Haloarchaea are prokaryotic microorganisms belonging to the Archaea domain that require salt concentrations to be alive (Oren 2008). Although initially they were described as moderate or extremophilic halophiles inhabiting extreme ecosystems, the studies carried out up to date reveal that they are more abundant and widely spread than initially thought. Most of the haloarchaeal species are grouped into two families (Halobacteriaceae and Haloferacaceae) and constitute the major microbial populations in salty environments (total salt concentrations above 20–25% w/v) (Gupta et al. 2015; Valentine 2007). These microorganisms inhabit ecosystems such as submarine brine pools, brine pockets within sea ice, natural salty lakes and lagoons, and salt marshes created by human beings. These environments are typically highly alkaline and can serve as sources of sodium chloride for human consumption (Oren 2008). In these ecosystems, haloarchaea constitute the major microbial populations.

From a metabolic point of view, several species can grow under microaerobic or anaerobic conditions. Regarding anaerobic metabolism, compounds such as oxychloride, acetate, and sulphur or nitrogenous compounds like nitrate or nitrate can be used as final electron acceptors instead of oxygen (Sorokin et al. 2016; Miralles-Robledillo et al. 2021). Several of the compounds mentioned can be toxic to living organisms depending on their concentration and specific chemical properties. However, microorganisms play a crucial role in environmental detoxification through their respiratory processes under microaerobic or anaerobic conditions, facilitating the removal of these compounds from soil or saline water. Thus, several species have been revealed as good candidates for biotechnological applications by both, using whole cells or their metabolites (Oren 2010; Martínez et al. 2022).

Currently, there is an increasing interest in the optimisation of bioremediation approaches in high-salt environments, which are mostly influenced by the discharge of industrial effluents. This interest is also increasing in the following:

Countries in which pollution is increasing in combination with the extension of arid and semiarid regions because of climate change (North Africa, India, Middle East, etc.) (see references displayed in Table 1).

Wastewater treatment-based companies looking for methods and strategies to recycle brines obtained after chemical and biological treatments (Oren 2010)

Table 1 Metabolic capabilities of haloarchaea of interest for the design of bioremediation approaches to remove pollutants

Thus, the increase of salinity and pollutants in soils and ground waters during the last years has indirectly reinforced attention in the search for microbial physiological and molecular mechanisms involved in salt-stress tolerance concomitantly with pollutant degradation, assimilation, and/or removal. However, the most used microbiological processes in biotechnology are not capable of being executed at high salt concentrations, indicating that microbial bioremediation of hypersaline-produced water requires halophiles or extreme halophiles (Oren 2010; Li et al. 2022).

In this context, haloarchaea have been successfully tested for biotechnological applications throughout the last decade (Martínez et al. 2022; Singh and Singh 2017). Among these applications, the following can be highlighted:

i)

Synthesis of pigments showing high antioxidant activity. Although some haloarchaea can synthesise different types of carotenoids, the major pigment produced by the cells is the rare carotenoids called bacterioruberin (C50-type carotenoid) (Martínez et al. 2022).

ii)

Synthesis of biopolymers of plastic nature. Several species have been described as efficient polyhydroxyalkanoate producers (PHAs), including the capability of producing PHBV-type biopolymer, which is one of the most marketed bioplastics due to its physicochemical properties (Oren 2010; Martínez et al. 2022).

iii)

Synthesis of enzymes of interesting catalytic properties able to be stable and active at high temperatures. Most of these enzymes are resistant to denaturing agents such as detergents, organic solvents, and stable at extreme pH values (Oren 2008, 2010; Singh and Singh 2017; Martínez et al. 2022). Moreover, their proteins are rich in acidic amino acids, which allows the maintenance of stable conformation and activity at high salt concentrations (Oren 2008).

Biochemical pathways related to most of the main biogeochemical cycles (like the iron, sulphur, or nitrogen cycles), heavy metals, aromatic compounds, or hydrocarbons have been described in archaea as potentially useful for biotechnological applications due to their catalytic efficiency. Based on databases, around 900 publications have been reported since 1978 demonstrating applications of various species of archaea in bioremediation (in all its variants) of water, soils, or sludge (Fig. 1). These studies cover from a variety of points of view (biochemistry, genetics, omics sciences, molecular engineering, system biology, etc.), all the benefits and disadvantages that the use of archaeal species in bioremediation would have, both on a small and large scale, as well as in situ and ex situ approaches (https://pubmed.ncbi.nlm.nih.gov/?term=archaea%20and%20bioremediation&sort=date&page=3). Only around 30 of them involved haloarchaeal species as model organisms for bioremediation proposals in saline and hypersaline wastewater treatments, thanks to their high tolerance to salt, metals, and organic pollutants (Oren 2010; Singh and Singh 2017; Martínez et al. 2022). These investigations focused on haloarchaea have been mainly conducted in the last decade as displayed in Fig. 1; therefore, this field of study can be considered innovative and promising.

Fig. 1

Number of publications identified through PubMed focused on the use of archaea (archaea AND bioremediation: orange colour) and haloarchaea (haloarchaea AND bioremediation: blue colour) as model organisms in bioremediation approaches (source PubMed, accessed on 17 May 2024). In the case of archaea, only data from the years that coincide with publications of studies with haloarchaea have been presented

The bibliometric analysis of the references identified as explained in Fig. 1 remarks the abundance of publications in countries like the USA followed by China, India, Kuwait, and Spain. Considering that the USA, China, India, and the European Union are among the most polluted areas in the world and that several areas of India, Spain, and the Middle Eastern countries are mainly characterised by hypersaline environments, it can be concluded that this recent research area is mainly supported by research groups directly facing the problems related to environment pollution and the expansion of extremophilic environments due to climate change in the geographical context where they are developing the work. So far, mesophilic microorganisms have successfully been used for wastewater treatment, and many of these processes produce brines that cannot be further treated biologically by mesophilic microbes due to their low tolerance to salt. Thus, haloarchaea are revealed as powerful tools to complete wastewater treatments including the management of the final brine produced. Table 1 summarises the main applications described up to date regarding the metabolic capabilities of haloarchaea that could be of interest in the bioremediation of salty soils and water.

Among all the haloarchaeal species tested for bioremediation, species belonging to the Haloferax genus, particularly Haloferax mediterranei, are probably the best characterised and revealed as good models for viable bioremediation applications. H. mediterranei is a haloarchaeon from the family Haloferacaceae (Gupta et al. 2015), firstly isolated from brines taken from seawater evaporation ponds located in the municipality of Santa Pola (near Alicante, Spain) (Rodríguez-Valera et al. 1980). This haloarchaeon can grow aerobically, microaerobically, and anaerobically in a broad range of NaCl concentrations ranging from 1.0 to 5.2 M (Gupta et al. 2015; Martínez et al. 2022; Rodríguez-Valera et al. 1980; Torregrosa-Crespo et al. 2019), thanks to its efficient metabolism and genome stability at moderate and high salt concentrations (Capes et al. 2011).

As can be concluded from the works listed in Table 1, H. mediterranei can remove most of the nitrogen compounds present in brines and soil (including nitrate, nitrite, and ammonium), specifically under anoxic conditions after the induction of the denitrification pathway (H. mediterranei shows a complete denitrifier phenotype) (Torregrosa-Crespo et al. 2019; Bernabeu et al. 2021). This is particularly interesting in the case of nitrate and nitrite which are highly toxic oxyanions for most living beings (nitrite for instance causes gastric cancer in human beings). Besides, this species can use nitrate and nitrite not only through denitrification but also as sole nitrogen for growth, thanks to the pathway termed assimilatory nitrate reduction. Considering both pathways, H. mediterranei can remove up to 2 M of nitrate and up to 50 mM of nitrite apart from ammonium from brines (Torregrosa-Crespo et al. 2019; Bernabeu et al. 2021; Miralles-Robledillo et al. 2021). In principle, the concentrations of nitrogenous compounds in natural brines of saltern ponds and marshes are relatively low or even insignificant. However, their proximity to vast extensions of lands used for agriculture, where there is excessive use of fertilisers, is leading to the appearance of concentrations of nitrate, nitrite, and ammonium above the thresholds established by current legislation in Europe.

Apart from the removal of nitrate and nitrite from water and brines, thanks to denitrifying haloarchaea like H. mediterranei, the enzyme termed “respiratory nitrate reductase” (catalysing the first reaction in the denitrification pathway) can efficiently reduce bromate and (per)chlorate, thanks to the use of these compounds as terminal electron acceptors under anoxic conditions (Martínez-Espinosa et al. 2015). (Per)chlorates are a by-product of chlorine-based products that can be found as a disinfectant in the food processing industry, in processes aiming for the purification of drinking water; as part of herbicides, and pesticide formulas; or as a component of fireworks among other uses (Martínez-Espinosa et al. 2015). In a 2015 study, the European Food Safety Authority (EFSA) found that the current level of chlorate that people get through food and drinking water is too high, and connections between (per)chlorate ingestion and health concerns for at-risk groups were connected at that time (Martínez-Espinosa et al. 2015; https://www.efsa.europa.eu/en/efsajournal/pub/4135). For this reason, it is important to decrease the use of oxychlorides and remove them from the environment. Here, haloarchaea are powerful biological tools because of their high capability to transform them into fewer toxic compounds (Martínez-Espinosa et al. 2015).

Other works recently demonstrated that H. mediterranei as well as other members of the haloarchaeal group have the necessary molecular machinery to grow in the presence of pollutants like crude oil, heavy metals, phenols, and hydrocarbons, thus resulting in the assimilation, modification, degradation, and even complete removal of those toxic compounds (Table 1). Regarding the removal of crude oil or phenols by haloarchaea, simple practises like in vitro haloarchaeal growth in culture media containing crude oil and supplemented with extra nitrogen sources or other essential ions like magnesium and potassium allowed the efficient removal of those toxic compounds. Besides, the incubation of the cells under continuous illumination lost double as much more oil than samples incubated in the dark. Other optimizations like the addition of vitamins to promote hydrocarbon removal by haloarchaea have been tested finding that the oil and pure hydrocarbon consumption potential of all haloarchaeal species monitored was enhanced by vitamin additions. The most effective vitamins were thiamin, pyridoxine, and vitamin B12 (Bonfá et al. 2011; Al-Mailem et al. 2012, 2017; Zhao et al. 2017).

It has also been described the capability of several haloarchaea to produce nanoparticles in the presence of metals. For example, Haloferax alexandrinus RK_AK2, Haloferax lucentense RK_MY6, Halococcus salifodinae BK3, and Halococcus salifodinae BK18 can make silver nanoparticles (Srivastava et al. 2013, 2014, 2015; Moopantakath et al. 2022; Buda et al. 2023). The production of gold particles as well as particles from metalloids like selenium has also been described from the Haloferax genus [60, 61]. Nanoparticles have been described as small particles showing sizes ranging between 1 and 100 nm (consequently, they are undetectable by the human eye). Nanoparticles can exhibit significantly different physical and chemical properties to their larger material counterparts, and currently, they are used in several industrial processes (manufacture of transparent sunscreens, scratchproof eyeglasses, crack-resistant paints, anti-graffiti coatings for walls, stain-repellent fabrics, self-cleaning windows, and ceramic coatings for solar cells, etc.) or biological/biomedicine approaches (as fluorescent biological labels, for drug and gene delivery, detection of pathogens (viruses or bacteria) and biomolecules of interest like proteins, tissue engineering, etc.). Considering the potential uses of nanoparticles and the current interest in them in biomedicine and pharmaceutics, haloarchaeal species could be successfully used as cell factories to naturally produce nanoparticles concomitantly with the removal of heavy metals (Martínez et al. 2022; Moopantakath et al. 2022; Joseph et al. 2023). Consequently, the capability of some haloarchaea to make nanoparticles in culture media containing metals makes it possible to design circular economy-based processes in which pollutants like metals and metalloids can be removed from salty soils, brines, and wastewaters by producing nanoparticles highly marketed.