Distribution of Denitrification among Haloarchaea: A Comprehensive Study

Abstract

Microorganisms from the Halobacteria class, also known as haloarchaea, inhabit a wide range of ecosystems of which the main characteristic is the presence of high salt concentration. These environments together with their microbial communities are not well characterized, but some of the common features that they share are high sun radiation and low availability of oxygen. To overcome these stressful conditions, and more particularly to deal with oxygen limitation, some microorganisms drive alternative respiratory pathways such as denitrification. In this paper, denitrification in haloarchaea has been studied from a phylogenetic point of view. It has been demonstrated that the presence of denitrification enzymes is a quite common characteristic in Halobacteria class, being nitrite reductase and nitric oxide reductase the enzymes with higher co-occurrence, maybe due to their possible role not only in denitrification, but also in detoxification. Moreover, copper-nitrite reductase (NirK) is the only class of respiratory nitrite reductase detected in these microorganisms up to date. The distribution of this alternative respiratory pathway and their enzymes among the families of haloarchaea has also been discussed and related with the environment in which they constitute the major populations. Complete denitrification phenotype is more common in some families like Haloarculaceae and Haloferacaceae, whilst less common in families such as Natrialbaceae and Halorubraceae.

Anaerobic carboxydotrophy in sulfur-respiring haloarchaea from hypersaline lakes

“…S5) and there was no growth with nitrite even at minimal tested concentration of 1 mM. Nevertheless, these are remarkable results, since, to our knowledge, even incomplete nitrate respiration to nitrite with H 2 as the electron donor has never been demonstrated before in haloarchaea [66].…”

Analysis of the external signals driving the transcriptional regulation of the main genes involved in denitrification in Haloferax mediterranei

“…The presence of denitrification genes in haloarchaeal genomes represents an evolutive adaptation to their environments, where oxygen solubility is very low ( Oren, 2016 ; Miralles-Robledillo et al, 2021 ). The next step in this study was to analyze whether low oxygen conditions are necessary for the activation of denitrification.…”

“…Denitrification in haloarchaea is a poorly understood pathway compared to bacterial denitrification. Nevertheless, the last studies have pointed out that denitrification in hypersaline environments could be a source of nitrogenous gasses to the atmosphere (mainly if partial denitrification predominates vs. complete denitrification), and greater efforts should be made to deepen the knowledge of these extreme environments ( Miralles-Robledillo et al, 2021 ). In this context, this work represents an advance in the understanding of the external signals that can modulate the activation of this alternative respiration.…”

“…It has been reported that in hypersaline environments the microbial population which is most prevalent is the haloarchaea, the Haloferacaceae family being the best well-studied ( Oren, 2002 ). Some important representatives of this family are Haloferax, Haloarcula, and Natronomonas genera due to their possible biotechnological applications and their important role in the biogeochemical cycles of these ecosystems ( Bonete et al, 2008 ; Giani et al, 2019 ; Miralles-Robledillo et al, 2021 ). In this context, the Haloferax genus is the best characterized from the biochemical point of view and it has been chosen as a model organism in many studies in order to decipher how N-cycle works in hypersaline environments ( Martínez-Espinosa et al, 2007 ; Torregrosa-Crespo et al, 2016 ).…”

The archaeal class Halobacteria and astrobiology: Knowledge gaps and research opportunities

“…Although members of the Halobacteria were typically seen as aerobic heterotrophs ( Andrei et al, 2012 ) and reliant on the “salt-in” strategy (e.g., Kunte et al, 2002 ), they have consistently proven to be a lot more diverse ( Müller et al, 2005 ; Oren, 2008 ; Gunde-Cimerman et al, 2018 ). An increasing number of species has been reported to use alternative anaerobic metabolic pathways, or even to show preference for anaerobic conditions or phototrophy (e.g., Antunes et al, 2008 ; Sorokin et al, 2017 , 2018 ; Weber et al, 2017 ; Miralles-Robledillo et al, 2021 ).…”