Genomic and phenotypic attributes of novel salinivibrios from stromatolites, sediment and water from a high altitude lake

BMC Genomics

Fabiano L Thompson³  Cristiane C Thompson²  Maria E Farias¹  Gustavo B Gregoracci²  Milene MA Mesquita²  Bruno S Silva²  Amaro E Trindade-Silva⁴  Luciane A Chimetto²  Graciela M Dias²  Marta F Gorriti² 

[1] Laboratorio de Investigaciones Microbiológicas de Lagunas Andinas (LIMLA), Planta Piloto de Procesos Industriales Microbiológicos (PROIMI), CCT, CONICET, San Miguel de Tucumán, Tucumán, Argentina;Laboratório de Microbiologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, Brasil;Av. Carlos Chagas Fo. S/N – CCS – IB –Laboratório de Microbiologia – Bloco A (Anexo) A3 – sl 102 – Cidade Universitária, Rio de Janeiro, RJ, Brasil;Núcleo de Biotecnologia Ambiental, Mestrado Profissional em Tecnologias Aplicáveis a Bioenergia, Faculdade de Tecnologia e Ciências (FTC), Salvador, Brasil

关键词: Extreme environment;    Xanthorhodopsin;    UV radiation;    Salinity;    Arsenic;   

Others  :  1216578
DOI  :  10.1186/1471-2164-15-473

 received in 2013-12-31, accepted in 2014-06-06,  发布年份 2014

【 摘 要 】

Background

Salinivibrios are moderately halophilic bacteria found in salted meats, brines and hypersaline environments. We obtained three novel conspecific Salinivibrio strains closely related to S. costicola, from Socompa Lake, a high altitude hypersaline Andean lake (approx. 3,570 meters above the sea level).

Results

The three novel Salinivibrio spp. were extremely resistant to arsenic (up to 200 mM HAsO4²⁻), NaCl (up to 15%), and UV-B radiation (19 KJ/m², corresponding to 240 minutes of exposure) by means of phenotypic tests. Our subsequent draft genome ionsequencing and RAST-based genome annotation revealed the presence of genes related to arsenic, NaCl, and UV radiation resistance. The three novel Salinivibrio genomes also had the xanthorhodopsin gene cluster phylogenetically related to Marinobacter and Spiribacter. The genomic taxonomy analysis, including multilocus sequence analysis, average amino acid identity, and genome-to-genome distance revealed that the three novel strains belong to a new Salinivibrio species.

Conclusions

Arsenic resistance genes, genes involved in DNA repair, resistance to extreme environmental conditions and the possible light-based energy production, may represent important attributes of the novel salinivibrios, allowing these microbes to thrive in the Socompa Lake.

【 授权许可】

   
2014 Gorriti et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Farias ME, Rascovan N, Toneatti DM, Albarracin VH, Flores MR, Poire DG, Collavino MM, Aguilar OM, Vazquez MP, Polerecky L: The discovery of stromatolites developing at 3570 m above sea level in a high-altitude volcanic lake Socompa, Argentinean Andes. PLos One 2013, 8(1):e53497.
• [2]Allwood AC, Walter MR, Kamber BS, Marshall CP, Burch IW: Stromatolite reef from the early Archaean era of Australia. Nature 2006, 441(7094):714-718.
• [3]Burne RV, Moore LS: Microbialites; organosedimentary deposits of benthic microbial communities. Palaios 1987, 2:241-254.
• [4]Schopf JW: Fossil evidence of Archaean life. Philos Trans R Soc B: Biol Sci 2006, 361(1470):869-885.
• [5]Riding R: The nature of stromatolites: 3,500 million years of history and a century of research. In Advances in Stromatolite Geobiology, Volume. Edited by Reitner J, Queric N-V, Gernot A. Berlin Heidelberg: Springer; 2011:29-74.
• [6]Hoffman P: Chapter 6.1 Stromatolite morphogenesis in Shark Bay, Western Australia, Volume 20. Amsterdam: Elsevier; 1976.
• [7]Jones B, Renaut RW, Konhauser KO: Genesis of large siliceous stromatolites at Frying Pan Lake, Waimangu geothermal field, North Island, New Zealand. Sedimentology 2005, 52:1229-1252.
• [8]Pedley M: Ambient temperature freshwater microbial tufas. Heidelberg: Springer; 2000.
• [9]Play ford PE, Cockbain AE: Modern Algal Stromatolites at Hamelin Pool, A Hypersaline Barred Basin in Shark Bay, Western Australia. In Developments in Sedimentology, Volume. Edited by Walter MR. Amsterdam: Elsevier; 1976:389-411.
• [10]Souza V, Espinosa-Asuar L, Escalante AE, Eguiarte LE, Farmer J, Forney L, Lloret L, Rodriguez-Martinez JM, Soberon X, Dirzo R, Elser JJ: An endangered oasis of aquatic microbial biodiversity in the Chihuahuan desert. Proc Natl Acad Sci U S A 2006, 103(17):6565-6570.
• [11]Takashima C, Kano A: Microbial processes forming daily lamination in a stromatolitic travertine. Sedimentary Geology 2008, 208(3–4):114-119.
• [12]Walter MR, Bauld J, Brock TD: Siliceous algal and bacterial stromatolites in hot spring and geyser effluents of yellowstone national park. Science 1972, 178(4059):402-405.
• [13]Smith FE: An investigation of a tait in rib bones of bacon. The determination of halophilic vibrio (n.ssp). Proc R Soc Queensland 1938, 49:29-52.
• [14]Mellado E, Moore ERB, Nieto JJ, Ventosa A: Analysis of 16S rRNA gene sequences of Vibrio costicola strains: description of Salinivibrio costicola gen. Nov., comb. nov. Int J Syst Bacteriol 1996, 46:817-821.
• [15]Amoozegar MA, Schumann P, Hajighasemi M, Fatemi AZ, Karbalaei-Heidari HR HR: Salinivibrio proteolyticus sp. nov., a moderately halophilic and proteolytic species from a hypersaline lake in Iran. Int J Syst Evol Microbiol 2008, 58(Pt 5):1159-1163.
• [16]Chamroensaksri N, Tanasupawat S, Akaracharanya A, Visessanguan W, Kudo T, Itoh T: Salinivibrio siamensis sp. nov., from fermented fish (pla-ra) in Thailand. Int J Syst Evol Microbiol 2009, 59(Pt 4):880-885.
• [17]Romano I, Orlando P, Gambacorta A, Nicolaus B, Dipasquale L, Pascual J, Giordano A, Lama L: Salinivibrio sharmensis sp. nov., a novel haloalkaliphilic bacterium from a saline lake in Ras Mohammed Park (Egypt). Extremophiles 2011, 15(2):213-220.
• [18]Garcia MT, Ventosa A, Ruiz-Barraquero F, Kocur M: Taxonomic study and amended description of Vibrio costicola. Int J System Bacteriol 1987, 37:251-256.
• [19]Huang CY, Garcia JL, Patel BK, Cayol JL, Baresi L, Mah RA: Salinivibrio costicola subsp. vallismortis subsp. nov., a halotolerant facultative anaerobe from Death Valley, and emended description of Salinivibrio costicola. Int J Syst Evol Microbiol 2000, 50 Pt 2:615-622.
• [20]Oren A: Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Ind Microbiol Biotechnol 2002, 28(1):56-63.
• [21]Oren A: Halophilic Microorganisms and their Environments. In Cellular Origin and Life in Extreme Habitats. Edited by Seckbach J. London: Kluwer Academic Press; 2002. [Volume 5]
• [22]Ellwood DC, Keevil CW, Marsh PD, Brown CM, Wardell JN: Surface-associated growth. Phil Trans R Soc B 1982, 297(1088):517-532.
• [23]Eboigbodin KE, Ojeda JJ, Biggs CA: Investigating the surface properties of escherichia coli under glucose controlled conditions and its effect on aggregation. Langmuir 2007, 23(12):6691-6697.
• [24]Thompson JR, Randa MA, Marcelino LA, Tomita-Mitchell A, Lim E, Polz MF: Diversity and dynamics of a north atlantic coastal Vibrio community. Appl Environ Microbiol 2004, 70(7):4103-4110.
• [25]Makarova KS, Haft DH, Barrangou R, Brouns SJJ, Charpentier E, Horvath P, Moineau S, Mojica FJM, Wolf YI, Yakunin AF, Van der Oost J, Koonin EV: Evolution and classification of the CRISPR-Cas systems. Nat Rev Micro 2011, 9(6):467-477.
• [26]Almendros C, Mojica FJM, Díez-Villaseñor C, Guzmán NM, García-Martínez J: CRISPR-Cas functional module exchange in escherichia coli. mBio 2014, 5(1):e00767-13.
• [27]Haines KC, Guillard RRL: Growth of vitamin B12-requiring marine diatoms in mixed laboratory cultures with vitamin B12- producing marine bacteria. J Phycol 1974, 10(3):245-252.
• [28]Thompson C, Chimetto L, Edwards R, Swings J, Stackebrandt E, Thompson F: Microbial genomic taxonomy. BMC Genomics 2013, 14(1):913.
• [29]Romano I, Gambacorta A, Lama L, Nicolaus B, Giordano A: Salinivibrio costicola subsp. alcaliphilus subsp. nov., a haloalkaliphilic aerobe from Campania Region (Italy). Syst Appl Microbiol 2005, 28(1):34-42.
• [30]Drees JC, Lusetti SL, Cox MM: Inhibition of RecA Protein by the Escherichia coli RecX Protein: modulation by the RecA C terminus and filament functional state. J Biol Chem 2004, 279(51):52991-52997.
• [31]Cox MM: The RecA protein as a recombinational repair system. Mol Microbiol 1991, 5(6):1295-1299.
• [32]Smith GR: How RecBCD enzyme and Chi promote DNA break repair and recombination: a molecular biologist’s view. Microbiol Mol Biol Rev 2012, 76(2):217-228.
• [33]Wang J, Grossman L: Mutations in the helix-turn-helix motif of the Escherichia coli UvrA protein eliminate its specificity for UV-damaged DNA. J Biol Chem 1993, 268(7):5323-5331.
• [34]Sancar GB: Enzymatic photoreactivation: 50 years and counting. Mutat Res 2000, 451(1–2):25-37.
• [35]Sancar A: Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem Rev 2003, 103(6):2203-2237.
• [36]Weber S: Light-driven enzymatic catalysis of DNA repair: a review of recent biophysical studies on photolyase. BBA-Bioenergetics 2005, 1707(1):1-23.
• [37]Albarracin VH, Pathak GP, Douki T, Cadet J, Borsarelli CD, Gartner W, Farias ME: Extremophilic Acinetobacter strains from high-altitude lakes in Argentinean Puna: remarkable UV-B resistance and efficient DNA damage repair. Orig Life Evol Biosph 2012, 42(2–3):201-221.
• [38]Shivaji S, Chaturvedi P, Begum Z, Pindi1 PK, Manorama R, Padmanaban DA, Shouche YS, Pawar S, Vaishampayan P, Dutt CBS, Datta GN, Manchanda RK, Rao UR, Bhargava PM, Narlikar JV: Janibacter hoylei sp. nov., Bacillus isronensis sp. nov. and Bacillus aryabhattai sp. nov., isolated from cryotubes used for collecting air from the upper atmosphere. Int J Syst Evol Microbiol 2009, 59(12):2977-2986.
• [39]Oremland RS, Stolz JF, Hollibaugh JT: The microbial arsenic cycle in Mono Lake. Calif FEMS Microbiol Ecol 2004, 48(1):15-27.
• [40]Silver S, Phung LT: Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Appl Environ Microbiol 2005, 71(2):599-608.
• [41]Belfiore C, Ordonez OF, Farias ME: Proteomic approach of adaptive response to arsenic stress in Exiguobacterium sp. S17, an extremophile strain isolated from a high-altitude Andean Lake stromatolite. Extremophiles 2013, 17(3):421-431.
• [42]Erb TJ, Kiefer P, Hattendorf B, Gunther D, Vorholt JA: GFAJ-1 is an arsenate-resistant, phosphate-dependent organism. Science 2012, 337(6093):467-470.
• [43]Reaves ML, Sinha S, Rabinowitz JD, Kruglyak L, Redfield RJ: Absence of detectable arsenate in DNA from arsenate-grown GFAJ-1 cells. Science 2012, 337(6093):470-473.
• [44]Chen CM, Misra TK, Silver S, Rosen BP: Nucleotide sequence of the structural genes for an anion pump. The plasmid-encoded arsenical resistance operon. J Biol Chem 1986, 261:15030-15038.
• [45]Yung-Feng Lin ARW, Rosen BP: An arsenic metallochaperone for an arsenic detoxification pump. Proc Natl Acad Sci U S A 2006, 103(42):15616-15622.
• [46]Christopher Rensing MG, Rosen BP: Families of soft-metal-ion-transporting ATPases. J Bacteriol 2006, 181(19):5891-5897.
• [47]Mukhopadhyay R, Rosen BP, Phung LT, Silver S: Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol Rev 2002, 26(3):311-325.
• [48]Deckert G, Wa PV, Gaasterland T, Young WG, Lenox AL, Graham DE, Overbeek R, Snead MA, Keller M, Aujay M, Huber R, Feldman RA, Short JM, Olsen GJ, Swanson RV: The complete genome of the hyperthermophilic bacterium Aquifex aeolicus. Nature 1998, 392:353-358.
• [49]Hideto Takami KN, Takaki Y, Maeno G, Sasaki R, Masui N, Fuji F, Hirama C, Nakamura Y, Ogasawara1 N, Kuhara2 S, Horikoshi K: Complete genome sequence of the alkaliphilic bacterium Bacillus halodurans and genomic sequence comparison with Bacillus subtilis. Nucleic Acid Res 2000, 28(21):4317-4331.
• [50]She Q, Sing RK, Confalonieri F, Zivanovic Y, Allard G, Awayez MJ, Chan-Weiher CC-Y, Clausen G, Curtis BA, De Moorse A, Erauso G, Fletcher C, Gordon PMK, Heikamp-de Jongg I, Jeffries AC, Kozera CJ, Medina N, Peng X, Thi-Ngoc HP, Redder P, Schenk ME, Theriault C, Tolstrup N, Charlebois RL, Doolittle WF, Duguet M, Gaasterland T, Garretta RA, Ragan MA, Sensen CW, et al.: The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc Natl Acad Sci U S A 2001, 98(14):7835-7840.
• [51]Landfald B, Strom AR: Choline-glycine betaine pathway confers a high level of osmotic tolerance in Escherichia coli. J Bacteriol 1986, 165(3):849-855.
• [52]Falb M, P F, Palm P, Rodewald K, Hickmann V, Tittor J, Oesterhelt D: Living with two extremes: Conclusions from the genome sequence of Natronomonas pharaonis. Genome Res 2005, 15:1336-1343.
• [53]Sculachev VP: Membrane Bioenergetics. Berlin, New York: Springer-Verlag; 1988.
• [54]Epstein E, Rains DW: Carrier-mediated cation transport in barley roots: kinetic evidence for a spectrum of active sites. Proc Natl Acad Sci U S A 1965, 53(6):1320-1324.
• [55]Lucht JM, Bremer E: Adaptation of Escherichia coli to high osmolarity environments: osmoregulation of the high-affinity glycine betaine transport system proU. FEMS Microbiol Rev 1994, 14(1):3-20.
• [56]Nakamura T, Yamamuro N, Stumpe S, Unemoto T, Bakker EP: Cloning of the trkAH gene cluster and characterization of the Trk K(+)-uptake system of Vibrio alginolyticus. Microbiology 1998, 144(Pt 8):2281-2289.
• [57]Borowitzka LJ, Brown AD: The salt relations of marine and halophilic species of the unicellular green alga, Dunaliella. The role of glycerol as a compatible solute. Arch Mikrobiol 1974, 96(1):37-52.
• [58]Petrovic U, Gunde-Cimerman N, Plemenitas A: Cellular responses to environmental salinity in the halophilic black yeast Hortaea werneckii. Mol Microbiol 2002, 45(3):665-672.
• [59]Roberts MF: Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst 2005, 1:5.
• [60]Ciulla RA, Diaz MR, Taylor BF, Roberts MF: Organic osmolytes in aerobic bacteria from mono lake, an alkaline, moderately hypersaline environment. Appl Environ Microbiol 1997, 63(1):220-226.
• [61]Severin J, Wohlfarth A, Galinski EA: The predominant role of recently discovered tetrahydropyrimidines for the osmoadaptation of halophilic eubacteria. J Gen Microbiol 1992, 138(8):1629-1638.
• [62]Karbalaei-Heidari HR, Ziaee AA, Amoozegar MA, Cheburkin Y, Budisa N: Molecular cloning and sequence analysis of a novel zinc-metalloprotease gene from the Salinivibrio sp. strain AF-2004 and its extracellular expression in E. coli. Gene 2008, 31(1–2):196-203.
• [63]Coronado MJ, Vargas C, Mellado E, Tegos G, Drainas C, Nieto JJ, Ventosa A: The alpha-amylase gene amyH of the moderate halophile Halomonas meridiana: cloning and molecular characterization. Microbiology 2000, 146(4):861-868.
• [64]Häse CC, Finkelstein RA: Bacterial extracellular zinc-containing metalloproteases. Microbiol Rev 1993, 57(4):823-837.
• [65]Lodeyro AF, Ceccoli RD, Pierella Karlusich JJ, Carrillo N: The importance of flavodoxin for environmental stress tolerance in photosynthetic microorganisms and transgenic plants. Mechanism, evolution and biotechnological potential. FEBS Lett 2012, 586(18):2917-2924.
• [66]Sancho J: Flavodoxins: sequence, folding, binding, function and beyond. Cell Mol Life Sci 2006, 63(7–8):855-864.
• [67]Hase T, Schürmann P, Knaff D: The Interaction of Ferredoxin with Ferredoxin-Dependent Enzymes. In Photosystem I, Volume 24. Edited by Golbeck J. Netherlands: Springer; 2006:477-498.
• [68]van der Ploeg JR, Eichhorn E, Leisinger T: Sulfonate-sulfur metabolism and its regulation in Escherichia coli. Arch Microbiol 2001, 176(1–2):1-8.
• [69]Béja O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP, Jovanovich SV, Gates CM, Feldman RA, Spudich JL, DeLong EF: Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 2000, 289:1902-1905.
• [70]Misawa N, Satomi Y, Kondo K, Yokoyama A, Kajiwara S, Saito T, Ohtani T, Miki W: Structure and functional analysis of a marine bacterial carotenoid biosynthesis gene cluster and astaxanthin biosynthetic pathway proposed at the gene level. J Bacteriol 1995, 177(22):6575-6584.
• [71]Peck RF, Echavarri-Erasun C, Johnson EA, Ng WV, Kennedy SP, Hood L, DasSarma S, Krebs MP: brp and blh are required for synthesis of the retinal cofactor of bacteriorhodopsin in Halobacterium salinarum. J Biol Chem 2001, 276(8):5739-5744.
• [72]Sabehi G, Loy A, Jung KH, Partha R, Spudich JL, Isaacson T, Hirschberg J, Wagner M, Beja O: New insights into metabolic properties of marine bacteria encoding proteorhodopsins. PLoS Biol 2005, 3(8):e273.
• [73]Balashov SP, Imasheva ES, Boichenko VA, Anton J, Wang JM, Lanyi JK: Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna. Science 2005, 309(5743):2061-2064.
• [74]Luecke H, Richter HT, Lanyi JK: Proton transfer pathways in bacteriorhodopsin at 2.3 angstrom resolution. Science 1998, 280(5371):1934-1937.
• [75]Peralvarez-Marin A, Marquez M, Bourdelande JL, Querol E, Padros E: Thr-90 plays a vital role in the structure and function of bacteriorhodopsin. J Biol Chem 2004, 279(16):16403-16409.
• [76]Spudich JL, Yang CS, Jung KH, Spudich EN: Retinylidene proteins: structures and functions from archaea to humans. Annu Rev Cell Dev Biol 2000, 16:365-392.
• [77]Lemke HD, Oesterhelt D: Lysine 216 is a binding site of the retinyl moiety in bacteriorhodopsin. FEBS Lett 1981, 128(2):255-260.
• [78]Rammelsberg R, Huhn G, Lubben M, Gerwert K: Bacteriorhodopsin’s intramolecular proton-release pathway consists of a hydrogen-bonded network. Biochemistry 1998, 37(14):5001-5009.
• [79]Quail MA, Smith M, Coupland P, Otto TD, Harris SR, Connor TR, Bertoni A, Swerdlow HP, Gu Y: A tale of three next generation sequencing platforms: comparison of Ion Torrent, Pacific Biosciences and Illumina MiSeq sequencers. BMC Genomics 2012, 13:341.
• [80]Rothberg JM, Hinz W, Rearick TM, Schultz J, Mileski W, Davey M, Leamon JH, Johnson K, Milgrew MJ, Edwards M, Hoon J, Simons JF, Marran D, Myers JW, Davidson JF, Branting A, Nobile JR, Puc BP, Light D, Clark TA, Huber M, Branciforte JT, Stoner IB, Cawley SE, Lyons M, Fu Y, Homer N, Sedova M, Miao X, Reed B: An integrated semiconductor device enabling non-optical genome sequencing. Nature 2011, 475(7356):348-352.
• [81]Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, Paern J, Lopez R: A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 2010, 38(suppl 2):W695-W699.
• [82]Man D, Wang W, Sabehi G, Aravind L, Post AF, Massana R, Spudich EN, Spudich JL, Beja O: Diversification and spectral tuning in marine proteorhodopsins. EMBO J 2003, 22(8):1725-1731.
• [83]Balashov SP, Imasheva ES, Choi AR, Jung KH, Liaaen-Jensen S, Lanyi JK: Reconstitution of gloeobacter rhodopsin with echinenone: role of the 4-keto group. Biochemistry 2010, 49(45):9792-9799.
• [84]Imasheva ESBS, Choi AR, Jung KH, Lanyi JK: Reconstitution of Gloeobacter violaceus rhodopsin with a light-harvesting carotenoid antenna. Bichemistry 2009, 48:10948-10955.
• [85]Luecke H, Schobert B, Stagno J, Imasheva ES, Wang JM, Balashov SP, Lanyi JK: Crystallographic structure of xanthorhodopsin, the light-driven proton pump with a dual chromophore. Proc Natl Acad Sci U S A 2008, 105(43):16561-16565.
• [86]Makino T, Harada H, Ikenaga H, Matsuda S, Takaichi S, Shindo K, Sandmann G, Ogata T, Misawa N: Characterization of cyanobacterial carotenoid ketolase CrtW and hydroxylase CrtR by complementation analysis in Escherichia coli. Plant Cell Physiol 2008, 49(12):1867-1878.
• [87]Mongodin EF, Nelson K, Daugherty S, Deboy R, Wister J, Khouri H, Weidman J, Walsh D, Papke R, Perez GS: The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc Natl Acad Sci U S A 2005, 102(50):18147-18152.
• [88]Vollmers J, Voget S, Dietrich S, Gollnow K, Smits M, Meyer K, Brinkhoff T, Simon M, Daniel R: Poles apart: arctic and antarctic octadecabacter strains share high genome plasticity and a new type of xanthorhodopsin. PLoS One 2013, 8(5):e63422.
• [89]Saitou N, Nei M: The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987, 4(4):406-425.
• [90]Jones DT, Taylor WR, Thornton JM: The rapid generation of mutation data matrices from protein sequences. Comp Appl Biosc 1992, 8(3):275-282.
• [91]Bohorquez LC, Ruiz-Perez CA, Zambrano MM: Proteorhodopsin-like genes present in thermoacidophilic high-mountain microbial communities. Appl Environ Microbiol 2012, 78(21):7813-7817.
• [92]Anton J, Oren A, Benlloch S, Rodriguez-Valera F, Amann R, Rossello-Mora R: Salinibacter ruber gen. nov., sp. nov., a novel, extremely halophilic member of the Bacteria from saltern crystallizer ponds. Int J Syst Evol Microbiol 2002, 52(Pt 2):485-491.
• [93]Fuhrman JA, Schwalbach MS, Stingl U: Proteorhodopsins: an array of physiological roles? Nat Rev Micro 2008, 6(6):488-494.
• [94]Kwon SK, Kim BK, Song JY, Kwak MJ, Lee CH, Yoon JH, Oh TK, Kim JF: Genomic makeup of the marine flavobacterium Nonlabens (Donghaeana) dokdonensis and identification of a novel class of rhodopsins. Genome Biol Evol 2013, 5(1):187-199.
• [95]Sharma AK, Spudich JL, Doolittle WF: Microbial rhodopsins: functional versatility and genetic mobility. Trends Microbiol 2006, 14(11):463-469.
• [96]Pitcher DG, Saunders NA, Owen RJ: Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett Appl Microbiol 1989, 8(4):151-156.
• [97]Chevreux BPT, Drescher B, Driesel AJ, Müller WEG, Wetter T, Suhai S: Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP Detection in sequenced ESTs. Genome Res 2004, 14:1147-1159.
• [98]Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O: The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008, 9:75.
• [99]Thompson CC, Vicente AC, Souza RC, Vasconcelos AT, Vesth T, Alves NJ, Ussery DW, Iida T, Thompson FL: Genomic taxonomy of vibrios. BMC Evol Biol 2009., 9(258)
• [100]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28(10):2731-2739.
• [101]Felsenstein J: Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783-791.
• [102]Tamura K, Nei M, Kumar S: Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 2004, 101(30):11030-11035.
• [103]Karlin S, Mrázek J, Campbell AM: Compositional biases of bacterial genomes and evolutionary implications. J Bacteriol 1997, 179(12):3899-3913.
• [104]Karlin S: Global dinucleotide signatures and analysis of genomic heterogeneity. Curr Opin Microbiol 1998, 1(5):598-610.
• [105]Auch AF, von Jan M, Klenk H-P, Göker M: Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2010, 2(1):117-134.
• [106]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23(21):2947-2948.