Soda lakes are salt lakes with a naturally alkaline pH due to evaporative concentration of sodium carbonates in the absence of major divalent cations. Hypersaline soda brines harbor microbial communities with a high species- and strain-level archaeal diversity and a large proportion of still uncultured poly-extremophiles compared to neutral brines of similar salinities. We present the first "metagenomic snapshots" of microbial communities thriving in the brines of four shallow soda lakes from the Kulunda Steppe (Altai, Russia) covering a salinity range from 170 to 400 g/L. Both amplicon sequencing of 16S rRNA fragments and direct metagenomic sequencing showed that the top-level taxa abundance was linked to the ambient salinity: Bacteroidetes, Alpha-, and Gamma-proteobacteria were dominant below a salinity of 250 g/L, Euryarchaeota at higher salinities. Within these taxa, amplicon sequences related to Halorubrum, Natrinema, Gracilimonas, purple non-sulfur bacteria (Rhizobiales, Rhodobacter, and Rhodobaca) and chemolithotrophic sulfur oxidizers (Thioalkalivibrio) were highly abundant. Twenty-four draft population genomes from novel members and ecotypes within the Nanohaloarchaea, Halobacteria, and Bacteroidetes were reconstructed to explore their metabolic features, environmental abundance and strategies for osmotic adaptation. The Halobacteria- and Bacteroidetes-related draft genomes belong to putative aerobic heterotrophs, likely with the capacity to ferment sugars in the absence of oxygen. Members from both taxonomic groups are likely involved in primary organic carbon degradation, since some of the reconstructed genomes encode the ability to hydrolyze recalcitrant substrates, such as cellulose and chitin. Putative sodium-pumping rhodopsins were found in both a Flavobacteriaceae- and a Chitinophagaceae-related draft genome. The predicted proteomes of both the latter and a Rhodothermaceae-related draft genome were indicative of a "salt-in" strategy of osmotic adaptation. The primary catabolic and respiratory pathways shared among all available reference genomes of Nanohaloarchaea and our novel genome reconstructions remain incomplete, but point to a primarily fermentative lifestyle. Encoded xenorhodopsins found in most drafts suggest that light plays an important role in the ecology of Nanohaloarchaea. Putative encoded halolysins and laccase-like oxidases might indicate the potential for extracellular degradation of proteins and peptides, and phenolic or aromatic compounds.

Australian Centre for Ecogenomics School of Chemistry and Molecular Biosciences and Institute for Molecular Bioscience The University of Queensland Brisbane QLD Australia

Evolutionary Genomics Group Departamento de Producción Vegetal y Microbiología Universidad Miguel Hernández San Juan de Alicante Spain

Evolutionary Genomics Group Departamento de Producción Vegetal y Microbiología Universidad Miguel HernándezSan Juan de Alicante Spain; Department of Aquatic Microbial Ecology Biology Centre of the Czech Academy of Sciences Institute of HydrobiologyČeské Budějovice Czech Republic

Microbial Systems Ecology Department of Aquatic Microbiology Institute for Biodiversity and Ecosystem Dynamics University of Amsterdam Amsterdam Netherlands

Research Centre of Biotechnology Winogradsky Institute of Microbiology Russian Academy of SciencesMoscow Russia; Department of Biotechnology Delft University of TechnologyDelft Netherlands

The Department of Energy Joint Genome Institute Walnut Creek CA USA

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Albertsen M., Hugenholtz P., Skarshewski A., Nielsen K. L., Tyson G. W., Nielsen P. H. (2013). Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat. Biotechnol. 31, 533–538. 10.1038/nbt.2579 PubMed DOI

Alneberg J., Bjarnason B. S., de Bruijn I., Schirmer M., Quick J., Ijaz U. Z., et al. . (2014). Binning metagenomic contigs by coverage and composition. Nat. Methods 11, 1144–1146. 10.1038/nmeth.3103 PubMed DOI

Andrade K., Logemann J., Heidelberg K. B., Emerson J. B., Comolli L. R., Hug L. A., et al. . (2015). Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem. ISME J. 9, 2697–2711. 10.1038/ismej.2015.66 PubMed DOI PMC

Antón J., Oren A., Benlloch S., Rodríguez-Valera F., Amann R., Rosselló-Mora R. (2002). Salinibacter ruber gen. nov., sp. nov., a novel, extremely halophilic member of the bacteria from saltern crystallizer ponds. Int. J. Syst. Evol. Microbiol. 52, 485–491. 10.1099/00207713-52-2-485 PubMed DOI

Antón J., Rosselló-Mora R., Rodríguez-Valera F., Amann R. (2000). Extremely halophilic bacteria in crystallizer ponds from solar salterns. Appl. Environ. Microbiol. 66, 3052–3057. 10.1128/AEM.66.7.3052-3057.2000 PubMed DOI PMC

Asao M., Pinkart H. C., Madigan M. T. (2011). Diversity of extremophilic purple phototrophic bacteria in soap lake, a central washington (USA) soda lake. Environ. Microbiol. 13, 2146–2157. 10.1111/j.1462-2920.2011.02449.x PubMed DOI

Ausec L., Zakrzewski M., Goesmann A., Schlüter A., Mandic-Mulec I. (2011). Bioinformatic analysis reveals high diversity of bacterial genes for laccase-like enzymes. PLoS ONE 6:e25724. 10.1371/journal.pone.0025724 PubMed DOI PMC

Banciu H. L., Sorokin D. Y. (2013). Adaptation in Haloalkaliphiles and Natronophilic bacteria, in Polyextremophiles, eds Seckbach J., Oren A., Stan-Lotter H. (Dordrecht: Springer; ), 121–178.

Bateman A., Coin L., Durbin R., Finn R. D., Hollich V., Griffiths-Jones S., et al. . (2004). The Pfam protein families database. Nucleic Acids Res. 32(Suppl. 1), D138–D141. 10.1093/nar/gkh121 PubMed DOI PMC

Bauer M., Kube M., Teeling H., Richter M., Lombardot T., Allers E., et al. (2006). Whole genome analysis of the marine Bacteroidetes ‘Gramella forsetii’ reveals adaptations to degradation of polymeric organic matter. Environ. Microbiol. 8, 2201–2213. 10.1111/j.1462-2920.2006.01152.x PubMed DOI

Béja O., Spudich E. N., Spudich J. L., Leclerc M., DeLong E. F. (2001). Proteorhodopsin phototrophy in the ocean. Nature 411, 786–789. 10.1038/35081051 PubMed DOI

Benlloch S., López-López A., Casamayor E. O., Øvreås L., Goddard V., Daae F. L., et al. . (2002). Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environ. Microbiol. 4, 349–360. 10.1046/j.1462-2920.2002.00306.x PubMed DOI

Boldareva E. N., Akimov V. N., Boychenko V. A., Stadnichuk I. N., Moskalenko A. A., Makhneva Z. K., et al. . (2008). Rhodobaca barguzinensis sp. nov., a new alkaliphilic purple nonsulfur bacterium isolated from a soda lake of the Barguzin Valley (Buryat Republic, Eastern Siberia). Microbiology 77, 206–218. 10.1134/S0026261708020148 PubMed DOI

Boldareva E. N., Bryantseva I. A., Tsapin A., Nelson K., Sorokin D. Y., Tourova T. P., et al. (2007). The new alkaliphilic bacteriochlorophyll a-containing bacterium Roseinatronobacter monicus sp. nov. from the hypersaline Soda Mono Lake (California, United States). Microbiology 76, 82–92. 10.1134/S0026261707010122 PubMed DOI

Bowman J. P., McCammon S. A., Lewis T., Skerratt J. H., Brown J. L., Nichols D. S., et al. . (1998). Psychroflexus torquis gen. nov., sp. nov. a psychrophilic species from Antarctic sea ice, and reclassification of Flavobacterium gondwanense (Dobson et al., 1993) as Psychroflexus gondwanense gen. nov., comb. nov. Microbiology 144, 1601–1609. 10.1099/00221287-144-6-1601 PubMed DOI

Cabello P., Roldán M. D., Moreno-Vivián C. (2004). Nitrate reduction and the nitrogen cycle in Archaea. Microbiology 150, 3527–3546. 10.1099/mic.0.27303-0 PubMed DOI

Casamayor E. O., Calderón-Paz J. I., Pedrós-Alió C. (2000). 5S rRNA fingerprints of marine Bacteria, halophilic Archaea and natural prokaryotic assemblages along a salinity gradient. FEMS Microbiol. Ecol. 34, 113–119. 10.1111/j.1574-6941.2000.tb00760.x PubMed DOI

Casamayor E. O., Massana R., Benlloch S., Øvreås L., Díez B., Goddard V. J., et al. . (2002). Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar saltern. Environ. Microbiol. 4, 338–348. 10.1046/j.1462-2920.2002.00297.x PubMed DOI

Castelle C. J., Wrighton K. C., Thomas B. C., Hug L. A., Brown C. T., Wilkins M. J., et al. . (2015). Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr. Biol. 25, 690–701. 10.1016/j.cub.2015.01.014 PubMed DOI

Cho Y., Chung H., Jang G. I., Choi D. H., Noh J. H., Cho B. C. (2013). Gracilimonas rosea sp. nov., isolated from tropical seawater, and emended description of the genus Gracilimonas. Int. J. Syst. Evol. Microbiol. 63, 4006–4011. 10.1099/ijs.0.052340-0 PubMed DOI

Choi D. H., Zhang G. I., Noh J. H., Kim W. S., Cho B. C. (2009). Gracilimonas tropica gen. nov., sp. nov., isolated from a Synechococcus culture. Int. J. Syst. Evol. Microbiol. 59, 1167–1172. 10.1099/ijs.0.005512-0 PubMed DOI

Cole J. R., Wang Q., Fish J. A., Chai B., McGarrell D. M., Sun Y., et al. . (2014). Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 41(Database issue):gkt1244. 10.1093/nar/gkt1244 PubMed DOI PMC

Cox M. P., Peterson D. A., Biggs P. J. (2010). SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinformatics 11:485. 10.1186/1471-2105-11-485 PubMed DOI PMC

Cunliffe M. (2011). Correlating carbon monoxide oxidation with cox genes in the abundant marine Roseobacter clade. ISME J. 5, 685–691. 10.1038/ismej.2010.170 PubMed DOI PMC

De Castro R. E., Maupin-Furlow J. A., Giménez M. I., Seitz M. K. H., Sánchez J. J. (2006). Haloarchaeal proteases and proteolytic systems. FEMS Microbiol. Rev. 30, 17–35. 10.1111/j.1574-6976.2005.00003.x PubMed DOI

Dillon J. G., Carlin M., Gutierrez A., Nguyen V., McLain N. (2013). Patterns of microbial diversity along a salinity gradient in the Guerrero Negro solar saltern, Baja CA Sur, Mexico. Front. Microbiol. 4:399. 10.3389/fmicb.2013.00399 PubMed DOI PMC

Dimitriu P. A., Pinkart H. C., Peyton B. M., Mormile M. R. (2008). Spatial and temporal patterns in the microbial diversity of a meromictic soda lake in washington state. Appl. Environ. Microbiol. 74, 4877–4888. 10.1128/AEM.00455-08 PubMed DOI PMC

Dobbek H., Svetlitchnyi V., Gremer L., Huber R., Meyer O. (2001). Crystal structure of a carbon monoxide dehydrogenase reveals a [Ni-4Fe-5S] cluster. Science 293, 1281–128510. 10.1126/science.1061500 PubMed DOI

Donachie S. P., Bowman J. P., Alam M. (2004). Psychroflexus tropicus sp. nov., an obligately halophilic Cytophaga–Flavobacterium–Bacteroides group bacterium from an Hawaiian hypersaline lake. Int. J. Syst. Evol. Microbiol. 54, 935–940. 10.1099/ijs.0.02733-0 PubMed DOI

Fernández A. B., Ghai R., Martin-Cuadrado A., Sánchez-Porro C., Rodriguez-Valera F., Ventosa A. (2014a). Prokaryotic taxonomic and metabolic diversity of an intermediate salinity hypersaline habitat assessed by metagenomics. FEMS Microbiol. Ecol. 88, 623–635. 10.1111/1574-6941.12329 PubMed DOI

Fernández A. B., Vera-Gargallo B., Sánchez-Porro C., Ghai R., Papke R. T., Rodriguez-Valera F., et al. . (2014b). Comparison of prokaryotic community structure from Mediterranean and Atlantic saltern concentrator ponds by a metagenomic approach. Front. Microbiol. 5:196. 10.3389/fmicb.2014.00196 PubMed DOI PMC

Foti M. J., Sorokin D. Y., Zacharova E. E., Pimenov N. V., Kuenen J. G., Muyzer G. (2008). Bacterial diversity and activity along a salinity gradient in soda lakes of the Kulunda Steppe (Altai, Russia). Extremophiles 12, 133–145. 10.1007/s00792-007-0117-7 PubMed DOI

Gareeb A. P., Setati M. E. (2009). Assessment of alkaliphilic haloarchaeal diversity in Sua pan evaporator ponds in Botswana. Afr. J. Biotechnol. 8, 259–267. 10.5897/AJB2009.000-9046 DOI

Ghai R., Pašić L., Fernández A. B., Martin-Cuadrado A., Mizuno C. M., McMahon K. D., et al. . (2011). New abundant microbial groups in aquatic hypersaline environments. Sci. Rep. 1:135. 10.1038/srep00135 PubMed DOI PMC

Gnida M., Ferner R., Gremer L., Meyer O., Meyer-Klaucke W. (2003). A novel binuclear [CuSMo] cluster at the active site of carbon monoxide dehydrogenase: characterization by X-ray absorption spectroscopy. Biochemistry 42, 222–230. 10.1021/bi026514n PubMed DOI

Goris J., Konstantinidis K. T., Klappenbach J. A., Coenye T., Vandamme P., Tiedje J. M. (2007). DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int. J. Syst. Evol. Microbiol. 57, 81–91. 10.1099/ijs.0.64483-0 PubMed DOI

Grant S., Grant W. D., Jones B. E., Kato C., Li L. (1999). Novel archaeal phylotypes from an East African alkaline saltern. Extremophiles 3, 139–145. 10.1007/s007920050109 PubMed DOI

Grant W. D. (2004). Life at low water activity. Philos. Trans. R. Soc. B Biol. Sci. 359, 1249–1267. 10.1098/rstb.2004.1502 PubMed DOI PMC

Gupta R. S., Naushad S., Baker S. (2014). Phylogenomic analyses and molecular signatures for the class Halobacteria and its two major clades: a proposal for division of the class Halobacteria into an emended order Halobacteriales and two new orders, Haloferacales ord. nov. and Natrialbales ord. nov. Int. J. Syst. Evol. Microbiol. 65, 1050–1069. 10.1099/ijs.0.070136-0 PubMed DOI

Haft D. H., Loftus B. J., Richardson D. L., Yang F., Eisen J. A., Paulsen I. T., et al. . (2001). TIGRFAMs: a protein family resource for the functional identification of proteins. Nucleic Acids Res. 29, 41–43. 10.1093/nar/29.1.41 PubMed DOI PMC

Hagedoorn P. L., Chen T., Schröder I., Piersma S. R., de Vries S., Hagen W. R. (2005). Purification and characterization of the tungsten enzyme aldehyde: ferredoxin oxidoreductase from the hyperthermophilic denitrifier Pyrobaculum aerophilum. J. Biol. Inorg. Chem. 10, 259–269. 10.1007/s00775-005-0637-5 PubMed DOI

Huang Y., Gilna P., Li W. (2009). Identification of ribosomal RNA genes in metagenomic fragments. Bioinformatics 25, 1338–1340. 10.1093/bioinformatics/btp161 PubMed DOI PMC

Hügler M., Huber H., Molyneaux S. J., Vetriani C., Sievert S. M. (2007). Autotrophic CO2 fixation via the reductive tricarboxylic acid cycle in different lineages within the phylum Aquificae: evidence for two ways of citrate cleavage. Environ. Microbiol. 9, 81–92. 10.1111/j.1462-2920.2006.01118.x PubMed DOI

Humayoun S. B., Bano N., Hollibaugh J. T. (2003). Depth distribution of microbial diversity in mono lake, a meromictic soda lake in California. Appl. Environ. Microbiol. 69, 1030–1042. 10.1128/AEM.69.2.1030-1042.2003 PubMed DOI PMC

Hyatt D., Chen G. L., LoCascio P. F., Land M. L., Larimer F. W., Hauser L. J. (2010). Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119. 10.1186/1471-2105-11-119 PubMed DOI PMC

Imhoff J. F. (1995). Taxonomy and physiology of phototrophic purple bacteria and green sulfur bacteria, in Anoxygenic Photosynthetic Bacteria, eds Blankenship R. E., Madigan M. T., Bauer C. E. (Dordrecht: Springer; ), 1–15.

Inoue K., Ono H., Abe-Yoshizumi R., Yoshizawa S., Ito H., Kogure K., et al. . (2013). A light-driven sodium ion pump in marine bacteria. Nat. Commun. 4:1678. 10.1038/ncomms2689 PubMed DOI

Isachenko B. L. (1951). Chloride, sulfate and soda lakes of the Kulunda steppe and the biogenic process in them, in Selected Works, Vol. 2 (Leningrad: Academy of Sciences USSR; ), 143–162.

Johnsen U., Selig M., Xavier K. B., Santos H., Schönheit P. (2001). Different glycolytic pathways for glucose and fructose in the halophilic archaeon Halococcus saccharolyticus. Arch. Microbiol. 175, 52–61. 10.1007/s002030000237 PubMed DOI

Jones B. F., Eugster H. P., Rettig S. L. (1977). Hydrochemistry of the Lake Magadi basin, Kenya. Geochim. Cosmochim. Acta 41, 53–72. 10.1016/0016-7037(77)90186-7 DOI

Jones C. M., Graf D. R., Bru D., Philippot L., Hallin S. (2013). The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink. ISME J. 7, 417–426. 10.1038/ismej.2012.125 PubMed DOI PMC

Jormakka M., Yokoyama K., Yano T., Tamakoshi M., Akimoto S., Shimamura T., et al. . (2008). Molecular mechanism of energy conservation in polysulfide respiration. Nat. Struct. Mol. Biol. 15, 730–737. 10.1038/nsmb.1434 PubMed DOI PMC

Keshri J., Mody K., Jha B. (2013). Bacterial community structure in a semi-arid haloalkaline soil using culture independent method. Geomicrobiol. J. 30, 517–529. 10.1080/01490451.2012.737092 DOI

King C. E. (2013). Diversity and Activity of Aerobic Thermophilic Carbon Monoxide-Oxidizing Bacteria on Kilauea Volcano, Hawaii. Ph.D. thesis, Louisiana State University.

King G. M. (2015). Carbon monoxide as a metabolic energy source for extremely halophilic microbes: implications for microbial activity in Mars regolith. Proc. Natl. Acad. Sci. U.S.A. 112, 4465–4470. 10.1073/pnas.1424989112 PubMed DOI PMC

King G. M., Weber C. F. (2007). Distribution, diversity and ecology of aerobic CO-oxidizing bacteria. Nat. Rev. Microbiol. 5, 107–118. 10.1038/nrmicro1595 PubMed DOI

Kompantseva E. I., Bryantseva I. A., Komova A. V., Namsaraev B. B. (2007). The structure of phototrophic communities of soda lakes of the southeastern Transbaikal Region. Microbiology 76, 211–219. 10.1134/S0026261707020130 PubMed DOI

Kompantseva E. I., Komova A. V., Sorokin D. Y. (2010). Communities of anoxygenic phototrophic bacteria in the saline soda lakes of the Kulunda Steppe (Altai region). Microbiology 79, 89–95. 10.1134/S0026261710010121 PubMed DOI

Kwon S. K., Kim B. K., Song J. Y., Kwak M. J., Lee C. H., Yoon J. H., et al. . (2013). Genomic makeup of the marine flavobacterium Nonlabens (Donghaeana) dokdonensis and identification of a novel class of rhodopsins. Genome Biol. Evol. 5, 187–199. 10.1093/gbe/evs134 PubMed DOI PMC

Lanzen A., Simachew A., Gessesse A., Chmolowska D., Jonassen I., Øvreås L. (2013). Surprising prokaryotic and eukaryotic diversity, community structure and biogeography of Ethiopian soda lakes. PLoS ONE 8:e72577. 10.1371/journal.pone.0072577 PubMed DOI PMC

Lassmann T., Sonnhammer E. L. (2005). Kalign–an accurate and fast multiple sequence alignment algorithm. BMC Bioinformatics 6:298. 10.1186/1471-2105-6-298 PubMed DOI PMC

Lauro F. M., DeMaere M. Z., Yau S., Brown M. V., Ng C., Wilkins D., et al. . (2011). An integrative study of a meromictic lake ecosystem in Antarctica. ISME J. 5, 879–895. 10.1038/ismej.2010.185 PubMed DOI PMC

León M. J., Fernández A. B., Ghai R., Sánchez-Porro C., Rodriguez-Valera F., Ventosa A. (2014). From metagenomics to pure culture: isolation and characterization of the moderately halophilic bacterium Spiribacter salinus gen. nov., sp. nov. Appl. Environ. Microbiol. 80, 3850–3857. 10.1128/AEM.00430-14 PubMed DOI PMC

Li D., Liu C. M., Luo R., Sadakane K., Lam T. W. (2015). MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31, 1674–1676. 10.1093/bioinformatics/btv033 PubMed DOI

Liu X., Gao C., Zhang A., Jin P., Wang L., Feng L. (2008). The nos gene cluster from gram-positive bacterium Geobacillus thermodenitrificans NG80-2 and functional characterization of the recombinant NosZ. FEMS Microbiol. Lett. 289, 46–52. 10.1111/j.1574-6968.2008.01362.x PubMed DOI

Llorens-Marès T., Yooseph S., Goll J., Hoffman J., Vila-Costa M., Borrego C. M., et al. . (2015). Connecting biodiversity and potential functional role in modern euxinic environments by microbial metagenomics. ISME J. 9, 1648–1661. 10.1038/ismej.2014.254 PubMed DOI PMC

Lombard V., Golaconda Ramulu H., Drula E., Coutinho P. M., Henrissat B. (2014). The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42(Database issue):D490–D495. 10.1093/nar/gkt1178 PubMed DOI PMC

López-Pérez M., Ghai R., Leon M. J., Rodríguez-Olmos Á., Copa-Patiño J. L., Soliveri J., et al. (2013). Genomes of “Spiribacter,” a streamlined, successful halophilic bacterium. BMC Genomics 14:787 10.1186/1471-2164-14-787 PubMed DOI PMC

Lowe T. M., Eddy S. R. (1997). tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955–964. 10.1093/nar/25.5.0955 PubMed DOI PMC

Lynch M. D., Neufeld J. D. (2015). Ecology and exploration of the rare biosphere. Nat. Rev. Microbiol. 13, 217–229. 10.1038/nrmicro3400 PubMed DOI

Marmur J. (1961). A procedure for isolation of DNA from microorganisms. J. Mol. Biol. 3, 208–214. 10.1016/S0022-2836(61)80047-8 DOI

Martin-Cuadrado A. B., Ghai R., Gonzaga A., Rodriguez-Valera F. (2009). CO dehydrogenase genes found in metagenomic fosmid clones from the deep Mediterranean Sea. Appl. Environ. Microbiol. 75, 7436–7444. 10.1128/AEM.01283-09 PubMed DOI PMC

Martin-Cuadrado A. B., Pašiæ L., Rodriguez-Valera F. (2015). Diversity of the cell-wall associated genomic island of the archaeon Haloquadratum walsbyi. BMC Genomics 16:603. 10.1186/s12864-015-1794-8 PubMed DOI PMC

Martínez-García M., Santos F., Moreno-Paz M., Parro V., Antón J. (2014). Unveiling viral–host interactions within the ‘microbial dark matter’. Nat. Commun. 5:4542. 10.1038/ncomms5542 PubMed DOI

Melack J. M. (1981). Photosynthetic activity of phytoplankton in tropical African soda lakes. Hydrobiologia 81, 71–85. 10.1007/BF00048707 DOI

Mesbah N. M., Abou-El-Ela S. H., Wiegel J. (2007). Novel and unexpected prokaryotic diversity in water and sediments of the alkaline, hypersaline lakes of the Wadi An Natrun, Egypt. Microbiol. Ecol. 54, 598–617. 10.1007/s00248-006-9193-y PubMed DOI

Milford A. D., Achenbach L. A., Jung D. O., Madigan M. T. (2000). Rhodobaca bogoriensis gen. nov. and sp. nov., an alkaliphilic purple nonsulfur bacterium from African Rift Valley soda lakes. Arch. Microbiol. 174, 18–27. 10.1007/s002030000166 PubMed DOI

Mongodin E. F., Nelson K. E., Daugherty S., Deboy R. T., Wister J., Khouri H., et al. . (2005). The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic Bacteria and Archaea. Proc. Natl. Acad. Sci. U.S.A. 102, 18147–18152. 10.1073/pnas.0509073102 PubMed DOI PMC

Moriya Y., Itoh M., Okuda S., Yoshizawa A., Kanehisa M. (2007). KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 35, 182–185. 10.1093/nar/gkm321 PubMed DOI PMC

Mwirichia R., Cousin S., Muigai A. W., Boga H. I., Stackebrandt E. (2011). Bacterial diversity in the haloalkaline Lake Elmenteita, Kenya. Curr. Microbiol. 62, 209–221. 10.1007/s00284-010-9692-4 PubMed DOI

Narasingarao P., Podell S., Ugalde J. A., Brochier-Armanet C., Emerson J. B., Brocks J. J., et al. . (2012). De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. ISME J. 6, 81–93. 10.1038/ismej.2011.78 PubMed DOI PMC

Ochsenreiter T., Pfeifer F., Schleper C. (2002). Diversity of Archaea in hypersaline environments characterized by molecular-phylogenetic and cultivation studies. Extremophiles 6, 267–274. 10.1007/s00792-001-0253-4 PubMed DOI

Oren A. (1994). The ecology of the extremely halophilic Archaea. FEMS Microbiol. Rev. 13, 415–439. 10.1111/j.1574-6976.1994.tb00060.x PubMed DOI

Oren A. (2013). Life at high salt concentrations, intracellular KCl concentrations, and acidic proteomes. Front. Microbiol. 4:315. 10.3389/fmicb.2013.00315 PubMed DOI PMC

Oren A. (2014). Taxonomy of halophilic Archaea: current status and future challenges. Extremophiles 18, 825–834. 10.1007/s00792-014-0654-9 PubMed DOI

Pagaling E., Wang H., Venables M., Wallace A., Grant W. D., Cowan D. A., et al. . (2009). Microbial biogeography of six salt lakes in inner Mongolia, China, and a salt lake in Argentina. Appl. Environ. Microbiol. 75, 5750–5760. 10.1128/AEM.00040-09 PubMed DOI PMC

Park B. H., Karpinets T. V., Syed M. H., Leuze M. R., Uberbacher E. C. (2010). CAZymes Analysis Toolkit (CAT): web service for searching and analyzing carbohydrate-active enzymes in a newly sequenced organism using CAZy database. Glycobiology 20, 1574–84. 10.1093/glycob/cwq106 PubMed DOI

Park S., Akira Y., Kazuhiro K. (2014). The family Rhodothermaceae, in The Prokaryotes– Other Major Lineages of Bacteria and the Archaea, eds Rosenberg E., DeLong E. F., Lory S., Stackebrandt E., Thompson F. (Berlin Heidelberg: Springer-Verlag; ), 849–856.

Parks D. H., Imelfort M., Skennerton C. T., Hugenholtz P., Tyson G. W. (2014). CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055. 10.1101/gr.186072.114 PubMed DOI PMC

Petitjean C., Deschamps P., López-García P., Moreira D. (2015). Rooting the domain Archaea by phylogenomic analysis supports the foundation of the new kingdom Proteoarchaeota. Genome Biol. Evol. 7, 191–204. 10.1093/gbe/evu274 PubMed DOI PMC

Rees H. C., Grant W. D., Jones B. E., Heaphy S. (2004). Diversity of Kenyan soda lake alkaliphiles assessed by molecular methods. Extremophiles 8, 63–71. 10.1007/s00792-003-0361-4 PubMed DOI

Rice P., Longden I., Bleasby A. (2000). EMBOSS: the European molecular biology open software suite. Trends Genet. 16, 276–277. 10.1016/S0168-9525(00)02024-2 PubMed DOI

Rinke C., Schwientek P., Sczyrba A., Ivanova N. N., Anderson I. J., Cheng J., et al. . (2013). Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431–437. 10.1038/nature12352 PubMed DOI

Rodriguez-Valera F., Ventosa A., Juez G., Imhoff J. F. (1985). Variation of environmental features and microbial populations with salt concentrations in a multi-pond saltern. Microbiol. Ecol. 11, 107–115. 10.1007/BF02010483 PubMed DOI

Say R. F., Fuchs G. (2010). Fructose 1, 6-bisphosphate aldolase/phosphatase may be an ancestral gluconeogenic enzyme. Nature 464, 1077–1081. 10.1038/nature08884 PubMed DOI

Sharon I., Banfield J. F. (2013). Genomes from metagenomics. Science 342, 1057–1058. 10.1126/science.1247023 PubMed DOI

Siebers B., Brinkmann H., Dörr C., Tjaden B., Lilie H., van der Oost J., et al. . (2001). Archaeal fructose-1, 6-bisphosphate aldolases constitute a new family of archaeal type class I aldolase. J. Biol. Chem. 276, 28710–28718. 10.1074/jbc.M103447200 PubMed DOI

Siebers B., Schönheit P. (2005). Unusual pathways and enzymes of central carbohydrate metabolism in Archaea. Curr. Opin. Microbiol. 8, 695–705. 10.1016/j.mib.2005.10.014 PubMed DOI

Simachew A., Lanzén A., Gessesse A., Øvreås L. (2015). Prokaryotic community diversity along an increasing salt gradient in a soda ash concentration pond. Microb. Ecol. 71, 326–338. 10.1007/s00248-015-0675-7 PubMed DOI

Sorokin D. Y., Abbas B., Geleijnse M., Pimenov G. N., Sukhacheva M. V., van Loosdrecht M. C. (2015b). Methanogenesis at extremely haloalkaline conditions in soda lakes of Kulunda Steppe (Altai, Russia). FEMS Microbiol. Ecol. 91:fiv016. 10.1093/femsec/fiv016 PubMed DOI

Sorokin D. Y., Banciu H. L., Muyzer G. (2015a). Functional microbiology of soda lakes. Curr. Opin. Microbiol. 25, 88–96. 10.1016/j.mib.2015.05.004 PubMed DOI

Sorokin D. Y., Berben T., Melton E. D., Overmars L., Vavourakis C. D., Muyzer G. (2014). Microbial diversity and biogeochemical cycling in soda lakes. Extremophiles 18, 791–809. 10.1007/s00792-014-0670-9 PubMed DOI PMC

Sorokin D. Y., Janssen A. J., Muyzer G. (2012). Biodegradation potential of halo (alkali) philic prokaryotes. Crit. Rev. Environ. Sci. Technol. 42, 811–856. 10.1080/10643389.2010.534037 DOI

Sorokin D. Y., Kublanov I. V., Gavrilov S. N., Rojo D., Roman P., Golyshin P. N., et al. . (2015c). Elemental sulfur and acetate can support life of a novel strictly anaerobic haloarchaeon. ISME J. 9, 240–252. 10.1038/ismej.2015.79 PubMed DOI PMC

Sorokin D. Y., Toshchakov S. V., Kolganova T. V., Kublanov I. V. (2015d). Halo(natrono)archaea isolated from hypersaline lakes utilize cellulose and chitin as growth substrates. Front. Microbiol. 6:942. 10.3389/fmicb.2015.00942 PubMed DOI PMC

Sorokin D. Y., Tourova T. P., Galinski E. A., Belloch C., Tindall B. J. (2006). Extremely halophilic denitrifying bacteria from hypersaline inland lakes Halovibrio denitrificans sp. nov. and Halospina denitrificans gen. nov., sp. nov., and evidence that the genus name Halovibrio (Fendrich 1989) with the type species H. variabilis should be associated with DSM 3050. Int. J. Syst. Evol. Microbiol. 56, 379–388. 10.1099/ijs.0.63964-0 PubMed DOI

Sorokin D. Y., Tourova T. P., Kuznetsov B. B., Bryantseva I. A., Gorlenko V. M. (2000). Roseinatronobacter thiooxidans gen. nov., sp. nov., a new alkaliphilic aerobic bacteriochlorophyll a—containing bacterium isolated from a soda lake. Microbiology 69, 75–82. 10.1007/BF02757261 PubMed DOI

Tamura K., Strecher G., Peterson D., Filipski A., Kumar S. (2013). MEGA6: molecular evolutionary genetics analysis version 6. Mol. Biol. Evol. 30, 2725–2729. 10.1093/molbev/mst197 PubMed DOI PMC

Tatusov R. L., Fedorova N. D., Jackson J. D., Jacobs A. R., Kiryutin B., Koonin E. V., et al. . (2003). The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:41. 10.1186/1471-2105-4-41 PubMed DOI PMC

Tindall B. J. (1988). Prokaryotic life in the alkaline, saline, athalassic environment, in Halophilic Bacteria, ed Rodriguez-Valera F. (Boca Raton, FL: CRC Press; ), 31–67.

Tourova T. P., Grechnikova M. A., Kuznetsov B. B., Sorokin D. Y. (2014). Phylogenetic diversity of bacteria in soda lake stratified sediments. Microbiology 83, 869–879. 10.1134/S0026261714060186 PubMed DOI

Tourova T. P., Kovaleva O. L., Bumazhkin B. K., Patutina E. O., Kuznetsov B. B., Bryantseva I. A., et al. (2011). Application of ribulose-1, 5-bisphosphate carboxylase/oxygenase genes as molecular markers for assessment of the diversity of autotrophic microbial communities inhabiting the upper sediment horizons of the saline and soda lakes of the Kulunda Steppe. Microbiology 80, 812–825. 10.1134/S0026261711060221 DOI

Tremblay J., Singh K., Fern A., Kirton E. S., He S., Woyke T., et al. . (2015). Primer and platform effects on 16S rRNA tag sequencing. Front. Microbiol. 6:771. 10.3389/fmicb.2015.00771 PubMed DOI PMC

Tyson G. W., Chapman J., Hugenholtz P., Allen E. E., Ram R. J., Richardson P. M., et al. . (2004) Community structure metabolism through reconstruction of microbial genomes. Nature 428, 37–43. 10.1038/nature02340 PubMed DOI

Ugalde J. A., Podell S., Narasingarao P., Allen E. E. (2011). Xenorhodopsins, an enigmatic new class of microbial rhodopsins horizontally transferred between archaea and bacteria. Biol. Direct 6:52. 10.1186/1745-6150-6-52 PubMed DOI PMC

Urios L., Agogué H., Lesongeur F., Stackebrandt E., Lebaron P. (2006). Balneola vulgaris gen. nov., sp. nov., a member of the phylum Bacteroidetes from the north-western Mediterranean Sea. Int. J. Syst. Evol. Microbiol. 56, 1883–1887. 10.1099/ijs.0.64285-0 PubMed DOI

Vaisman N., Oren A. (2009). Salisaeta longa gen. nov., sp. nov., a red, halophilic member of the Bacteroidetes. Int. J. Syst. Evol. Microbiol. 59, 2571–2574. 10.1099/ijs.0.010892-0 PubMed DOI

Wang Y. X., Li Y. P., Liu J. H., Xiao W., Lai Y. H., Li Z. Y., et al. . (2013). Gracilimonas mengyeensis sp. nov., a moderately halophilic bacterium isolated from a salt mine in Yunnan, south-western China. Int. J. Syst. Evol. Microbiol. 63, 3989–3993. 10.1099/ijs.0.052043-0 PubMed DOI

Wood D., Setubal J., Kaul R., Monks D., Kitajima J., Okura V., et al. . (2001). The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294, 2317–2323. 10.1126/science.1066804 PubMed DOI

Yoon J. H., Kang S. J., Jung Y. T., Oh T. K. (2009). Psychroflexus salinarum sp. nov., isolated from a marine solar saltern. Int. J. Syst. Evol. Microbiol. 59, 2404–2407. 10.1099/ijs.0.008359-0 PubMed DOI

Youssef N. H., Savage-Ashlock K. N., McCully A. L., Luedtke B., Shaw E. I., Hoff W. D., et al. . (2014). Trehalose/2-sulfotrehalose biosynthesis and glycine-betaine uptake are widely spread mechanisms for osmoadaptation in the Halobacteriales. ISME J. 8, 636–649. 10.1038/ismej.2013.165 PubMed DOI PMC

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