Prokaryotic and viral community of the sulfate-rich crust from Peñahueca ephemeral lake, an astrobiology analogue.


Journal

Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692

Informations de publication

Date de publication:
10 2019
Historique:
received: 29 01 2019
revised: 09 05 2019
accepted: 11 05 2019
pubmed: 16 5 2019
medline: 13 5 2020
entrez: 16 5 2019
Statut: ppublish

Résumé

Peñahueca is an athalassohaline hypersaline inland ephemeral lake originated under semiarid conditions in the central Iberian Peninsula (Spain). Its chemical composition makes it extreme for microbial life as well as a terrestrial analogue of other planetary environments. To investigate the persistence of microbial life associated with sulfate-rich crusts, we applied cultivation-independent methods (optical and electron microscopy, 16S rRNA gene profiling and metagenomics) to describe the prokaryotic community and its associated viruses. The diversity for Bacteria was very low and was vastly dominated by endospore formers related to Pontibacillus marinus of the Firmicutes phylum. The archaeal assemblage was more diverse and included taxa related to those normally found in hypersaline environments. Several 'metagenome assembled genomes' were recovered, corresponding to new species of Pontibacillus, several species from the Halobacteria and one new member of the Nanohaloarchaeota. The viral assemblage, although composed of the morphotypes typical of high salt systems, showed little similarity to previously isolated/reconstructed halophages. Several putative prophages of Pontibacillus and haloarchaeal hosts were identified. Remarkably, the Peñahueca sulfate-rich metagenome contained CRISPR-associated proteins and repetitions which were over 10-fold higher than in most hypersaline systems analysed so far.

Identifiants

pubmed: 31087616
doi: 10.1111/1462-2920.14680
doi:

Substances chimiques

RNA, Ribosomal, 16S 0
Sulfates 0
Sodium Chloride 451W47IQ8X

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3577-3600

Subventions

Organisme : European Regional Development Fund
ID : ESP2015-69540-R
Pays : International
Organisme : European Regional Development Fund
ID : AYA2011-24803
Pays : International
Organisme : Spanish Ministry of Economy
ID : CGL2015-66455-R
Pays : International
Organisme : Spanish Ministry of Economy
ID : CLG2015_66686-C3-3
Pays : International
Organisme : Spanish Ministry of Economy
ID : CLG2015_66686-C3-1
Pays : International

Informations de copyright

© 2019 Society for Applied Microbiology and John Wiley & Sons Ltd.

Références

Albertsen, M., Hugenholtz, P., Skarshewski, A., Nielsen, K.L., Tyson, G.W., and Nielsen, P.H. (2013) Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat Biotechnol 31: 533-538.
Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
Amann, R.I., Ludwig, W., and Schleifer, K.H. (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59: 143-169.
Andrei, A.S., Banciu, H.L., and Oren, A. (2012) Living with salt: metabolic and phylogenetic diversity of archaea inhabiting saline ecosystems. FEMS Microbiol Lett 330: 1-9.
Andrei, A.S., Robeson, M.S., 2nd, Baricz, A., Coman, C., Muntean, V., Ionescu, A., et al. (2015) Contrasting taxonomic stratification of microbial communities in two hypersaline meromictic lakes. ISME J 9: 2642-2656.
Antón, J., Llobet-Brossa, E., Rodriguez-Valera, F., and Amann, R. (1999) Fluorescence in situ hybridization analysis of the prokaryotic community inhabiting crystallizer ponds. Environ Microbiol 1: 517-523.
Antón, J., Rossello-Mora, R., Rodriguez-Valera, F., and Amann, R. (2000) Extremely halophilic bacteria in crystallizer ponds from solar salterns. Appl Environ Microbiol 66: 3052-3057.
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: D138-D141.
Baxter, B.K., Mangalea, M.R., Willcox, S., Sabet, S., Nagoulat, M.-N., and Griffith, J.D. (2011) Haloviruses of great salt Lake: a model for understanding viral diversity. In Halophiles and Hypersalyne Environments, Ventosa, A., Oren, A., and Ma, Y. (eds). Berlin: Springer, p. 190.
Belitsky, B.R., Brill, J., Bremer, E., and Sonenshein, A.L. (2001) Multiple genes for the last step of proline biosynthesis in Bacillus subtilis. J Bacteriol 183: 4389-4392.
Blanco, Y., Moreno-Paz, M., and Parro, V. (2017) Experimental protocol for detecting cyanobacteria in liquid and solid samples with an antibody microarray chip. J Vis Exp 120: e54994.
Bland, C., Ramsey, T.L., Sabree, F., Lowe, M., Brown, K., Kyrpides, N.C., and Hugenholtz, P. (2007) CRISPR recognition tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinformatics 8: 209.
Boujelben, I., Gomariz, M., Martinez-Garcia, M., Santos, F., Pena, A., Lopez, C., et al. (2012a) Spatial and seasonal prokaryotic community dynamics in ponds of increasing salinity of Sfax solar saltern in Tunisia. Antonie Van Leeuwenhoek 101: 845-857.
Boujelben, I., Yarza, P., Almansa, C., Villamor, J., Maalej, S., Anton, J., and Santos, F. (2012b) Virioplankton community structure in Tunisian solar salterns. Appl Environ Microbiol 78: 7429-7437.
Brum, J.R., Hurwitz, B.L., Schofield, O., Ducklow, H.W., and Sullivan, M.B. (2016) Seasonal time bombs: dominant temperate viruses affect Southern Ocean microbial dynamics. ISME J 10: 437-449.
Buchfink, B., Xie, C., and Huson, D.H. (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12: 59-60.
Burns, D.G., Camakaris, H.M., Janssen, P.H., and Dyall-Smith, M.L. (2004) Combined use of cultivation-dependent and cultivation-independent methods indicates that members of most haloarchaeal groups in an Australian crystallizer pond are cultivable. Appl Environ Microbiol 70: 5258-5265.
Burstein, D., Harrington, L.B., Strutt, S.C., Probst, A.J., Anantharaman, K., Thomas, B.C., et al. (2016) New CRISPR-Cas systems from uncultivated microbes. Nature 542: 237-241.
Cabello-Yeves, P.J., Zemskaya, T.I., Rosselli, R., Coutinho, F.H., Zakharenko, A.S., Blinov, V.V., and Rodriguez-Valera, F. (2017) Genomes of novel microbial lineages assembled from the sub-ice waters of Lake Baikal. Appl Environ Microbiol 8: e02132-e02117.
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
Chen, F., Lu, J.R., Binder, B.J., Liu, Y.C., and Hodson, R.E. (2001) Application of digital image analysis and flow cytometry to enumerate marine viruses stained with SYBR gold. Appl Environ Microbiol 67: 539-545.
Chen, Y.G., Zhang, Y.Q., Xiao, H.D., Liu, Z.X., Yi, L.B., Shi, J.X., et al. (2009) Pontibacillus halophilus sp. nov., a moderately halophilic bacterium isolated from a sea urchin. Int J Syst Evol Microbiol 59: 1635-1639.
Chen, Y.G., Zhang, Y.Q., Yi, L.B., Li, Z.Y., Wang, Y.X., Xiao, H.D., et al. (2010) Pontibacillus litoralis sp. nov., a facultatively anaerobic bacterium isolated from a sea anemone, and emended description of the genus Pontibacillus. Int J Syst Evol Microbiol 60: 560-565.
Chou, I.M., and Seal Li, R.R. (2007) Magnesium and calcium sulfate stabilities and the water budget of Mars. J Geophys Res E: Planets 112: E11004.
Crisler, J.D., Newville, T.M., Chen, F., Clark, B.C., and Schneegurt, M.A. (2012) Bacterial growth at the high concentrations of magnesium sulfate found in martian soils. Astrobiology 12: 98-106.
Crits-Christoph, A., Gelsinger, D.R., Ma, B., Wierzchos, J., Ravel, J., Davila, A., et al. (2016) Functional interactions of archaea, bacteria and viruses in a hypersaline endolithic community. Environ Microbiol 18: 2064-2077.
Daas, M.S., Rosana, A.R.R., Acedo, J.Z., Nateche, F., Kebbouche-Gana, S., Vederas J.C., and Case, R.J. (2017) Draft genome sequences of Bacillus cereus E41 and Bacillus anthracis F34 isolated from Algerian salt lakes. Genome Announc 5.
Deole, R., Challacombe, J., Raiford, D.W., and Hoff, W.D. (2013) An extremely halophilic proteobacterium combines a highly acidic proteome with a low cytoplasmic potassium content. J Biol Chem 288: 581-588.
Di Meglio, L., Santos, F., Gomariz, M., Almansa, C., Lopez, C., Anton, J., and Nercessian, D. (2016) Seasonal dynamics of extremely halophilic microbial communities in three Argentinian salterns. FEMS Microbiol Ecol 92: 1-15.
Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., and Smith, F. (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28: 350-356.
Eddy, S.R. (2008) A probabilistic model of local sequence alignment that simplifies statistical significance estimation. PLoS Comput Biol 4: e1000069.
Emerson, J.B., Thomas, B.C., Andrade, K., Allen, E.E., Heidelberg, K.B., and Banfield, J.F. (2012) Dynamic viral populations in hypersaline systems as revealed by metagenomic assembly. Appl Environ Microbiol 78: 6309-6320.
Emerson, J.B., Andrade, K., Thomas, B.C., Norman, A., Allen, E.E., Heidelberg, K.B., and Banfield, J.F. (2013a) Virus-host and CRISPR dynamics in Archaea-dominated hypersaline Lake Tyrrell, Victoria, Australia. Archaea 2013: 370871.
Emerson, J.B., Thomas, B.C., Andrade, K., Heidelberg, K.B., and Banfield, J.F. (2013b) New approaches indicate constant viral diversity despite shifts in assemblage structure in an Australian hypersaline lake. Appl Environ Microbiol 79: 6755-6764.
Farlow, J., Bolkvadze, D., Leshkasheli, L., Kusradze, I., Kotorashvili, A., Kotaria, N., et al. (2018) Genomic characterization of three novel basilisk-like phages infecting Bacillus anthracis. BMC Genomics 19: 685.
Fernandez, A.B., Leon, M.J., Vera, B., Sanchez-Porro, C., and Ventosa, A. (2013) Metagenomic sequence of prokaryotic microbiota from an intermediate-salinity pond of a saltern in Isla Cristina. Spain Genome Announc 2: e00045-14.
Franca, L., Lopez-Lopez, A., Rossello-Mora, R., and da Costa, M.S. (2014) Microbial diversity and dynamics of a groundwater and a still bottled natural mineral water. Environ Microbiol 17: 577-593.
Gaillard, F., Michalski, J., Berger, G., McLennan, S.M., and Scaillet, B. (2013) Geochemical reservoirs and timing of sulfur cycling on Mars. Space Sci Rev 174: 251-300.
Galperin, M.Y., Makarova, K.S., Wolf, Y.I., and Koonin, E.V. (2015) Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acids Res 43: D261-D269.
Garcia, P., Monjardin, C., Martin, R., Madera, C., Soberon, N., Garcia, E., et al. (2008) Isolation of new Stenotrophomonas bacteriophages and genomic characterization of temperate phage S1. Appl Environ Microbiol 74: 7552-7560.
Garcia-Heredia, I., Martin-Cuadrado, A.B., Mojica, F.J., Santos, F., Mira, A., Antón, J., and Rodriguez-Valera, F. (2012) Reconstructing viral genomes from the environment using fosmid clones: the case of haloviruses. PLoS One 7: e33802.
Gendrin, A., Mangold, N., Bibring, J.P., Langevin, Y., Gondet, B., Poulet, F., et al. (2005) Sulfates in Martian layered terrains: the OMEGA/Mars express view. Science 307: 1587-1591.
Ghai, R., Martin-Cuadrado, A., Gonzaga, A., Garcia-Heredia, I., Cabrera, R., Martin, J., et al. (2010) Metagenome of the Mediterranenan deep Chlorophyl maximum studied by direct and fosmid library 454 pyrosequencing. ISME J 4: 1154-1166.
Ghai, R., Pašić, L., Fernández, A.B., Martin-Cuadrado, A.-B., Mizuno, C.M., McMahon, K.D., et al. (2011) New abundant microbial groups in aquatic hypersaline environments. Sci Rep 1: 135.
Gill, S., Catchpole, R., and Forterre, P. (2018) Extracellular membrane vesicles (EVs) in the three domains of life and beyond. FEMS Microbiol Rev 43: 273-303.
Godde, J.S., and Bickerton, A. (2006) The repetitive DNA elements called CRISPRs and their associated genes: evidence of horizontal transfer among prokaryotes. J Mol Evol 62: 718-729.
Gomariz, M., Martinez-Garcia, M., Santos, F., Rodriguez, F., Capella-Gutierrez, S., Gabaldon, T., et al. (2015) From community approaches to single-cell genomics: the discovery of ubiquitous hyperhalophilic Bacteroidetes generalists. ISME J 9: 16-31.
Goris, J., Konstantinidis, K.T., Klappenbach, J.A., Coenye, T., Vandamme, P., and Tiedje, J.M. (2007) DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57: 81-91.
Guixa-Boixereu, N. (1996) Viral lysis and bacterivory as prokaryotic loss factors along a salinity gradient. Aquat Microb Ecol 11: 213-227.
Haferburg, G., Groning, J.A.D., Schmidt, N., Kummer, N.A., Erquicia, J.C., and Schlomann, M. (2017) Microbial diversity of the hypersaline and lithium-rich Salar de Uyuni, Bolivia. Microbiol Res 199: 19-28.
Hammer, O., Harper, D., and Ryan, P. (2001) PAST: paleontological statistics software package for education and data analysis. Paleontol Electron 9: 9.
Han, R., Zhang, X., Liu, J., Long, Q., Chen, L., and Liu, D. Z. D(2017) Microbial community structure and diversity within hypersaline Keke salt Lake environments. Can J Microbiol 63: 895-908.
Hand, K.P., Murray, A.E., Garvin, J.B., Brinckerhoff, W.B., Christner, B.C., Edgett, K.S., et al. (2017) Report of the Europa Lander Sciwence Definition Team. Washington, DC: National Aeronautics and Space Administration.
Hawley, E.R., Schackwitz, W., and Hess, M. (2014) Metagenomic sequencing of two Salton Sea microbiomes. Genome Announc 2: e01208-13.
Hua, N.P., Hamza-Chaffai, A., Vreeland, R.H., Isoda H., and Naganuma, T. (2008) Virgibacillus salarius sp. nov., a halophilic bacterium isolated from a Saharan salt lake. Int J Syst Evol Microbiol 58: 2409-2414.
Huang, Y., Gilna, P., and Li, W. (2009) Identification of ribosomal RNA genes in metagenomic fragments. Bioinformatics 25: 1338-1340.
Huang, Y., Niu, B., Gao, Y., Fu, L., and Li, W. (2010) CD-HIT suite: a web server for clustering and comparing biological sequences. Bioinformatics 26: 680-682.
Huang, J., Qiao, Z.X., Tang, J.W., and Wang, G. (2015) High quality draft genome sequence of the moderately halophilic bacterium Pontibacillus yanchengensis Y32(T) and comparison among Pontibacillus genomes. Stand Genomic Sci 10: 93.
Hurlbert, S. (1971) The non-concept of species diversity: a critique and alternative parameters. Ecology 52: 577-586.
Huson, D.H., Auch, A.F., Qi, J., and Schuster, S.C. (2007) MEGAN analysis of metagenomic data. Genome Res 17: 377-386.
Hyatt, D., Chen, G.L., Locascio, P.F., Land, M.L., Larimer, F.W., and Hauser, L.J. (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119.
Jackson, S.A., McKenzie, R.E., Fagerlund, R.D., Kieper, S.N., Fineran, P.C., and Brouns, S.J. (2017) CRISPR-Cas: adapting to change. Science 7: 356.
Jeon, C.O., Lim, J.M., Jang, H.H., Park, D.J., Xu, L.H., Jiang C.L., and Kim, C.J. (2008) Gracilibacillus lacisalsi sp. nov., a halophilic Gram-positive bacterium from a salt lake in China. Int J Syst Evol Microbiol 58: 2282-2286.
Kertesz, M.A., and Wietek, C. (2001) Desulfurization and desulfonation: applications of sulfur-controlled gene expression in bacteria. Appl Microbiol Biotechnol 57: 460-466.
Konstantinidis, K.T., Rosselló-Móra, R., and Amann, R. (2017) Uncultivated microbes in need of their own taxonomy. ISME J 11: 2399-2406.
Koonin, E.V., Makarova, K.S., and Zhang, F. (2017) Diversity, classification and evolution of CRISPR-Cas systems. Curr Opin Microbiol 37: 67-78.
Kristensen, D.M., Waller, A.S., Yamada, T., Bork, P., Mushegian, A.R., and Koonin, E.V. (2013) Orthologous gene clusters and taxon signature genes for viruses of prokaryotes. J Bacteriol 195: 941-950.
Kumar, S., Stecher, G., and Tamura, K. (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33: 1870-1874.
Kunst, F., Ogasawara, N., Moszer, I., Albertini, A.M., Alloni, G., Azevedo, V., et al. (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390: 249-256.
La Cono, V., Smedile, F., Bortoluzzi, G., Arcadi, E., Maimone, G., Messina, E., et al. (2011) Unveiling microbial life in new deep-sea hypersaline Lake Thetis. Part I: prokaryotes and environmental settings. Environ Microbiol 13: 2250-2268.
La Cono, V., Bortoluzzi, G., Messina, E., La Spada, G., Smedile, F., Giuliano, L., et al. (2019) The discovery of Lake Hephaestus, the youngest athalassohaline deep-sea formation on earth. Sci Rep 9: 1679.
Lassmann, T., and Sonnhammer, E.L. (2005) Kalign--an accurate and fast multiple sequence alignment algorithm. BMC Bioinformatics 6: 298.
Lee, J.C., Kim, Y.S., Yun, B.S., and Whang, K.S. (2015) Pontibacillus salicampi sp. nov., a moderately halophilic bacterium isolated from saltern soil. Int J Syst Evol Microbiol 65: 375-380.
Lim, J.M., Jeon, C.O., Park, D.J., Kim, H.R., Yoon, B.J., and Kim, C.J. (2005) Pontibacillus marinus sp. nov., a moderately halophilic bacterium from a solar saltern, and emended description of the genus Pontibacillus. Int J Syst Evol Microbiol 55: 1027-1031.
Lopez-Perez, M., Ghai, R., Leon, M.J., Rodriguez-Olmos, A., Copa-Patino, J.L., Soliveri, J., et al. (2013) Genomes of "Spiribacter", a streamlined, successful halophilic bacterium. BMC Genomics 14: 787.
Lowe, T.M., and Eddy, S.R. (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955-964.
Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
Macau, F., and Riba, O. (1965) Situación, características y extensión de los terrenos yesíferos en España I. Madrid: Col. Internac. Las Obras Públicas en los Terrenos Yesíferos, pp. 1-28.
Makarova, K.S., Wolf, Y.I., and Koonin, E.V. (2015) Archaeal clusters of orthologous genes (arCOGs): an update and application for analysis of shared features between Thermococcales, Methanococcales, and Methanobacteriales. Life (Basel) 5: 818-840.
McCord, T.B., Hansen, G.B., Fanale, F.P., Carlson, R.W., Matson, D.L., Johnson, T.V., et al. (1998) Salts on Europa's surface detected by Galileo's near infrared mapping spectrometer, The NIMS Team. Science 280: 1242-1245.
Milliken, R.E., Ewing, R.C., Fischer, W.W., and Hurowitz, J. (2014) Wind-blown sandstones cemented by sulfate and clay minerals in gale crater, Mars. Geophys Res Lett 41: 1149-1154.
Montoya, L., Vizioli, C., Rodriguez, N., Rastoll, M.J., Amils, R., and Marin, I. (2013) Microbial community composition of Tirez lagoon (Spain), a highly sulfated athalassohaline environment. Aquat Biosyst 9: 19.
Mora-Ruiz Mdel, R., Font-Verdera, F., Diaz-Gil, C., Urdiain, M., Rodriguez-Valdecantos, G., Gonzalez, B., et al. (2015) Moderate halophilic bacteria colonizing the phylloplane of halophytes of the subfamily Salicornioideae (Amaranthaceae). Syst Appl Microbiol 38: 406-416.
Mora-Ruiz, M.D.R., Cifuentes, A., Font-Verdera, F., Perez-Fernandez, C., Farias, M.E., Gonzalez, B., et al. (2018) Biogeographical patterns of bacterial and archaeal communities from distant hypersaline environments. Syst Appl Microbiol 41: 139-150.
Munoz, R., Rossello-Mora, R., and Amann, R. (2016) Revised phylogeny of Bacteroidetes and proposal of sixteen new taxa and two new combinations including Rhodothermaeota phyl. Nov. Syst Appl Microbiol 39: 281-296.
Mutlu, M.B., Martinez-Garcia, M., Santos, F., Pena, A., Guven, K., and Anton, J. (2008) Prokaryotic diversity in Tuz Lake, a hypersaline environment in inland Turkey. FEMS Microbiol Ecol 65: 474-483.
Muyzer, G., and Smalla, K. (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek 73: 127-141.
Naghoni, A., Emtiazi, G., Amoozegar, M.A., Cretoiu, M.S., Stal, L.J., Etemadifar, Z., et al. (2017) Microbial diversity in the hypersaline Lake Meyghan, Iran. Sci Rep 7: 11522.
Nakonieczna, A., Cooper, C.J., and Gryko, R. (2015) Bacteriophages and bacteriophage-derived endolysins as potential therapeutics to combat gram-positive spore forming bacteria. J Appl Microbiol 119: 620-631.
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.
Oren, A. (2002a) Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Ind Microbiol Biotechnol 28: 56-63.
Oren, A. (2002b) Molecular ecology of extremely halophilic Archaea and bacteria. FEMS Microbiol Ecol 39: 1-7.
Oren, A. (2008) Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Syst 4: 2.
Oren, A. (2013) Life at high salt concentrations, intracellular KCl concentrations, and acidic proteomes. Front Microbiol 4: 315.
Oren, A., Bratbak, G., and Heldal, M. (1997) Occurrence of virus-like particles in the Dead Sea. Extremophiles 1: 143-149.
Oren, A., Sørensen, K., Canfield, D.E., Teske, A., Ionescu, D., Lipski, A., and Altendorf, K. (2009) Microbial communities and processes within a hypersaline gypsum crust in a saltern evaporation pond (Eilat, Israel). Hydrobiologia 626: 15-26.
Orlando, T.M., McCord, T.B., and Grieves, G.A. (2005) The chemical nature of Europa surface material and the relation to a subsurface ocean. Icarus 177: 528-533.
Ortmann, A.C., and Suttle, C.A. (2009) Determination of virus abundance by epifluorescence microscopy. Methods Mol Biol 501: 87-95.
Pagaling, E., Haigh, R.D., Grant, W.D., Cowan, D.A., Jones, B.E., Ma, Y., et al. (2007) Sequence analysis of an archaeal virus isolated from a hypersaline lake in Inner Mongolia, China. BMC Genomics 8: 410.
Parks, D.H., Imelfort, M., Skennerton, C.T., Hugenholtz, P., and Tyson, G.W. (2014) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25: 1043-1055.
Parro, V., Fernandez-Calvo, P., Rodriguez Manfredi, J.A., Moreno-Paz, M., Rivas, L.A., Garcia-Villadangos, M., et al. (2008) SOLID2: an antibody array-based life-detector instrument in a Mars drilling simulation experiment (MARTE). Astrobiology 8: 987-999.
Parro, V., de Diego-Castilla, G., Rodriguez-Manfredi, J.A., Rivas, L.A., Blanco-Lopez, Y., Sebastian, E., et al. (2011) SOLID3: a multiplex antibody microarray-based optical sensor instrument for in situ life detection in planetary exploration. Astrobiology 11: 15-28.
Peng, Y., Leung, H.C., Yiu, S.M., and Chin, F.Y. (2012) IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28: 1420-1428.
Pernthaler, A., and Amann, R. (2004) Simultaneous fluorescence in situ hybridization of mRNA and rRNA in environmental bacteria. Appl Environ Microbiol 70: 5426-5433.
Pietila, M.K., Laurinavicius, S., Sund, J., Roine, E., and Bamford, D.H. (2010) The single-stranded DNA genome of novel archaeal virus halorubrum pleomorphic virus 1 is enclosed in the envelope decorated with glycoprotein spikes. J Virol 84: 788-798.
Pilsyk, S., and Paszewski, A. (2009) Sulfate permeasesphylogenetic diversity of sulfate transport. Acta Biochim Pol 56: 375-384.
Pina, M., Bize, A., Forterre, P., and Prangishvili, D. (2011) The archeoviruses. FEMS Microbiol Rev 35: 1035-1054.
Podell, S., Ugalde, J.A., Narasingarao, P., Banfield, J.F., Heidelberg, K.B., and Allen, E.E. (2013) Assembly-driven community genomics of a hypersaline microbial ecosystem. PLoS One 8: e61692.
Porter, K., Kukkaro, P., Bamford, J.K., Bath, C., Kivela, H.M., Dyall-Smith, M.L., and Bamford, D.H. (2005) SH1: a novel, spherical halovirus isolated from an Australian hypersaline lake. Virology 335: 22-33.
Price, M.N., Dehal, P.S., and Arkin, A.P. (2010) FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One 5: e9490.
Prieto-Ballesteros, O., Rodriguez, N., Kargel, J.S., Kessler, C.G., Amils, R., and Remolar, D.F. (2003) Tirez lake as a terrestrial analog of Europa. Astrobiology 3: 863-877.
Pruesse, E., Peplies, J., and Glockner, F.O. (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28: 1823-1829.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., et al. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: D590-D596.
Raes, J., Korbel, J.O., Lercher, M.J., von Mering, C., and Bork, P. (2007) Prediction of effective genome size in metagenomic samples. Genome Biol 8: R10.
Ramos-Barbero, M.D., Martin-Cuadrado, A.B., Viver, T., Santos, F., Martinez-Garcia, M., and Anton, J. (2019a) Recovering microbial genomes from metagenomes in hypersaline environments: the good, the bad and the ugly. Syst Appl Microbiol 42: 30-40.
Ramos-Barbero, M.D., Martínez, J.M., Almansa, C., Rodríguez, N., Villamor, J., Gomariz, M., et al. (2019b) Prokaryotic and viral community structure in the singular chaotropic salt Lake Salar de Uyuni. Environ Microbio doi: 10.1111/1462-2920.14549. [Epub ahead of print].
Rasuk, M.C., Fernandez, A.B., Kurth, D., Contreras, M., Novoa, F., Poire, D., and Farias, M.E. (2016) Bacterial diversity in microbial Mats and Sediments from the Atacama Desert. Microb Ecol 71: 44-56.
Reith, J., and Mayer, C. (2011) Peptidoglycan turnover and recycling in gram-positive bacteria. Appl Microbiol Biotechnol 92: 1-11.
Rice, P., Longden, I., and Bleasby, A. (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16: 276-277.
Richter, M., and Rossello-Mora, R. (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106: 19126-19131.
Rivas, L.A., Garcia-Villadangos, M., Moreno-Paz, M., Cruz-Gil, P., Gomez-Elvira, J., and Parro, V. (2008) A 200-antibody microarray biochip for environmental monitoring: searching for universal microbial biomarkers through immunoprofiling. Anal Chem 80: 7970-7979.
Rocha, E.P., and Danchin, A. (2002) Base composition bias might result from competition for metabolic resources. Trends Genet 18: 291-294.
Rodriguez, R.L., Gunturu, S., Harvey, W.T., Rossello-Mora, R., Tiedje, J.M., Cole, J.R., and Konstantinidis, K.T. (2018) The microbial genomes atlas (MiGA) webserver: taxonomic and gene diversity analysis of Archaea and bacteria at the whole genome level. Nucleic Acids Res 46: W282-W288.
Rodriguez-Brito, B., Li, L., Wegley, L., Furlan, M., Angly, F., Breitbart, M., et al. (2010) Viral and microbial community dynamics in four aquatic environments. ISME J 4: 739-751.
Rodriguez-Valera, F., Ventosa, A., Juez, G., and Imhoff, J.F. (1985) Variation of environmental features and microbial populations with salt concentrations in a multi-pond saltern. Microb Ecol 11: 107-115.
Rothschild, L.J., and Mancinelli, R.L. (2001) Life in extreme environments. Nature 409: 1092-1101.
Roux, S., Krupovic, M., Debroas, D., Forterre, P., and Enault, F. (2013) Assessment of viral community functional potential from viral metagenomes may be hampered by contamination with cellular sequences. Open Biol 3: 130160.
Roux, S., Enault, F., Hurwitz, B.L., and Sullivan, M.B. (2015) VirSorter: mining viral signal from microbial genomic data. PeerJ 3: e985.
Rubin, S.S., Marin, I., Gomez, M.J., Morales, E.A., Zekker, I., San Martin-Uriz, P., et al. (2017) Prokaryotic diversity and community composition in the Salar de Uyuni, a large scale, chaotropic salt flat. Environ Microbiol 19: 3745-3754.
Rusch, D.B., Halpern, A.L., Sutton, G., Heidelberg, K.B., Williamson, S., Yooseph, S., et al. (2007) The sorcerer II Global Ocean sampling expedition: Northwest Atlantic through eastern tropical Pacific. PLoS Biol 5: e77.
Santos, F., Meyerdierks, A., Pena, A., Rossello-Mora, R., Amann, R., and Antón, J. (2007) Metagenomic approach to the study of halophages: the environmental halophage 1. Environ Microbiol 9: 1711-1723.
Santos, F., Yarza, P., Parro, V., Briones, C., and Antón, J. (2010) The metavirome of a hypersaline environment. Environ Microbiol 12: 2965-2976.
Santos, F., Moreno-Paz, M., Meseguer, I., Lopez, C., Rossello-Mora, R., Parro, V., and Antón, J. (2011) Metatranscriptomic analysis of extremely halophilic viral communities. ISME J 5: 1621-1633.
Sass, A.M., McKew, B.A., Sass, H., Fichtel, J., Timmis, K.N., and McGenity, T.J. (2008) Diversity of Bacillus-like organisms isolated from deep-sea hypersaline anoxic sediments. Saline Syst 4: 8.
Saum, S.H., and Müller, V. (2007) Salinity-dependent switching of osmolyte strategies in a moderately halophilic bacterium: glutamate induces proline biosynthesis in Halobacillus halophilus. J Bacteriol 189: 6968-6975.
Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., et al. (2009) Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
Schwenzer, S.P., Bridges, J.C., Wiens, R.C., Conrad, P.G., Kelley, S.P., Leveille, R., et al. (2016) Fluids during diagenesis and sulfate vein formation in sediments at Gale crater. Mars. Meteorit Planet Sci 51: 2175-2202.
Seed, K.D., Lazinski, D.W., Calderwood, S.B., and Camilli, A. (2013) A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 494: 489-491.
Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504.
Sime-Ngando, T., Lucas, S., Robin, A., Tucker, K.P., Colombet, J., Bettarel, Y., et al. (2010) Diversity of virus-host systems in hypersaline Lake Retba, Senegal. Environ Microbiol 13: 1956-1972.
Snaidr, J., Amann, R., Huber, I., Ludwig, W., and Schleifer, K.H. (1997) Phylogenetic analysis and in situ identification of bacteria in activated sludge. Appl Environ Microbiol 63: 2884-2896.
Soding, J., Biegert, A., and Lupas, A.N. (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33: W244-W248.
Sorokin, D.Y., Tourova, T.P., Kolganova, T.V., Detkova, E.N., Galinski, E.A., and Muyzer, G. (2011) Culturable diversity of lithotrophic haloalkaliphilic sulfate-reducing bacteria in soda lakes and the description of Desulfonatronum thioautotrophicum sp. nov., Desulfonatronum thiosulfatophilum sp. nov., Desulfonatronovibrio thiodismutans sp. nov., and Desulfonatronovibrio magnus sp. nov. Extremophiles 15: 391-401.
Summer, E.J., Gill, J.J., Upton, C., Gonzalez, C.F., and Young, R. (2007) Role of phages in the pathogenesis of Burkholderia, or 'Where are the toxin genes in Burkholderia phages?'. Curr Opin Microbiol 10: 410-417.
Suttle, C.A., and Fuhrman, J. (2010) Enumeration of virus particles in aquatic or sediment samples by epifluorescence microscopy. In Manual of Aquatic Viral Ecology, Wilhelm, S.W., Weinbauer, M.G., and Suttle, C.A. (eds). Waco, TX: American Society of Limnology and Oceanography, pp. 145-153.
Tang, S.L., Nuttall, S., Ngui, K., Fisher, C., Lopez, P., and Dyall-Smith, M. (2002) HF2: a double-stranded DNA tailed haloarchaeal virus with a mosaic genome. Mol Microbiol 44: 283-296.
Tatusov, R.L., Natale, D.A., Garkavtsev, I.V., Tatusova, T.A., Shankavaram, U.T., Rao, B.S., et al. (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29: 22-28.
Tuross, N., and Stathoplos, L. (1993) Ancient proteins in fossil bones. Methods Enzymol 224: 121-129.
Ulyantsev, V.I., Kazakov, S.V., Dubinkina, V.B., Tyakht, A.V., and Alexeev, D.G. (2016) MetaFast: fast reference-free graph-based comparison of shotgun metagenomic data. Bioinformatics 32: 2760-2767.
Vaniman, D.T., Bish, D.L., Chipera, S.J., Fialips, C.I., Carey, J.W., and Feldman, W.C. (2004) Magnesium sulphate salts and the history of water on Mars. Nature 431: 663-665.
Vavourakis, C.D., Ghai, R., Rodriguez-Valera, F., Sorokin, D.Y., Tringe, S.G., Hugenholtz, P., and Muyzer, G. (2016) Metagenomic insights into the uncultured diversity and physiology of microbes in four hypersaline soda lake brines. Front Microbiol 7: 211.
Ventosa, A., de la Haba, R.R., Sanchez-Porro, C., and Papke, R.T. (2015) Microbial diversity of hypersaline environments: a metagenomic approach. Curr Opin Microbiol 25: 80-87.
Vera-Gargallo, B., and Ventosa, A. (2018) Metagenomic insights into the phylogenetic and metabolic diversity of the prokaryotic community dwelling in hypersaline soils from the Odiel saltmarshes (SW Spain). Genes (Basel) 9: E152.
Wu, Y.W., Simmons, B.A., and Singer, S.W. (2016) MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics 32: 605-607.
Yakimov, M.M., La Cono, V., Slepak, V.Z., La Spada, G., Arcadi, E., Messina, E., et al. (2013) Microbial life in the Lake Medee, the largest deep-sea salt-saturated formation. Sci Rep 3: 3554.
Yang, Y., Zou, Z., He, M., and Wang, G. (2011) Pontibacillus yanchengensis sp. nov., a moderately halophilic bacterium isolated from salt field soil. Int J Syst Evol Microbiol 61: 1906-1911.
Yarza, P., Ludwig, W., Euzeby, J., Amann, R., Schleifer, K.H., Glockner, F.O., and Rossello-Mora, R. (2010) Update of the all-species living tree project based on 16S and 23S rRNA sequence analyses. Syst Appl Microbiol 33: 291-299.
Yébenes, A., Marfil, R., Soriano, Y., De La Peña, Y.A., and Díaz Molina, M. (1977) El Trías de Alcázar de San Juan (Región de La Mancha). J Iber Geol 4: 495-508.
Zolotov, M.Y., and Shock, E.L. (2001) Composition and stability of salts on the surface of Europa and their oceanic origin. J Geophys Res 106: 32815-32827.

Auteurs

Ana-Belen Martin-Cuadrado (AB)

Department of Physiology, Genetics and Microbiology, University of Alicante, Alicante, Spain.

Ece Senel (E)

Department of Physiology, Genetics and Microbiology, University of Alicante, Alicante, Spain.
Department of Biology, Graduate School of Sciences, Eskisehir Technical University, Yunusemre Campus, Eskisehir, 26470, Turkey.

Manuel Martínez-García (M)

Department of Physiology, Genetics and Microbiology, University of Alicante, Alicante, Spain.

Ana Cifuentes (A)

Department of Ecology and Marine Resources, Marine Microbiology Group, Mediterranean Institute for Advanced Studies (IMEDEA, CSIC-UIB), Esporles, Spain.

Fernando Santos (F)

Department of Physiology, Genetics and Microbiology, University of Alicante, Alicante, Spain.

Cristina Almansa (C)

Research Technical Services (SSTTI), Microscopy Unit, University of Alicante, Alicante, Spain.

Mercedes Moreno-Paz (M)

Department of Molecular Evolution, Centro de Astrobiología (INTA-CSIC), Madrid, Spain.

Yolanda Blanco (Y)

Department of Molecular Evolution, Centro de Astrobiología (INTA-CSIC), Madrid, Spain.

Miriam García-Villadangos (M)

Department of Molecular Evolution, Centro de Astrobiología (INTA-CSIC), Madrid, Spain.

María Ángeles García Del Cura (MÁG)

Institute of Geosciences IGEO (CSIC, UCM), Madrid, Spain.

María Esther Sanz-Montero (ME)

Department of Mineralogy and Petrology, Faculty of Geology, Complutense University, Madrid, Spain.

Juan Pablo Rodríguez-Aranda (JP)

Department of Didactics of Sciences, Faculty of Education, Complutense University, Madrid, Spain.

Ramon Rosselló-Móra (R)

Department of Biology, Graduate School of Sciences, Eskisehir Technical University, Yunusemre Campus, Eskisehir, 26470, Turkey.

Josefa Antón (J)

Department of Physiology, Genetics and Microbiology, University of Alicante, Alicante, Spain.

Víctor Parro (V)

Department of Molecular Evolution, Centro de Astrobiología (INTA-CSIC), Madrid, Spain.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing
Animals Hemiptera Insect Proteins Phylogeny Insecticides
Populus Soil Microbiology Soil Microbiota Fungi
Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins

Classifications MeSH