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

Abstract

Summary Haloarchaea are extremophiles, generally thriving at high temperatures and salt concentrations, thus, with limited access to oxygen. As a strategy to maintain a respiratory metabolism, many halophilic archaea are capable of denitrification. Among them are members of the genus Haloferax, which are abundant in saline/hypersaline environments. Three reported haloarchaeal denitrifiers, Haloferax mediterranei, Haloferax denitrificans and Haloferax volcanii, were characterized with respect to their denitrification phenotype. A semi‐automatic incubation system was used to monitor the depletion of electron acceptors and accumulation of gaseous intermediates in batch cultures under a range of conditions. Out of the species tested, only H. mediterranei was able to consistently reduce all available N‐oxyanions to N2, while the other two released significant amounts of NO and N2O, which affect tropospheric and stratospheric chemistries respectively. The prevalence and magnitude of hypersaline ecosystems are on the rise due to climate change and anthropogenic activity. Thus, the biology of halophilic denitrifiers is inherently interesting, due to their contribution to the global nitrogen cycle, and potential application in bioremediation. This work is the first detailed physiological study of denitrification in haloarchaea, and as such a seed for our understanding of the drivers of nitrogen turnover in hypersaline systems.

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

“…The observed gas kinetics were as expected for H. mediterranei under the relevant conditions (Torregrosa-Crespo et al, 2019). The cultures reduced all available nitrate to N 2 with minimal and transient accumulation of intermediates.…”

“…During the last decade, denitrification in haloarchaea has gained new attention (Nájera-Fernández et al, 2012;Oren and Hallsworth, 2014;Torregrosa-Crespo et al, 2016). Recently, H. mediterranei was identified as a promising candidate model organism for haloarchaeal denitrification (Torregrosa-Crespo et al, 2019) and the present study elaborates on its respiratory physiology.…”

“…Hypersaline environments accommodate representatives of all the three Domains of Life, but when the salt concentration exceeds 16%, haloarchaea dominate (Andrei et al, 2012;Edbeib et al, 2016;Torregrosa-Crespo et al, 2019). 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). This opens the door to further exploration of its respiratory physiology and regulation of denitrification.…”

Nitrate Respiration in Thermus Thermophilus NAR1: From Horizontal Gene Transfer to Internal Evolution

“…about this process in Gram-positives (Firmicutes) [15], and in few extremophiles, both archaea [16] and bacteria [17]. Among these last ones, denitrification genes and actual functionality have been described for phylogenetically diverse species, many of which are thermophiles [18].…”