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 CO2 and H2S‐absorbing capacity of the soda brines makes sulfidogenesis and methanogenesis at haloalkaline conditions attractive for application.

Keywords: soda lakes; haloalkaliphiles; anaerobes; fermenters; sulfidogens; acetogens methanogens

Figure 1. Typical examples of soda habitats in south‐western Siberia (Altai, Russia). (a) Hypersaline soda lake Bitter‐1. (b) Patches of soda solonchak soil with massive formation of mixed sodium carbonate minerals in the surface layer during dry season.
close

References

Baesman SM, Stolz JF, Kulp TR and Oremland RS (2009) Enrichment and isolation of Bacillus beveridgei sp. nov., a facultative anaerobic haloalkaliphile from Mono Lake, California, that respires oxyanions of tellurium, selenium, and arsenic. Extremophiles 13: 695–705.

Bazilevich NI (1970) The Geochemistry of Soda Soils. Jerusalem: USDA, NSF and Israel Program for Scientific Translations396 p.

Brazelton WJ, Morrill PL, Szponar N and Schrenk MO (2013) Bacterial communities associated with subsurface geochemical processes in continental serpentinite springs. Applied Environmental Microbiology 79: 3906–3916.

Daelman MRJ, Sorokin DY, Kruse O, et al. (2016) Haloalkaline bioconversions for methane production from micro‐algae grown on sunlight. Trends in Biotechnology 34: 450–457.

Deocampo DM and Renaut RW (2016) Geochemistry of African soda lakes. In: Schagerl M (ed) Soda Lakes of East Africa, pp. 77–93. Springer International Publishing: Switzerland.

Detkova EN and Pusheva MA (2006) Energy metabolism in halophilic and alkaliphilic acetogenic bacteria. Microbiology (Moscow, English Translation) 75: 1–11.

Eugster HP (1980) Geochemistry of evaporitic lacustrine deposits. Annual Reviews in Earth & Planetary Sciences 8: 35–63.

Ferguson SA, Keis S and Cook GM (2006) Biochemical and molecular characterization of a Na+‐translocating F1F0‐ATPase from the thermoalkaliphilic bacterium Clostridium paradoxum. Journal of Bacteriology 188: 5045–5054.

Finster K (2008) Microbiological disproportionation of inorganic sulfur compounds. Journal of Sulfur Chemistry 29: 281–292.

Grant WD and Jones BE (2016) Bacteria, archaea and viruses of soda lakes. In: Schagerl M (ed) Soda Lakes of East Africa, pp. 97–147. Springer International Publishing: Switzerland.

Kevbrin V, Boltyanskaya Y, Zhilina T, et al. (2013) Proteinivorax tanatarense gen. nov., sp. nov., an anaerobic, haloalkaliphilic, proteolytic bacterium isolated from a decaying algal bloom, and proposal of Proteinivoraceae fam. nov. Extremophiles 17: 747–756.

Klimmek O, Kreis V, Klein C, et al. (1998) The function of the periplasmic Sud protein in polysulfide respiration of Wolinella succinogenes. European Journal of Biochemistry 253: 263–269.

Krienitz L and Schagerl M (2016) Tiny and tough: microphytes of East African soda lakes. In: Schagerl M (ed) Soda Lakes of East Africa, pp. 149–178. Springer International Publishing: Switzerland.

Krulwich TA, Liu J, Morino M, et al. (2011) Adaptive mechanisms of extreme alkaliphiles. In: Horikoshi K (ed) Extremophiles Handbook, pp. 119–140. Tokyo: Springer.

Lloyd JR and Oremland RS (2006) Microbial transformations of arsenic in the environment: from soda lakes to aquifers. Elements 2: 85–90.

Mesbah NM, Hedrick DB, Peacock AD, et al. (2007) Natranaerobius thermophilus gen. nov., sp. nov., a halophilic, alkalithermophilic bacterium from soda lakes of the Wadi An Natrun, Egypt, and proposal of Natranaerobiaceae fam. nov. and Natranaerobiales ord. nov. International Journal of Systematic and Evolutionary Microbiology 57: 2507–2512.

Mesbah NM and Wiegel J (2011) The Na+‐translocating F1F0‐ATPase from the halophilic, alkalithermophile Natranaerobius thermophilus. Biochimica et Biophysica Acta 1807: 1133–1142.

Mesbah NM and Wiegel J (2012) Life under multiple extreme conditions: diversity and physiology of the halophilic alkalithermophiles. Applied and Environmental Microbiology 78: 4074–4082.

Oremland RS, Hoeft SE, Santini JM, et al. (2002) Anaerobic oxidation of arsenite in Mono Lake water and by a facultative, arsenite‐oxidizing chemoautotroph, strain MLHE‐1. Applied and Environmental Microbiology 68: 4795–4802.

Oremland RS, Stolz JF and Hollibaugh JT (2004) The microbial arsenic cycle in Mono Lake, California. FEMS Microbiology Ecology 48: 15–27.

Oren A (2011) Thermodynamic limits to microbial life at high salt concentrations. Environmental Microbiology 13: 1908–1923.

Pfeffer C, Larsen S, Song J, et al. (2012) Filamentous bacteria transport electrons over centimetre distances. Nature 293: 218–221.

Poser A, Vogt C, Knoeller K, et al. (2013) Disproportionation of elemental sulfur by haloalkaliphilic bacteria from soda lakes. Extremophiles 17: 1003–1012.

Preiss L, Hicks DB, Suzuki S, et al. (2015) Alkaliphilic bacteria with impact on industrial applications, concepts of early life forms, and bioenergetics of ATP synthesis. Frontiers in Bioengineering and Biotechnology 3: article 75.

Samylina OS, Sapozhnikov FV, Gainova OY, et al. (2014) Algo‐bacterial phototrophic communities of soda lakes in Kulunda Steppe (Altai, Russia). Microbiology (English Translation) 83: 849–860.

Sorokin DY, Kuenen JG and Jetten M (2001) Denitrification at extremely alkaline conditions in obligately autotrophic alkaliphilic sulfur‐oxidizing bacterium Thioalkalivibrio denitrificans. Archives in Microbiology 175: 94–101.

Sorokin DY, Antipov AN and Kuenen JG (2003) Complete denitrification in a coculture of haloalkaliphilic sulfur‐oxidizing bacteria from a soda lake. Archives in Microbiology 180: 127–133.

Sorokin DY, Foti M, Tindall BJ and Muyzer G (2007) Desulfurispirillum alkaliphilum gen. nov. sp. nov., a novel obligately anaerobic sulfur‐ and dissimilatory nitrate‐reducing bacterium from a full‐scale sulfide‐removing bioreactor. Extremophiles 11: 363–370.

Sorokin DY and Muyzer G (2010) Bacterial dissimilatory MnO2 reduction at extremely haloalkaline conditions. Extremophiles 14: 41–46.

Sorokin DY, Kuenen JG and Muyzer G (2011) The microbial sulfur cycle in soda lakes. Frontiers in Microbial Physiology 2: article 44.

Sorokin DY, Banciu H, Robertson LA, et al. (2013) Halophilic and haloalkaliphilic sulfur‐oxidizing bacteria from hypersaline habitats and soda lakes. In: Rosenberg E, DeLong EF, Stackebrandt E, Lory S and Thompson F (eds) The Prokaryotes – Prokaryotic Physiology and Biochemistry, pp. 529–555. Springer‐Verlag: Berlin‐Heidelberg.

Sorokin DY, Gumerov VM, Rakitin AL, et al. (2014a) Genome analysis of Chitinivibrio alkaliphilus gen. nov., sp. nov., a novel extremely haloalkaliphilic anaerobic chitinolytic bacterium from the candidate phylum TG3. Environmental Microbiology 16: 1549–1565.

Sorokin DY, Berben T, Melton ED, et al. (2014b) Microbial diversity and biogeochemical cycling in soda lakes. Extremophiles 18: 791–809.

Sorokin DY, Abbas B, Tourova TP, et al. (2014c) Sulfate‐dependent acetate oxidation at extremely natron‐alkaline conditions by syntrophic associations from hypersaline soda lakes. Microbiology (SGM) 160: 723–732.

Sorokin DY, Banciu HA and Muyzer G (2015a) Functional microbiology of soda lakes. Current Opinions in Microbiology 25: 88–96.

Sorokin DY, Abbas B, Geleijnse M, et al. (2015b) Methanogenesis at extremely haloalkaline conditions in soda lakes of Kulunda Steppe (Altai, Russia). FEMS Microbiology Ecology 91 (4). DOI: 10.1093/femsec/fiv016.

Sorokin DY, Abbas BA, Sinninghe Damsté JS, et al. (2015c) Methanocalculus alkaliphilus sp. nov., and Methanosalsum natronophilus sp. nov., novel haloalkaliphilic methanogens from hypersaline soda lakes. International Journal of Systematic and Evolutionary Microbiology 65: 3739–3745.

Sorokin DY, Rakitin AL, Gumerov VM, Beletsky AV, et al. (2016a) Phenotypic and genomic properties of Chitinispirillum alkaliphilum gen. nov., sp. nov., a haloalkaliphilic anaerobic chitinolytic bacterium from the candidate phylum TG3. Frontiers in Microbiology 7: article 407.

Sorokin DY, Abbas B, Geleijnse M, et al. (2016b) Syntrophic associations from hypersaline soda lakes converting organic acids and alcohols to methane at extremely haloalkaline conditions. Environmental Microbiology 18: 3189–3202.

Sorokin DY, Makarova KS, Abbas B, et al. (2017) Discovery of extremely halophilic, methyl‐reducing euryarchaea provides insights into the evolutionary origin of methanogenesis. Nature Microbiology 2: article 17081.

Sousa JAB, Sorokin DY and Bijmans MFM (2015) Ecology and application of haloalkaliphilic microbial communities. Applied Microbiology and Biotechnology 99: 9331–9336.

Wiegel J (2011) Anaerobic alkaliphiles and alkaliphilic poly‐extremophiles. In: Horikoshi K (ed) Extremophiles Handbook, pp. 72–97. Springer: Tokyo, Dordrecht, Heidelberg, London, New York.

Wolfe‐Simon F, Switzer Blum J, Kulp TR, et al. (2011) A bacterium that can grow by using arsenic instead of phosphorus. Science 332: 1163–1166.

Zavarzin GA, Zhilina TN and Pikuta EV (1996) Secondary anaerobes in haloalkaliphilic communities in lakes of Tuva. Microbiology (Moscow, English Translation) 65: 546–553.

Zavarzina DG, Kolganova TV, Bulygina ES, et al. (2006) Geoalkalibacter ferrihydriticus gen. nov. sp. nov., the first alkaliphilic representative of the family Geobacteraceae isolated from a soda lake. Microbiology (Moscow, English Translation) 75: 673–682.

Zhilina TN, Zavarzina DG, Kolganova TV, et al. (2005) ‘Candidatus Contubernalis alkalaceticum’, an obligately syntrophic alkaliphilic bacterium capable of anaerobic acetate oxidation in a coculture with Desulfonatronum cooperativum. Microbiology (Moscow, English Translation) 74: 695–703.

Zhilina TN, Zavarzina DG, Kevbrin VV, et al. (2013) Methanocalculus natronophilus sp. nov., a new alkaliphilic hydogenotrophic methanogenic archaeon from soda lake and proposal of the new family Methanocalculaceae. Microbiology (Moscow, English Translation) 82: 698–706.

Zhilina TN, Zavarzina DG, Detkova EN, et al. (2015) Fuchsiella ferrireducens sp. nov., a novel haloalkaliphilic, lithoautotrophic homoacetogen capable of iron reduction, and emendation of the description of the genus Fuchsiella. International Journal of Systematic and Evolutionary Microbiology 65: 2432–2440.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Sorokin, Dimitry Y(Aug 2017) Anaerobic Haloalkaliphiles. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0027654]