Anaerobic Haloalkaliphiles

Abstract

Halo‐alkali‐philes is a type of double extremophiles functioning optimally in saline brines of soda lakes. Soda lakes are a specific type of salt lakes with their brines consisting mostly of alkaline sodium carbonates. With rare exceptions, the haloalkaliphiles are prokaryotes, represented by four major metabolic blocks: aerobic and anoxygenic phototrophs as primary producers and aerobic and anaerobic chemotrophs mostly involved in mineral cycling and mineralisation of organic carbon. The fermentative anaerobes in soda lakes mostly include members of Clostridia involved in polymer hydrolysis and further fermentation of the monomers. The halolalkaliphilic denitrifiers are represented mostly by the members of Gammaproteobacteria from the genera Halomonas and Alkalilimnicola/Alkalispirillum group. The sulfidogens is the most active group of secondary anaerobes in soda lakes and include two major groups – sulfate/thiosulfate reducers from the Deltaproteobacteria with a prominent capacity for sulfite and thiosulfate disproportionation and sulfur/polysulfide reducers from the phylum Chrysiogenetes. Furthermore, soda lake natronoarchaea can also participate in polysulfide respiration. Methanogenesis in soda lakes is active with all three classical pathway represented by haloalkaliphilic species, but, similar to salt lakes, it is dominated by methylotrophs. So far, little is known about the specific bioenergetic features of the soda lake anaerobes allowing them to thrive at high pH. One of it, however, seems to be in common – the substantial use of sodium‐pumping, both by primary and secondary cation pumps. Key Concepts Soda lakes is not the only highly alkaline habitat on Earth, but it is the only one where the extremely high pH is stable. Not only the high pH, but also a combination of chemical parameters created by extremely high carbonate alkalinity in brines of the soda lakes makes them a unique habitat dominated by Prokaryotic life. The salinity caused by strongly electrolytic NaCl in pH‐neutral brines differs substantially from the salinity of weakly electrolytic sodium carbonates in its osmotic effect on salt‐tolerant organisms. Extreme salinity and high pH impose extra energy demands on haloalkalphilic microbes, especially anaerobes with low energy‐producing metabolism. Nevertheless, all major functional groups of anaerobic microbes are present in soda lakes. The primary organic matter in soda lakes is mostly produced by protein-rich cyanobacteria. However, the identity of haloalkaliphilic anaerobes degrading proteins in soda lake sediments is still mostly unknown. The denitrifying haloalkaliphilies in soda lakes belong to Gammaproteobacteria but the identity of dissimilatory ammonifyers remains unknown. Many haloalkaliphilic anaerobes isolated from soda lakes are capable of using toxic metal oxyanions as electron acceptors but very few can use Fe(III). The most prominent property of the soda lake sulfidogens is the ability to grow by disproportionation of inorganic sulfur compounds. The methogenesis in soda lakes is dominated by methylotrophic pathways but, in contrast to salt lakes, the other pathways are also active at haloalkaline conditions. Low sulfide toxicity and high CO 2 and H 2 S‐absorbing capacity of the soda brines makes sulfidogenesis and methanogenesis at haloalkaline conditions attractive for application.

Effect of salinity on diazotrophic activity and microbial composition of phototrophic communities from Bitter-1 soda lake (Kulunda Steppe, Russia)

“…On the other hand, an earlier analysis of nifH gene in the samples from Bitter-1 lake collected at a salinity of 300 g/L in 2009 (Tourova et al 2014) detected a presence of extremely salt-tolerant diazotrophic cyanobacteria of the genus Euhalothece and anoxygenic purple sulfur bacteria of the genus Halorhodospira. Although, at such salinity, sulfate-reducing bacteria were predicted to be inhibited due to the thermodynamic constraints of low-energy-generating catabolism (Oren 1999(Oren , 2011b, they were still detectable both by the specific molecular marker (dsrB) in situ (Foti et al 2007(Foti et al , 2008 and also by cultivation approach, in particular the extremely salt-tolerant lithotrophic genera Desulfonatronospira and Desulfonatronovibrio and the acetate-propionate oxidizing genera Desulfonatronobacter and 'Candidatus 1 3 Synthrophonatronum' (Sorokin et al 2015a, b;Sorokin 2017).…”

“…At the salinities higher than 70 g/L, the heterocystous cyanobacteria are not usually detected (Oren 2011a). At these conditions, the diazotrophic bacteria are represented by heterotrophic microaerobes and anaerobes (Sorokin et al 2014a(Sorokin et al , b, 2015aSorokin 2017). A study of the nifH gene diversity in the highly mineralized lakes of the Kulunda steppe and the Wadi Natrun (Egypt) showed the presence of genes belonging to representatives of various phyla, including anoxygenic purple sulfur and nonsulfur proteobacteria, green nonsulfur bacteria, heliobacteria, and oxygenic cyanobacteria, as well as anaerobic heterotrophic bacteria (Tourova et al 2014).…”

Metagenomes and metatranscriptomes shed new light on the microbial-mediated sulfur cycle in a Siberian soda lake

“…Hypersaline soda lakes are evaporative terrestrial lakes with total salt concentrations above 50 g L −1 and a stable high pH roughly around 10 [6, 7]. These unique environmental conditions form a strong selective force and microbes adapted to these double extremes are called “haloalkaliphiles.” Driven by high sulfate concentrations and primary productivity in the brines, the inorganic sulfur cycle is one of the most active cycles occurring in soda lakes [7–11]. At high pH, ƩH 2 S occur mainly in the deprotonated hydrosulfide form (HS − ).…”

Distribution of Denitrification among Haloarchaea: A Comprehensive Study

“…Haloalkaliphilic ecosystems are soda lakes and soda soils characterized by presenting extremely high salinity and pH (up to 11). The biological sulphur cycle is one of the most active in that kind of habitats and it is connected to many other cycles, such as carbon, nitrogen, or metal cycles [ 62 , 63 , 64 , 65 ]. Functional groups of fermenters and sulfidogens are the main anaerobic microorganisms in these ecosystems due to the availability of organic matter and oxidized sulphur species, whereas complete denitrifiers are scarce and denitrification does not have the same important role and abundance as in neutral ecosystems [ 64 , 65 ].…”