) (Bartossek et al, 2010;Lund et al, 2012), which is prominent among the candidate genes proposed to be involved in archaeal ammonia oxidation (Stahl and de la Torre, 2012;Kerou et al, 2016;Kozlowski et al, 2016;Tolar et al, 2017;Carini et al, 2018). Several models have been proposed incorporating NirK into the core ammonia oxidation pathway: in one, NirK catalyses the oxidation of either NH 2 OH to NO, or NO to NO 2 − (Carini et al, 2018).…”

“…Nitrosopelagicus sp. revealed a coherent coexpression module consisting of nirK and amoA/B, along with ammonium transporter proteins (Carini et al, 2018).…”

Archaeal nitrification is constrained by copper complexation with organic matter in municipal wastewater treatment plants

“…Copper is required for ammonia oxidation by both AOA and AOB due to the presence of essential mono-and dinuclear copper centers of the key enzyme AMO [46,47]. In addition, copper is essential for the functioning of the nitrite reductase NirK that is encoded by most AOA and AOB and plays important roles for their physiologies [48,49]. However, the electron transport system of AOB contains some iron (Fe)-dependent metalloenzymes and proteins [the multiheme cytochrome c hydroxylamine oxidoreductase (HAO) and other c-type cytochromes] that are not encoded in known AOA genomes [50].…”

“…However, the electron transport system of AOB contains some iron (Fe)-dependent metalloenzymes and proteins [the multiheme cytochrome c hydroxylamine oxidoreductase (HAO) and other c-type cytochromes] that are not encoded in known AOA genomes [50]. In contrast, AOA are postulated to possess a more copper-based electron-transfer system inferred from (i) the numerous genes encoding copper-containing proteins such as multicopper oxidases and proteins with small Cu-binding plastocyanin-like domains in AOA genomes [25,51,52] and (ii) their detection in AOA proteomes [51,53,54], although the iron-containing electron carrier protein ferredoxin is also encoded and expressed in AOA [48,51,53,54]. Thus, the strong inhibition of AOA by copper-complexing organic compounds is most likely caused by impaired function of copper-containing proteins in AOA which are essential for growth.…”