Silicified virus-like nanoparticles in an extreme thermal environment: Implications for the preservation of viruses in the geological record

Geobiology

Volumn 11, Issue 6, 2013, Pages 511-526

  Peng, X ^a,b   Xu, H ^a,b   Jones, B ^c   Chen, S ^a   Zhou, H ^a  

^a Tongji University   (China)

^b Chinese Academy of Sciences   (China)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOFILM; CYANOBACTERIUM; EXOPOLYMER; EXTREMOPHILE; GEOLOGICAL RECORD; GEOMICROBIOLOGY; NANOTECHNOLOGY; PRESERVATION; SILICA; SILICIFICATION; THERMAL SPRING; THERMOPHILIC BACTERIUM; VIRUS;

CHINA; TENGCHONG; YUNNAN;

AQUIFICAE; AQUIFICAE (CLASS); CYANOBACTERIA; DESULFUROCOCCALES; FIRMICUTES; THERMODESULFOBACTERIA; THERMOPROTEALES;

NANOPARTICLE; VIROSOME;

ARCHAEON; ARTICLE; BACTERIUM; BIOFILM; CHINA; MICROBIOLOGY; PRESERVATION; THERMAL SPRING; VIROLOGY;

ARCHAEA; BACTERIA; BIOFILMS; CHINA; ENVIRONMENTAL MICROBIOLOGY; HOT SPRINGS; NANOPARTICLES; PRESERVATION, BIOLOGICAL; VIROSOMES;

EID: 84885871098     PISSN: 14724677     EISSN: 14724669     Source Type: Journal    
DOI: 10.1111/gbi.12052     Document Type: Article

References (91)

1. Ahn DG, Kim SI, Rhee JK, Kim KP, Pan JG, Oh JW (2006) TTSV1, a new virus-like particle isolated from the hyperthermophilic crenarchaeote Thermoproteus tenax. Virology 351, 280-290.
2. Arab H, Völker H, Thomm M (2000) Thermococcus aegaeicus sp. nov. and Staphylothermus hellenicus sp. nov., two novel hyperthermophilic archaea isolated from geothermally heated vents off Palaeochori Bay, Milos, Greece. International Journal of Systematic and Evolutionary Microbiology 50, 2101-2108.
3. Arnold HP, Ziese Zillig W (2000) SNDV, a novel virus of the extremely thermophilic and acidophilic archaeon Sulfolobus. Virology 272, 409-416.
4. Banfield JF, Moreau JW, Chan CS, Welch SA, Little B (2001) Mineralogical biosignatures and the search for life on Mars. Astrobiology 1, 447-465.
5. Bettstetter M, Peng X, Garrett RA, Prangishvili D (2003) AFV1, a novel virus infecting hyperthermophilic archaea of the genus Acidianus. Virology 315, 68-79.
6. Bird DF, Juniper SK, Ricciardi-Rigault M, Martineu P, Prairie YT, Calvert SE (2001) Subsurface viruses and bacteria in Holocene/Late Pleistocene sediments of Saanich Inlet, BC: ODP Holes 1033B and 1034B, Leg 169S. Marine Geology 174, 227-239.
7. Borriss M, Helmke E, Hanschke R, Schweder T (2003) Isolation and characterization of marine psychrophilic phage-host systems from Arctic sea ice. Extremophiles 7, 377-384.
8. Buick R (1990) Microfossil recognition in Archean rocks: an appraisal of spheroids and filaments from a 3500 m.y. old chert-barite unit at North Pole, Western Australia. Palaios 5, 441-459.
9. Cady SL (2001) Paleobiology of the Archean. Advances in Applied Microbiology 50, 1-35.
10. Cady SL, Farmer JD, Grotzinger JP, Schopf JW, Steele A (2003) Morphological biosignatures and the search for life on Mars. Astrobiology 3, 351-368.
11. Chrisostomos S, Patel BKC, Dwivedi PP, Denman S (1996) Caloramator indicus sp. nov., a new thermophilic anaerobic bacterium isolated from the deep-seated non-volcanically heated waters of an Indian Artesian Aquifer. International Journal of Systematic Bacteriology 46, 497-501.
12. Coradin T, Durupthy O, Livage J (2002) Interactions of amino-containing peptides with sodium silicate and colloidal silica: a biomimetic approach of silicification. Langmuir 18, 2331-2336.
13. Du J, Liu C, Fu B, Ninomia Y, Zhang Y, Wang C, Wang H, Sun Z (2005) Variations of geothermometry and chemical-isotope compositions of hot spring fluids in the Rehai geothermal field, southwestern China. Journal of Volcanology and Geothermal Research 142, 243-261.
14. Dyall-Smith M, Tang SL, Bath C (2003) Haloarchaeal viruses: how diverse are they? Research in Microbiology 154, 309-313.
15. Farmer JD, DesMarais DJ (1999) Exploring for a record of ancient Martian life. Journal of Geophysical Research 104, 26977-26995.
16. Ferris FG, Magalhaes E (2008) Interfacial energetics of bacterial silicification. Geomicrobiology Journal 25, 333-337.
17. Ferris FG, Beveridge TJ, Fyfe WS (1986) Iron-silica crystallite nucleation by bacteria in a geothermal sediment. Nature 320, 9-11.
18. Ferris FG, Fyfe WS, Beveridge TJ (1987) Bacteria as nucleation sites for authigenic minerals in a Metal-Contaminated Lake Sediment. Chemical Geology 63, 225-232.
19. Ferris FG, Fyfe WS, Beveridge TJ (1988) Metallic ion binding by Bacillus Subtilis: implications for the fossilization of microorganisms. Geology 16, 149-152.
20. Forterre P, Prangishvili D (2009) The origin of viruses. Research in Microbiology 160, 466-472.
21. Fortin D (2004) What biogenic minerals tell us. Science 303, 1618-1619.
22. Fortin D, Beveridge TJ (1997) Role of the bacterium Thiobacillus in the formation of silicates in acidic mine tailings. Chemical Geology 141, 235-250.
23. Fortin D, Langley S (2005) Formation and occurrence of biogenic iron-rich minerals. Earth-Science Reviews 72, 1-19.
24. Fortin D, Ferris FG, Beveridge TJ (1997) Surface-mediated mineral development by bacteria. Reviews in Mineralogy 35, 161-180.
25. Fowler CE, Shenton W, Stubbs G, Mann S (2001) Tobacco mosaic virus liquid crystals as templates for the interior design of silica mesophases and nanoparticles. Advanced Materials 13, 1266-1269.
26. Geslin C, Le Romancer M, Erauso G, Gaillard M, Perrot G, Prieur D (2003) PAV1, the first virus-like particle isolated from a hyperthermophilic euryarchaeote, 'Pyrococcus abyssi'. Journal of Bacteriology 185, 3888-3894.
27. Happonen LJ, Redder P, Peng X, Reigstad LJ, Prangishvili D, Butcher SJ (2010) Familial relationships in hyperthermo- and acidophilic archaeal viruses. Journal of Virology 84, 4747-4754.
28. Häring M, Peng X, Brugger K, Rachel R, Stetter KO, Garret RA, Prangishvili D (2004) Morphology and genome organization of the virus PSV of the hyperthermophilic archaeal genera Pyrobaculum and Thermoproteus: a novel virus family, the Globuloviridae. Virology 323, 233-242.
29. Häring M, Rachel R, Peng X, Garrett RA, Prangishvili D (2005a) Viral diversity in hot springs of Pozzuoli, Italy, and characterization of a unique archaeal virus, Acidianus bottleshaped virus, from a new family, the Ampullaviridae. Journal of Virology 79, 9904-9911.
30. Häring M, Vestergaard G, Rachel R, Chen L, Garrett RA, Prangishvili D (2005b) Virology: independent virus development outside a host. Nature 436, 1101-1102.
31. Hayat MA (1993) Stains and Cytochemical Methods, Plenum Press, New York, pp. 223-229.
32. Hegde NR, Maddur MS, Kaveri SV, Bayry J (2009) Reasons to include viruses in the tree of life. Nature Reviews Biology 7, 615.
33. Hofmann HJ (2000) Archean stromatolites as microbial archives. In Microbial Sediments (eds Riding RE, Awramik SM). Springer, Berlin, pp. 315-327.
34. House CH, Schopf JW, McKeegan KD, Coath CD, Harrison TM, Stetter KO (2000) Carbon isotopic composition of individual Precambrian microfossils. Geology 28, 707-710.
35. Hsueh HT, Chu H, Chang CC (2007) Identification and characteristics of a Cyanobacterium isolated from a hot spring with dissolved inorganic carbon. Environmental Science & Technology 41, 1909-1914.
36. Jones B, Renaut RW, Rosen MR (1997) Biogenicity of silica precipitation around geysers and hot-spring vents, North Island, New Zealand. Journal of Sedimentary Research 67, 88-104.
37. Jones B, Renaut RW, Rosen MR (2001) Taphonomy of silicified filamentous microbes in modern geothermal sinters-implications for identification. Palaios 16, 580-592.
38. Jones B, Konhauser KO, Renaut RW, Wheeler RS (2004) Microbial silicification in Iodine Pool, Waimangu geothermal area, North Island, New Zealand: implications for recognition and identification of ancient silicified microbes. Journal of the Geological Society [London] 161, 983-993.
39. Konhauser KO (1998) Diversity of bacterial iron mineralization. Earth Science Reviews 43, 92-121.
40. Konhauser KO, Ferris FG (1996) Diversity of iron and silica precipitation by microbial mats in hydrothermal waters, Iceland: implications for Precambrian iron formations. Geology 24, 323-326.
41. Konhauser KO, Jones B, Phoenix VR, Ferris FG, Renaut RW (2004) The microbial role in hot spring silicification. Ambio 33, 552-558.
42. Konhauser KO, Lalonde SV, Phoenix VR (2008) Bacterial biomineralization: where to from here? Geobiology 6, 298-302.
43. Koonin EV, Senkevich TG, Dolja VV (2006) The ancient Virus World and evolution of cells. Biology Direct 1, 29.
44. Kuisiene N, Raugalas J, Chitavichius D (2004) Geobacillus lituanicus sp. nov. International Journal of Systematic and Evolutionary Microbiology 54, 1991-1995.
45. Kyle JE, Eydal HSC, Ferris FG, Pedersen K (2008a) Viruses in granitic groundwater from 69 to 450 m depth of the Äspö hard rock laboratory, Sweden. ISME Journal 2, 571-574.
46. Kyle JE, Pedersen K, Ferris FG (2008b) Virus mineralization at low pH in the Rio Tinto, Spain. Geomicrobiology Journal 25, 338-345.
47. Kyle JE, Jahnke LL, Stedman KM (2012) Preservation potential of lipid-containing viruses under silicifying conditions. 43rd Lunar and Planetary Science Conference. LPI Contribution No. 1659, id. 2228.
48. Laidler JR, Stedman KM (2010) Virus silicification under simulated hot spring conditions. Astrobiology 10, 569-576.
49. Lalonde SV, Konhauser KO, Reysenbach AL, Ferris FG (2005) The experimental silicification of Aquificales and their role in hot spring sinter formation. Geobiology 3, 41-52.
50. Lawrence JG, Hendrix RW, Casjens S (2001) Where are the pseudogenes in bacterial genomes? Trends in Microbiology 9, 535-540.
51. Mochizuki T, Yoshida T, Tanaka R, Forterre P, Sako Y, Prangishvili D (2010) Diversity of viruses of the hyperthermophilic archaeal genus Aeropyrum, and isolation of the Aeropyrum pernix bacilliform virus 1, APBV1, the first representative of the family Clavaviridae. Virology 402, 347-354.
52. Moreira D, López-Garcia P (2009) Ten reasons to exclude viruses from the tree of life. Nature Reviews Biology 7, 306-311.
53. Orange F, Chabin A, Gorlas A, Lucas-Staat S, Geslin C, Le Romancer M, Prangishvili D, Forterre P, Westall F (2011) Experimental fossilisation of viruses from extremophilic Archaea. Biogeosciences 8, 1465-1475.
54. Padan E, Bibi E, Ito M, Krulwich TA (2005) Alkaline pH homeostasis in bacteria: new insights. Biochimica et Biophysica Acta 1717, 67-88.
55. Palm P, Schleper C, Grampp B, Yeats S, McWilliam P, Reiter WD, Zillig W (1991) Complete nucleotide sequence of the virus SSV1 of the archaebacterium Sulfolobus shibatae. Virology 185, 242-250.
56. Parkhurst DL, Appelo CAJ (1999) User's Guide to PHREEQC (version 2) - a Computer Program for Speciation, Reaction-Path, 1D-Transport, and Inverse Geochemical Calculations. United States Geological Survey, Water Resource Investigations Report, Washington, DC, pp. 312.
57. Peng X, Jones B (2012) Rapid precipitation of silica (opal-A) disguises evidence of biogenicity in high-temperature geothermal deposits: case study from Dagunguo hot spring, China. Sedimentary Geology 229, 193-206.
58. Peng X, Chen S, Zhou H, Zhang L, Wu Z, Li J, Li J (2011) Diversity of biogenic minerals in low-temperature Si-rich deposits from a newly discovered hydrothermal field on the ultraslow spreading Southwest Indian Ridge. Journal of Geophysical Research 116, G03030.
59. Phoenix VR, Adams DG, Konhauser KO (2000) Cyanobacterial viability during hydrothermal biomineralization. Chemical Geology 169, 329-338.
60. Prangishvili D, Garrett RA (2005) Viruses of hyperthermophilic Crenarchaea. Trends in Microbiology 13, 535-542.
61. Prangishvili D, Stedman KM, Zillig W (2001) Viruses of the extremely thermophilic archaeon Sulfolobus. Trends in Microbiology 9, 39-43.
62. Prangishvili D, Forterre P, Garrett RA (2006) Viruses of the Archaea: a unifying view. Nature Reviews Microbiology 4, 837-848.
63. Prigent M, Leroy M, Confalonieri F, Dutertre M, DuBow MS (2005) A diversity of bacteriophage forms and genomes can be isolated from the surface sands of the Sahara Desert. Extremophiles 9, 289-296.
64. Renaut RW, Jones B, Tiercelin JJ (1998) Rapid in situ silicification of microbes at Loburu hot springs, Lake Bogoria, Kenya Rift Valley. Sedimentology 45, 1083-1103.
65. Renaut RW, Jones B, Tiercelin JJ, Tarits C (2002) Sublacustrine precipitation of hydrothermal silica in rift lakes: evidence from Lake Baringo, central Kenya Rift Valley. Sedimentary Geology 148, 235-257.
66. Rice G, Stedman KM, Snyder J, Wiedenheft B, Willits D, Brumfield S, McDermott T, Young MJ (2001) Viruses from extreme thermal environments. Proceedings of the National Academy of Sciences of the United States of America 98, 13341-13345.
67. Rice G, Tang L, Stedman K, Roberto F, Spuhler J, Gillitzer E, Johnson JE, Douglas T, Young M (2004) The structure of a thermophilic archaeal virus shows a double-stranded DNA viral capsid type that spans all domains of life. Proceedings of the National Academy of Sciences of the United States of America 101, 7716-7720.
68. Roeselers G, Norris TB, Castenholz RW, Rysgaard S, Glud RN, Kühl M, Muyzer G (2007) Diversity of phototrophic bacteria in microbial mats from Arctic hot springs (Greenland). Environmental Microbiology 9, 26-38.
69. Sakaki Y, Oshima T (1975) Isolation and characterization of a bacteriophage infectious to an extreme thermophile, Thermus thermophilus HB8. Journal of virology 15, 1449-1453.
70. Schopf JW (1993) Microfossils of the early Archean apex chert: new evidence of the antiquity of life. Science 260, 640-646.
71. Schopf JW (2006) Fossil evidence of Archaean life. Philisophical transactions of the royal society B: biological sciences 361, 869-885.
72. Schopf JW, Kudryavtsev AB, Agresti DG, Wdowiak TJ, Czaja AD (2002) Laser Raman imagery of Earth's earliest fossils. Nature 416, 73-76.
73. Schultze-Lam S, Ferris FG, Konhauser KO, Wiese RG (1995) In situ silicification of an Icelandic hot spring microbial mat: implications for microfossil formation. Canadian Journal of Earth Sciences 32, 2021-2026.
74. Slonczewski JL, Fujisawa M, Dopson M, Krulwich TA (2009) Cytoplasmic pH measurement and homeostasis in bacteria and archaea. Advances in Microbial Physiology 55, 1-78.
75. Stedman KM, She Q, Phan H, Arnold HP, Holz I, Garrett RA, Zillig W (2003) Relationships between fusello viruses infecting the extremely thermophilic archaeon Sulfolobus: SSV1 and SSV2. Research in Microbiology 154, 295-302.
76. Stedman KM, Prangishvili D, Zillig W (2005) Viruses of Archaea. In The Bacteriophages, 2nd edn, (ed Calendar R). Oxford University Press, New York, pp. 499-516.
77. Stedman KM, Clore A, Combet-Blanc Y (2006) Biogeographical diversity of archaeal viruses. In SGM Symposium 66: Prokaryotic Diversity: Mechanisms and Significance (eds Logan NA, Pappin-Scott HM, Oynston PCF). Cambridge University Press, Cambridge, pp. 131-144.
78. Walker JJ, Spear JR, Pace NR (2005) Geobiology of a microbial endolithic community in the Yellowstone geothermal environment. Nature 434, 1011-1014.
79. Wallace AF, DeYoreo JJ, Dove PM (2009) Kinetics of silica nucleation on carboxyl- and amine-terminated surfaces: insights for biomineralization. Journal of the American Chemical Society 131, 5244-5250.
80. Walter MR, Buick R, Dunlop JSR (1980) Stromatolites, 3, 400-3, 500 Myr old from the North Pole area, Western Australia. Nature 284, 443-445.
81. Wang T, Chai L, Guo C, Cui X, Xu L (2003) Study on nine 16S rDNA clones came from two hot springs in the west of Yunnan. Microbiology 30, 38-42.
82. Westall F (1999) The nature of fossil bacteria: a guide to the search for extraterrestrial life. Journal of Geophysical Research 104, 16437-16451.
83. Westall F, Boni L, Guerzoni E (1995) The experimental silicification of microorganisms. Palaeontology 38, 495-528.
84. Westall F, de Wit MJ, Dann J, van der Gaast S, de Ronde CEJ, Gerneke D (2001) Early Archean fossil bacteria and biofilms in hydrothermally-influenced sediments from the Barberton greenstone belt, South Africa. Precambrian Research 106, 93-116.
85. Wiegel J (1986) Methods for isolation and study of thermophiles. In Thermophiles: General, Molecular, AND Applied Microbiology (ed Brock TD). John Wiley and Sons, New York, pp. 17-37.
86. Yee N, Phoenix VR, Konhauser KO (2003) The effect of cyanobacteria on silica precipitation at neutral implications for bacterial silicification in geothermal hot. Chemical Geology 199, 83-90.
87. Young M, Wiedenheft B, Snyder J, Spuhler J, Roberto F, Douglas T (2005) Archaeal viruses from Yellowstone's high temperature environments. In Geothermal Biology and Geochemistry in YNP (eds Inskeep WP, McDermott TR). Montana State University Publications, Bozeman, MT, pp. 289-304.
88. Yu MX, Slater MR, Ackermann HW (2006) Isolation and characterization of Thermus bacteriophages. Archives of Virology 151, 663-679.
89. Zhang G, Liu CQ, Liu H, Jin Z, Han G, Li L (2008) Geochemistry of the Rehai and Ruidian geothermal waters, Yunnan Province, China. Geothermics 37, 73-83.
90. Zillig W, Kletzin A, Schleper C, Holz I, Janekovic D, Hain J, Lanzendörfer M, Kristjanson JK (1994) Screening for Sulfolobales, their plasmids and their viruses in Icelandic Solfataras. Systematic Applied Microbiology 16, 609-628.
91. Zillig W, Prangishvilli D, Schleper C, Elferink M, Holz I, Albers S, Janekovic D, Gotz D (1996) Viruses, plasmids and other genetic elements of thermophilic and hyperthermophilic Archaea. FEMS Microbiololgy Reviews 18, 225-236.