Phylogenetic Analysis of a Microbialite-Forming Microbial Mat from a Hypersaline Lake of the Kiritimati Atoll, Central Pacific

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Schneider, Dominik ^a   Arp, Gernot ^a   Reimer, Andreas ^a   Reitner, Joachim ^a   Daniel, Rolf ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CARBONATE; CALCIUM SULFATE; RNA 16S;

16S RRNA GENE; ALPHAPROTEOBACTERIA; ANAEROLINEAE; ARTICLE; BACTEROIDETES; CALDILINEAE; CHROMATIALES; CONTROLLED STUDY; CYANOBACTERIUM; DELTAPROTEOBACTERIA; EURYARCHAEOTA; GENE AMPLIFICATION; GENE SEQUENCE; HALOBACTERIALES; LAKE; MARINILABIACAE; MICROBIAL COMMUNITY; MICROBIAL MAT; MICROBIALITE; NITROSPIRAE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANCTOMYCETES; PYROSEQUENCING; SPIROCHETE; THAUMARCHAEOTA; THERMOPLASMATALES;

ARCHAEA; BACTERIA; BIODIVERSITY; DNA, ARCHAEAL; DNA, BACTERIAL; GEOLOGIC SEDIMENTS; LAKES; PHYLOGENY; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SALINITY; SEQUENCE ANALYSIS, DNA;

ALPHAPROTEOBACTERIA; ANAEROLINEAE; ARCHAEA; BACTERIA (MICROORGANISMS); BACTEROIDETES; CHLOROFLEXI; CHLOROFLEXI (CLASS); CHROMATIACEAE; CHROMATIALES; CYANOBACTERIA; DELTAPROTEOBACTERIA; EURYARCHAEOTA; HALOBACTERIA; HALOTHECE CLUSTER; NITROSPIRAE; PLANCTOMYCETES; PROTEOBACTERIA; SPIROCHAETES; THERMOPLASMATA;

EID: 84878872665     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066662     Document Type: Article

References (84)

1. Van Kranendonk MJ, Philippot P, Lepot K, Bodorkos S, Pirajno F, (2008) Geological setting of Earth's oldest fossils in the ca. 3.5 Ga Dresser Formation, Pilbara Craton, Western Australia. Precambrian Res 167: 93-124.
2. Allwood AC, Walter MR, Kamber BS, Marshall CP, Burch IW, (2006) Stromatolite reef from the Early Archaean era of Australia. Nature 441: 714-718.
3. Bontognali TR, Sessions AL, Allwood AC, Fischer WW, Grotzinger JP, et al. (2012) Sulfur isotopes of organic matter preserved in 3.45-billion-year-old stromatolites reveal microbial metabolism. Proc Natl Acad Sci U S A 109: 15146-15151.
4. Hoehler TM, Bebout BM, Des Marais DJ, (2001) The role of microbial mats in the production of reduced gases on the early Earth. Nature 412: 324-327.
5. Tice MM, Lowe DR, (2004) Photosynthetic microbial mats in the 3,416-Myr-old ocean. Nature 431: 549-552.
6. Dupraz C, Reid RP, Braissant O, Decho AW, Norman RS, et al. (2009) Processes of carbonate precipitation in modern microbial mats. Earth-Science Reviews 96: 141-162.
7. Van Gemerden H, (1993) Microbial mats: A joint venture. Marine Geology 113: 3-25.
8. Seckbach J, Oren A (2010) Microbial mats: modern and ancient microorganisms in stratified systems; Seckbach J, OrenA, Dordrecht; New York: Springer. 606.
9. Kirk Harris J, Gregory Caporaso J, Walker JJ, Spear JR, Gold NJ, et al. (2013) Phylogenetic stratigraphy in the Guerrero Negro hypersaline microbial mat. Isme J 7: 50-60.
10. Robertson CE, Spear JR, Harris JK, Pace NR, (2009) Diversity and stratification of archaea in a hypersaline microbial mat. Appl Environ Microbiol 75: 1801-1810.
11. Ley RE, Harris JK, Wilcox J, Spear JR, Miller SR, et al. (2006) Unexpected diversity and complexity of the Guerrero Negro hypersaline microbial mat. Appl Environ Microbiol 72: 3685-3695.
12. Feazel LM, Spear JR, Berger AB, Harris JK, Frank DN, et al. (2008) Eucaryotic diversity in a hypersaline microbial mat. Appl Environ Microbiol 74: 329-332.
13. Jahnke LL, Orphan VJ, Embaye T, Turk KA, Kubo MD, et al. (2008) Lipid biomarker and phylogenetic analyses to reveal archaeal biodiversity and distribution in hypersaline microbial mat and underlying sediment. Geobiology 6: 394-410.
14. Mobberley JM, Ortega MC, Foster JS, (2012) Comparative microbial diversity analyses of modern marine thrombolitic mats by barcoded pyrosequencing. Environ Microbiol 14: 82-100.
15. Myshrall KL, Mobberley JM, Green SJ, Visscher PT, Havemann SA, et al. (2010) Biogeochemical cycling and microbial diversity in the thrombolitic microbialites of Highborne Cay, Bahamas. Geobiology 8: 337-354.
16. Allen MA, Goh F, Burns BP, Neilan BA, (2009) Bacterial, archaeal and eukaryotic diversity of smooth and pustular microbial mat communities in the hypersaline lagoon of Shark Bay. Geobiology 7: 82-96.
17. Goh F, Allen MA, Leuko S, Kawaguchi T, Decho AW, et al. (2009) Determining the specific microbial populations and their spatial distribution within the stromatolite ecosystem of Shark Bay. Isme J 3: 383-396.
18. Sørensen KB, Canfield DE, Teske AP, Oren A, (2005) Community composition of a hypersaline endoevaporitic microbial mat. Appl Environ Microbiol 71: 7352-7365.
19. Arp G, Helms G, Karlinska K, Schumann G, Reimer A, et al. (2012) Photosynthesis versus Exopolymer Degradation in the Formation of Microbialites on the Atoll of Kiritimati, Republic of Kiribati, Central Pacific. Geomicrobiology Journal 29: 29-65.
20. Bühring SI, Smittenberg RH, Sachse D, Lipp JS, Golubic S, et al. (2009) A hypersaline microbial mat from the Pacific Atoll Kiritimati: insights into composition and carbon fixation using biomarker analyses and a 13C-labeling approach. Geobiology 7: 308-323.
21. Trichet J, Défarge C, Tribble J, Tribble GW, Sansone FJ, (2001) Christmas Island lagoonal lakes, models for the deposition of carbonate-evaporite-organic laminated sediments. Sedimentary Geology 140: 177-189.
22. Blumenberg M, Arp G, Reitner J, Schneider D, Daniel R, et al. (2013) Bacteriohopanepolyols in a stratified cyanobacterial mat from Kiritimati (Christmas Island, Kiribati). Organic Geochemistry 55: 55-62.
23. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P, (2008) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6: 245-252.
24. Woodroffe CD, McLean RF, (1998) Pleistocene morphology and Holocene emergence of Christmas (Kiritimati) Island, Pacific Ocean. Coral Reefs 17: 235-248.
25. Saenger C, Miller M, Smittenberg RH, Sachs JP, (2006) A physico-chemical survey of inland lakes and saline ponds: Christmas Island (Kiritimati) and Washington (Teraina) Islands, Republic of Kiribati. Saline Systems 2: 8.
26. Liu Z, Lozupone C, Hamady M, Bushman FD, Knight R, (2007) Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res 35: e120.
27. Wang Y, Qian PY, (2009) Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS One 4: e7401.
28. Gantner S, Andersson AF, Alonso-Saez L, Bertilsson S, (2011) Novel primers for 16S rRNA-based archaeal community analyses in environmental samples. J Microbiol Methods 84: 12-18.
29. Teske A, Sorensen KB, (2008) Uncultured archaea in deep marine subsurface sediments: have we caught them all? Isme J 2: 3-18.
30. Walters WA, Caporaso JG, Lauber CL, Berg-Lyons D, Fierer N, et al. (2011) PrimerProspector: de novo design and taxonomic analysis of barcoded polymerase chain reaction primers. Bioinformatics 27: 1159-1161.
31. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
32. Reeder J, Knight R, (2010) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 7: 668-669.
33. Martin M, (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal 17: 10-12.
34. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R, (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
35. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, et al. (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72: 5069-5072.
36. Edgar RC, (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
37. Schloss PD, Handelsman J, (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71: 1501-1506.
38. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
39. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, et al. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
40. Parkhurst DL, Appelo CAJ (1999) User's guide to PHREEQC, Version 2: a computer program for speciation, batch-reaction, one-dimensional transport, and inverse geochemical calculations. Denver, Colo.: U.S. Geological Survey: Earth Science Information Center, Open-File Reports Section. 312.
41. Breitbart M, Hoare A, Nitti A, Siefert J, Haynes M, et al. (2009) Metagenomic and stable isotopic analyses of modern freshwater microbialites in Cuatro Cienegas, Mexico. Environ Microbiol 11: 16-34.
42. Kunin V, Raes J, Harris JK, Spear JR, Walker JJ, et al. (2008) Millimeter-scale genetic gradients and community-level molecular convergence in a hypersaline microbial mat. Mol Syst Biol 4: 198.
43. Papineau D, Walker JJ, Mojzsis SJ, Pace NR, (2005) Composition and structure of microbial communities from stromatolites of Hamelin Pool in Shark Bay, Western Australia. Appl Environ Microbiol 71: 4822-4832.
44. Spear JR, Ley RE, Berger AB, Pace NR, (2003) Complexity in natural microbial ecosystems: the Guerrero Negro experience. Biol Bull 204: 168-173.
45. 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.
46. Garcia-Pichel F, Nubel U, Muyzer G, (1998) The phylogeny of unicellular, extremely halotolerant cyanobacteria. Arch Microbiol 169: 469-482.
47. Bebout BM, Carpenter SP, Des Marais DJ, Discipulo M, Embaye T, et al. (2002) Long-term manipulations of intact microbial mat communities in a greenhouse collaboratory: simulating earth's present and past field environments. Astrobiology 2: 383-402.
48. Sahl JW, Pace NR, Spear JR, (2008) Comparative molecular analysis of endoevaporitic microbial communities. Appl Environ Microbiol 74: 6444-6446.
49. Garrity GM, Brenner DJ, Krieg NR, Staley JT (2005) Part C The Alpha-, Beta-, Delta-, and Epsilonproteobacteria; GarrityGM, New York: Springer. 1388.
50. Anton J, Pena A, Santos F, Martinez-Garcia M, Schmitt-Kopplin P, et al. (2008) Distribution, abundance and diversity of the extremely halophilic bacterium Salinibacter ruber. Saline Systems 4: 15.
51. Mongodin EF, Nelson KE, Daugherty S, Deboy RT, Wister J, 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.
52. Atanasova NS, Roine E, Oren A, Bamford DH, Oksanen HM, (2012) Global network of specific virus-host interactions in hypersaline environments. Environ Microbiol 14: 426-440.
53. Hirsch P, Hoffmann B, (1989) Dichotomicrobium thermohalophilum, gen. nov., spec, nov., Budding Prosthecate Bacteria from the Solar Lake (Sinai) and Some Related Strains. Systematic and Applied Microbiology 11: 291-301.
54. Yamada T, Sekiguchi Y, Hanada S, Imachi H, Ohashi A, et al. (2006) Anaerolinea thermolimosa sp. nov., Levilinea saccharolytica gen. nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov. and Caldilineae classis nov. in the bacterial phylum Chloroflexi. Int J Syst Evol Microbiol 56: 1331-1340.
55. Baumgartner LK, Reid RP, Dupraz C, Decho AW, Buckley DH, et al. (2006) Sulfate reducing bacteria in microbial mats: Changing paradigms, new discoveries. Sedimentary Geology 185: 131-145.
56. Krekeler D, Cypionka H, (1995) The preferred electron acceptor of Desulfovibrio desulfuricans CSN. FEMS Microbiol Ecol 17: 271-277.
57. Krekeler D, Sigalevich P, Teske A, Cypionka H, Cohen Y, (1997) A sulfate-reducing bacterium from the oxic layer of a microbial mat from Solar Lake (Sinai), Desulfovibrio oxyclinae sp. nov. Arch Microbiol 167: 369-375.
58. Isenbarger TA, Finney M, Rios-Velazquez C, Handelsman J, Ruvkun G, (2008) Miniprimer PCR, a new lens for viewing the microbial world. Appl Environ Microbiol 74: 840-849.
59. Jakobsen TF, Kjeldsen KU, Ingvorsen K, (2006) Desulfohalobium utahense sp. nov., a moderately halophilic, sulfate-reducing bacterium isolated from Great Salt Lake. Int J Syst Evol Microbiol 56: 2063-2069.
60. Garrity GM, Brenner DJ, Krieg NR, Staley JT (2005) Part B The Gammaproteobacteria; GarrityGM, New York: Springer. 1006.
61. Sun H, Spring S, Lapidus A, Davenport K, Del Rio TG, et al. (2010) Complete genome sequence of Desulfarculus baarsii type strain (2st14). Stand Genomic Sci 3: 276-284.
62. Daffonchio D, Borin S, Brusa T, Brusetti L, van der Wielen PW, et al. (2006) Stratified prokaryote network in the oxic-anoxic transition of a deep-sea halocline. Nature 440: 203-207.
63. Alfreider A, Vogt C, Babel W, (2002) Microbial diversity in an in situ reactor system treating monochlorobenzene contaminated groundwater as revealed by 16S ribosomal DNA analysis. Systematic and Applied Microbiology 25: 232-240.
64. Hugenholtz P, Pitulle C, Hershberger KL, Pace NR, (1998) Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180: 366-376.
65. Pynaert K, Smets BF, Wyffels S, Beheydt D, Siciliano SD, et al. (2003) Characterization of an autotrophic nitrogen-removing biofilm from a highly loaded lab-scale rotating biological contactor. Appl Environ Microbiol 69: 3626-3635.
66. Elevi Bardavid R, Oren A, (2012) The amino acid composition of proteins from anaerobic halophilic bacteria of the order Halanaerobiales. Extremophiles 16: 567-572.
67. Miroshnichenko ML, Kostrikina NA, Chernyh NA, Pimenov NV, Tourova TP, et al. (2003) Caldithrix abyssi gen. nov., sp. nov., a nitrate-reducing, thermophilic, anaerobic bacterium isolated from a Mid-Atlantic Ridge hydrothermal vent, represents a novel bacterial lineage. Int J Syst Evol Microbiol 53: 323-329.
68. Miroshnichenko ML, Kolganova TV, Spring S, Chernyh N, Bonch-Osmolovskaya EA, (2010) Caldithrix palaeochoryensis sp. nov., a thermophilic, anaerobic, chemo-organotrophic bacterium from a geothermally heated sediment, and emended description of the genus Caldithrix. Int J Syst Evol Microbiol 60: 2120-2123.
69. Garrity GM, Brenner DJ, Krieg NR, Staley JT (2001) The Archaea and the Deeply Branching and Phototrophic Bacteria; GarrityGM, New York: Springer. 721.
70. Takai K, Horikoshi K, (1999) Genetic diversity of archaea in deep-sea hydrothermal vent environments. Genetics 152: 1285-1297.
71. Vetriani C, Jannasch HW, MacGregor BJ, Stahl DA, Reysenbach AL, (1999) Population structure and phylogenetic characterization of marine benthic Archaea in deep-sea sediments. Appl Environ Microbiol 65: 4375-4384.
72. Stoeck T, Epstein S, (2003) Novel eukaryotic lineages inferred from small-subunit rRNA analyses of oxygen-depleted marine environments. Appl Environ Microbiol 69: 2657-2663.
73. Ferrer M, Guazzaroni ME, Richter M, Garcia-Salamanca A, Yarza P, et al. (2011) Taxonomic and functional metagenomic profiling of the microbial community in the anoxic sediment of a sub-saline shallow lake (Laguna de Carrizo, Central Spain). Microb Ecol 62: 824-837.
74. Lloyd KG, Schreiber L, Petersen DG, Kjeldsen KU, Lever MA, et al. (2013) Predominant archaea in marine sediments degrade detrital proteins. Nature 496: 215-218.
75. Knittel K, Lösekann T, Boetius A, Kort R, Amann R, (2005) Diversity and Distribution of Methanotrophic Archaea at Cold Seeps. Appl Environ Microbiol 71: 467-479.
76. Turova TP, Kolganova TV, Kuznetsov BB, Pimenov NV, (2002) Phylogenetic diversity of the archaeal component in microbial mats on coral-like structures associated with methane seeps in the Black Sea. Mikrobiologiia 71: 230-236.
77. DeLong EF, Pace NR, (2001) Environmental diversity of bacteria and archaea. Syst Biol 50: 470-478.
78. Kempe S, Kazmierczak J (1990) Calcium carbonate supersaturation and the formation of in situ calcified stromatolites. In: Ittekkot VA, Kempe S, Michaelis W, Spitzy A, editors. Facets of Modern Biogeochemistry. New York: Springer. 255-278.
79. Trichet J, Défarge C (1995) Non-biologically supported organomineralization. Monaco: l′Institut Océanographique de Monaco. 203-236.
80. Arp G, Wedemeyer N, Reitner J, (2001) Fluvival tufa formation in a hard-water creek (Deinschwanger Bach, Franconian Alb, Germany). Facies 44: 1-22.
81. Arp G, Reimer A, Reitner J, (2003) Microbialite formation in seawater of increased alkalinity, Satonda Crater Lake, Indonesia. Society for Sedimentary Geology 73: 105-127.
82. Dupraz C, Visscher PT, (2005) Microbial lithification in marine stromatolites and hypersaline mats. Trends Microbiol 13: 429-438.
83. Cohen Y, Castenholz RW, Halvorson HO (1984) Microbial Mats: Stromatolites. Canada: John Wiley & Sons. 498.
84. Pester M, Schleper C, Wagner M, (2011) The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr Opin Microbiol 14: 300-306.