Analysis of multiple haloarchaeal genomes suggests that the quinone‐dependent respiratory nitric oxide reductase is an important source of nitrous oxide in hypersaline environments

Abstract

Microorganisms, including Bacteria and Archaea, play a key role in denitrification, which is the major mechanism by which fixed nitrogen returns to the atmosphere from soil and water. While the enzymology of denitrification is well understood in Bacteria, the details of the last two reactions in this pathway, which catalyse the reduction of nitric oxide (NO) via nitrous oxide (N O) to nitrogen (N ), are little studied in Archaea, and hardly at all in haloarchaea. This work describes an extensive interspecies analysis of both complete and draft haloarchaeal genomes aimed at identifying the genes that encode respiratory nitric oxide reductases (Nors). The study revealed that the only nor gene found in haloarchaea is one that encodes a single subunit quinone dependent Nor homologous to the qNor found in bacteria. This surprising discovery is considered in terms of our emerging understanding of haloarchaeal bioenergetics and NO management.

Deciphering Pathways for Carotenogenesis in Haloarchaea

“…One of these two genes, which is located outside the three-gene cluster, can be identified as a FAD-dependent oxidoreductase but is also annotated as an identical protein of phytoene desaturase. This conflict of annotation and the problems related to the incomplete or not completely accurate genome assembling have been previously described in other haloarchaeal studies [70]. Consequently, one of the main conclusions from this study is that more effort must be made in the next future to assembly haloarchaeal draft genomes and to review and update gene annotations in completely sequenced haloarchaeal genomes.…”

“…The considerable diversity in the organization of genes around those ORFs coding for carotenoid protein, prenyltransferase, phytoene desaturase, and phytoene synthase, and the existence of more than one copy for these genes in some of the analyzed species could be accounted for by the recent acquisition of those genes through horizontal gene transfer and subsequent recombination events, as it has also been reported for other genes like those related to denitrification in haloarchaea [70]. In order to get a complete view of the evolutionary relationship of carotenogenesis in selected haloarchaeal species, a phylogenetic tree for each of the three genes included in the cluster has been elaborated and analyzed (Figure 4).…”

Haloferax mediterranei, an Archaeal Model for Denitrification in Saline Systems, Characterized Through Integrated Physiological and Transcriptional Analyses

“…Among them are several denitrifiers and the microorganism that has emerged as a representative model is Haloferax mediterranei. It has the full set of metalloenzymes to catalyze the reduction of NO 3 − to N 2 : the membrane-bound nitrate reductase facing the pseudo periplasm (NAR) (Lledó et al, 2004;Martínez-Espinosa et al, 2007), the copper-containing nitrite reductase (NIR) (Martínez-Espinosa et al, 2006), the nitric oxide reductase (NOR) (Torregrosa-Crespo et al, 2017), and the nitrous oxide reductase (N 2 OR) (Torregrosa-Crespo et al, 2016). Currently, it is one out of very few archaea for which detailed phenotypic data exist, and it is the only one which has been shown to be a complete denitrifier, able to reduce NO 3 − to N 2 while displaying low and transient accumulation of the gaseous intermediates NO and N 2 O (Torregrosa-Crespo et al, 2019).…”

Denitrifying haloarchaea within the genus Haloferax display divergent respiratory phenotypes, with implications for their release of nitrogenous gases

“…The native nitrite reductase, purified in H. denitrificans, is a copper-containing enzyme resembling the bacterial NirK (Inatomi and Hochstein, 1996). Neither of the remaining two reductases have been purified in haloarchaea, but the latest advances indicate that the nitric oxide reductase in this group of microorganisms is the qNOR type (Torregrosa-Crespo et al, 2017).…”