Fossilization of acidophilic microorganisms

Geomicrobiology Journal

Volumn 27, Issue 8, 2010, Pages 692-706

  Souza Egipsy, Virginia ^a   Aguilera, Angeles ^a   Mateo Martí, Eva ^a   Martín Gago, José Angel ^a,b   Amils, Ricardo ^a,c  

^a CENTRO DE ASTROBIOLOGÍA CSIC INTA   (Spain)

^b INSTITUTO DE CIENCIA DE MATERIALES DE MADRID   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Aquatic sediments; Biofilm; Biomineralization

Indexed keywords

ACIDOPHILY; ALGA; BIOFILM; BIOMINERALIZATION; ENCRUSTATION; FOSSILIZATION; FUNGUS; MICROORGANISM; SCHWERTMANNITE;

ANDALUCIA; HUELVA [ANDALUCIA]; RIO TINTO [(RVR) HUELVA]; SPAIN;

ALGAE; BACTERIA (MICROORGANISMS); FUNGI;

EID: 77957932551     PISSN: 01490451     EISSN: 15210529     Source Type: Journal    
DOI: 10.1080/01490450903564096     Document Type: Article

References (80)

1. Aguilera A, Gómez F, Lospitao E, Amils R. 2006a. A molecular approach to the caracterization of the eukaryotic communities of an extreme acidic environment: methods for DNA extraction and denaturing gradient gel elec-trophoresis analysis. System Appl Microbiol 29:593-605.
2. Aguilera A, Manrubia SC, Gómez F, Amils R. 2006b. Eukaryotic community distribution and its relationship to water physicochemical parameters in an extreme acidic environment, Río Tinto (Southwestern Spain). Appl Environ Microbiol 72:5325-5330.
3. Aguilera A, Souza-Egipsy V, Gómez F, Amils R. 2007a. Development and structure of eukaryotic biofilms in an extreme acidic environment, Rio Tinto (SW, Spain). Microb Ecol 53:294-305.
4. Aguilera A, Zettler E, Góómez F, Amaral-Zettler L, Rodríguez N, Amils R. 2007b. Distribution and seasonal variability in the benthic eukaryotic community of Rio Tinto (SW, Spain), an acidic, high metal extreme environment. System Appl Microbiol 30:531-546.
5. Amaral-Zettler L, Gómez F, Zettler E, Keenan BG, Amils R, Sogin ML. 2002. Eukaryotic diversity in Spain's River of Fire. Nature 417:137.
6. Asada R, Tazaki K. 2001. Silica biomineralization of unicellular microbes under strongly acidic conditions. Can Mineral 39:1-16.
7. Ascaso C, Wierzchos J. 1994. Structural aspects of the lichen-rock interface using back-scattered electron imaging. Botan Acta 107:251-256.
8. Beveridge TJ, Fyfe WS. 1985. Metal fixation by bacterial cell walls. Can J Earth Sci 22:1893-1898.
9. Bigham JM, Schwertmann U, Carlson L, Murad E. 1990. A poorly crystallized oxyhydroxysulfate of iron formed by bacterial oxidation of Fe(II) in acid mine waters. Geochim Cosmochim Acta 54:7741-7758.
10. Bigham JM, Carlson L, Murad E 1994. Schwertmannite, a new iron oxyhy-droxysulphate from Pyhasalmi, Finland, and other localities. Mineral Mag 58:641-648.
11. Brake SS, Dannelly HK, Connors KA. 2001a. Controls on the nature and distribution of an alga in coal mine-waste environments and its potential impact on water quality. Environ Geol 40:458-469.
12. Brake SS, Dannelly HK, Connors KA, Hasiotis ST. 2001b. Influence of water chemistry on the distribution of an acidophilic protozoan in an acid mine drainage system at the abandoned Green Valley coal mine, Indiana, USA. Appl Geochem 16:1641-1652.
13. Brake SS, Hasiotis ST, Dannelly HK, Connors KA. 2002. Eukaryotic stromatolite builders in acid mine drainage: implications for Precambrian iron formations and oxygenation of the atmosphere? Geology 30:599-602.
14. Brake SS, Hasiotis ST, Dannelly HK. 2004. Diatoms in acid mine drainage and their role in the formation of iron-rich stromatolites. Geomicrobiol J 21:331-340.
15. Cady SL, Farmer JD. 1996. Fossilization processes in siliceous thermal springs: trends in preservation along thermal gradients. In: Evolution of hydrothermal ecosystems on earth (and Mars?) (eds. Bock GR, Goode JA) John Wiley and Sons, New York. P. 150-173.
16. Clark BC, Morris RV, McLennan SM, Gellert R, Jolliff BL, Knoll AH, Squyres SW, Lowenstein TK, Ming DW, Tosca NJ, Yen A, Christensen PR, Gorevan S, Brückner J, Calvin W, Dreibus G, Farrand W, Klingelhöfer G, Waenke H, Zipfel J, Bell III JF, Grotzinger JP, McSween HY, Rieder R. 2005. Chemistry and mineralogy of outcrops at Meridiani Planum. Earth Planet Sci Lett 240:73-94.
17. Cornell RM, Schwertmann U. 1996. The Iron Oxides: Structure, Properties, Reactions, Occurrence and Uses. VCH, Weinheim, Germany.
18. Descotes M, Mercier F, Thromat N, Beaucaire C, Gautier-Soyer M. 2000. Use of XPS in the determination of chemical environment of iron and sulfur samples: constitution of a data basis in binding energies for Fe and S reference compounds and applications to the evidence of surface species of an oxidized pyrite in a carbonate medium. Appl Surf Sci 165:288-302.
19. Dupraz C, Visscher PT. 2005. Microbial lithification in marine stromatolite and hypersaline mats. Trends Microbiol 13;429-438.
20. Dzombak DA, Morel FMM. 1990. Surface complexation modelling: hydrous ferric oxides. New York: John Wiley. 416 p.
21. Ehrlich HL. 1996. How microbes influence mineral growth and dissolution. Chemical Geology 132:5-9.
22. Fernández-Remolar D, Gómez-Elvira J, Gómez F, Sebastian E, Martín J, Manfredi JA, Torres J, González Kesler C, Amils R. 2004. The Tinto River, an extreme acidic environment under control of iron, as an analog of the Terra Meridiani hematite site of Mars. Planet Space Sci 52:239-248.
23. Fernández-Remolar DC, Knoll, AH. 2008. Fossilization potential of iron-bearing minerals in acidic environments of Rio Tinto, Spain: Implications for Mars exploration. Icarus 194:72-85.
24. Fernández-Remolar D, Morris RV, Gruener JE, Amils R, Knoll AH. 2005. The Rio Tinto Basin, Spain: mineralogy, sedimentary geobiology, and implications for interpretation of outcrop rocks at Meridiani Planum. Earth Planet Sci Lett 240:149-167.
25. Fernández-Remolar D, Rodríguez N, Gómez F, Amils R. 2003. Geological record of an acidic environment driven by iron hydrochemistry: The Tinto River system. J Geophys Res 108: doi: 10.1029/2002JE001918.
26. Ferris FG, Beveridge TJ, Fyfe WS. 1986. Iron-silica crystalline nucleation by bacteria in a geothermal sediment. Nature 320:609-611.
27. Ferris FG, Fyfe WS, Beveridge TJ. 1987. Bacteria as nucleation sites for authigenic minerals in a metal-contaminated lake sediment. Chem Geol 63:225-232.
28. Ferris FG, Fyfe WS, Beveridge TJ. 1988. Metallic ion binding by Bacillus subtilis: implications for the fossilization of microorganisms. Geology 16:149-152.
29. Ferris FG, Hallbeck L, Kennedy CB, Pedersen K. 2004. Geochemistry of acidic Rio Tinto headwaters and role of bacteria in solid phase metal partitioning. Chem Geol 212:291-300.
30. Ferris FG, Schultze S, Witten TC, Fyfe WS, Beveridge TJ. 1989a. Metal interactions with microbial biofilms in acidic and neutral pH environments. Appl Environ Microbiol 55:1249-1257.
31. Ferris FG, Tazaki K, Fyfe WS. 1989b. Iron-oxides in acid-mine drainage environments and their association with bacteria. Chem Geol 74:321-330.
32. Fortin D, Ferris FG, Beveridge TJ. 1997. Surface mediated mineral development by bacteria. In: Banfield JF, Nealson KH, editors. Geomicrobiology: interactions between microbes and minerals. Reviews in Mineralogy 35. Min-eralogical Society of America, Washington, DC. P. 161-180.
33. Foulke BW, Bonheyo GT, Sanzenbacher B, Frías-López J. 2003. Partitioning of bacterial communities between travertine depositional facies at Mammoth Hot Springs, Yellowstone National Park, USA. Can J Earth Sci 40: 1531-1548.
34. Freytet P, Verrecchia EP. 1998. Freshwater organisms that build stromatolites: a synopsis of biocrystallization by prokaryotic and eukaryotic algae. Sedi-mentology 45:535-563.
35. González-Toril E, Llobet-Brossa E, Casamayor EO, Amann R, Amils R. 2003. Microbial ecology of an extreme acidic environment, The Tinto River. Appl Environ Microbiol 69:4853-4865.
36. Grotzinger JP, Arvidson RE, Bell III JF, Calvin W, Clark BC, Fike DA, Golombek M, Greeley R, Haldemann A, Herkenhoff KE, Jolliff BL, Knoll AH, Malin M, McLennan SM, Parker T, Soderblom LA, Sohl-Dickstein JN, Squyres SW, Tosca NJ, Watters WA. 2005. Stratigraphy and sedimentol-ogy of a dry to wet eolian depositional system, Burns formation, Meridiani Planum. Mars. Earth Planet Sci Lett 240:11-72.
37. Hagadorn J, Bottjer D. 1997. Wrinkle structures: Microbially mediated sedimentary structures common in subtidal siliciclastic settings at the Proterozoic-Phanerozoic transition. Geology 25:1047-1050.
38. Hofmann BA, Farmer JD. 2000 Filamentous fabrics in low-temperature mineral assemblages: are they fossil biomarkers? Implications for the search for a subsurface fossil record on the early Earth and Mars. Planet Space Sci 48:1077-1086.
39. Jones B, Renaut RW. 2007. Selective mineralization of microbes in Fe-rich precipitates (jarosite, hydrous ferric oxides) from acid hot springs in the Waiotapu geothermal area, North Island, New Zealand. Sediment Geol 194:77-98.
40. Kawano M, Tomita K. 2001. Geochemical modeling of bacterially induced mineralization of schwertmannite and jarosite in sulfuric acid spring water. Amer Mineral 86:1156-1165.
41. Kennedy CB, Martinez RE, Scott SD, Ferris FG. 2003. Surface chemistry and reactivity of bacteriogenic iron oxides from Axial Volcano, Juan de Fuca Ridge, north-east Pacific Ocean. Geobiology 1:59-69.
42. Knoll AH, Carr M, Clark B, Des Marais D, Farmer JD, Fischer WW, Grotzinger JP, McLennan SM, Malin MC, Schröder C, Squyres SW, Tosca NJ, Wdowiak T. 2005. An astrobiological perspective on Meridiani Planum. Earth Planet Sci Lett 240:179-189.
43. Konhauser KO. 1998. Diversity of bacterial iron mineralization. Earth Sci Rev 43:91-121.
44. 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.
45. Konhauser KO, Phoenix VR, Bottrell SH, Adams DG, Head IM. 2001. Microbial-silica interactions in Icelandic hot spring sinter: possible analogues for some Precambrian siliceous stromatolites. Sedimentology 48: 415-433.
46. Lazaroff N, Melanson L, Lewis E, Santoro N, Pueschel C. 1985. Scanning electron microscopy and infrared spectroscopy of iron sediments formed by Thiobacillus ferrooxidans. Geomicrobiol J 4:23-268.
47. Léveillé RJ, Fyfe WS, Longstaffe FJ. 2002. Unusual secondary Ca-Mg-Carbonate-Kerolite deposits in basaltic caves, Kauai, Hawaii. J Geol 108:613-621.
48. Little BJ, Wagner P, Lewandowski Z. 1997. Spatial relations between bacteria and mineral surfaces. In: Banfield JF, Nealson KH, editors. Geomicrobiol-ogy; interactions between microbes and minerals. Reviews in Mineralogy 35. Mineralogical Society of America, Washington, DC. P. 123-159.
49. López-Archilla AI, González A, Terrón M, Amils R. 2004. Ecological study of the fungal populations of the acidic Tinto River in southwestern Spain. Can J Microbiol 50:923-934.
50. López-Archilla AI, Marín I, Amils R. 2001. Microbial community composition and ecology of an acidic aquatic environment: The Tinto River, Spain. Microb Ecol 41:20-35.
51. López-Archilla AI, Marín I, González A, Amils R. 1995. Identification of fungi from an acidic river, In: Rossen L, Rubio V, Dawson MT, Frisvad J, editors. Fungal Identification Techniques-European Commission, Luxemburg. P. 202-211.
52. MacIntyre IG, Prufert-Bebout L, Reid RP. 2000. The role of endolithic cyanobacteria in the formation of lithified laminae in Bahamian stromatolites. Sedimentology 47:915-921.
53. Mann H, Fyfe WS. 1985. Alga uptake of U and some other metals: implications for global geochemical cycling. Precambr Res 30:337-349.
54. Mann H, Tazaki K, Fyfe WS, Beveridge TJ, Humphrey R. 1987. Cellular lepi-docrocite precipitation and heavy-metal sorption in Euglena sp. (unicellular alga): implications for biomineralization. Chem Geol 63:39-43.
55. McLennan SM, Bell III JF, Calvin W, Christensen PR, Clark BC, de Souza PA, Farmer J, Farrand WH, Fike DA, Gellert R, Ghosh A, Glotch TD, Grotzinger JP, Hahn B, Herkenhoff KE, Hurowitz JA, Johnson JR, Johnson SS, Jolliff BL, Klingelhöfer, G, Knoll AH, Learner ZA, Malin MC, McSween Jr HY, Pocock J, Ruff SW, Soderblom LA, Squyres SW, Tosca NJ, Watters WA, Wyatt MB, Yen A. 2005. Provenance and diagenesis of the evaporite-bearing Burns formation, Meridiani Planum, Mars. Earth Planet Sci Lett 240: 95-121.
56. Moulder JF, Stickle WF, Sobol PE, Bomben K. 1992. In: Chastain J, King RC, editors. Handbook of X-ray photoelectron spectroscopy. Perkin-Elmer Corporation, Eden Praire, MN.
57. Noffke N, Gerdes G, Klenke T, Krumbein WE. 2001. Microbially induced sedimentary structures- a new category within the classification of primary sedimentary structures. J Sediment Res 71:649-656.
58. Nordstrom DK, Alpers C. 1999. Negative pH, efflorescent mineralogy, and consequences for environmental restoration at the Iron Mountain Superfund site, California. PNAS 96:3455-3462.
59. Norris TB, Castenholz RW. 2006. Endolithic photosynthetic communities within ancient and recent travertine deposits in Yellowstone National Park. FEMS Microbiol Ecol 57:470-483.
60. Phoenix VR, Renaut RW, Jones B, Ferris FG. 2005. Bacterial S-layer preservation and rare arsenic-antimony-sulphide bioimmobilization in siliceous sediments from Champagne Pool hot-spring, Waiotapu, New Zealand. J Geol Society Lond 162:323-332.
61. Pierson BK, Parenteau MN. 2000. Phototrophs in high iron microbial mats: microstructure of mats in iron-depositing hot springs. FEMS Microbiol Ecol 32:181-196.
62. Prave AR. 2002. Life on land in the Proterozoic: Evidence from the Torridonian rocks of northwest Scotland. Geology 30:811-814.
63. Renaut RW, Jones B. 2000. Microbial precipitates around continental hot springs and Geysers. In: Riding RE, Awramik SM, editors. Microbial Sediments. Springer-Verlag. Berlin Heilderberg. P. 187-195.
64. Riding RE, Awramik SM. 2000. Microbial Sediments. Springer-Verlag, Berlin Heidelberg. 331 p.
65. Sánchez-España J, López Pamo E, Santofimia E, Aduvire O, Reyes J, Barettino D. 2005a. Acid mine drainage in the Iberian Pyrite Belt (Odiel river watershed, Huelva, SW Spain): Geochemistry, mineralogy and environmental implications. Appl Geochem 20:1320-1356.
66. Sánchez-España J, López Pamo E, Santofimia E, Reyes J, Martín Rubí JA. 2005b. The natural attenuation of two acidic effluents in Tharsis and La Zarza-Perrunal mines (Iberian pyrite belt, Spain). Environ Geol 49:253-266.
67. Sánchez-España J, López Pamo E, Santofimia E, Reyes J, Martín Rubi JA. 2006. The removal of dissolved metals by hydroxysulphate precipitates during oxidation and neutralization of acid mine waters, Iberian pyrite belt, Spain. Aquat Geochem 12:269-298.
68. Sánchez-España J, Santofimia Pastor E, López Pamo, E. 2007. Iron terraces in acid mine drainage systems: a discussion about the organic and inorganic factors involved in their formation through observations from the Tintillo acidic river (Riotinto mine, Huelva, Spain). Geosphere 3:33-151.
69. Schultze-Lam S, Ferris FG, Konhauser KO, Wiese RG. 1995. In situ silicifi-cation of an Icelandic hot spring microbial mat implications for microfossil formation. Can J Earth Sci 32:2021-2026.
70. Souza-Egipsy V, Gónzalez-Toril E, Zettler E, Amaral-Zettler L, Amils R, Aguilera A. 2008. Prokaryotic community structure in algal photosynthetic biofilms from extreme acidic streams in Río Tinto (SW, Spain). Inter Micro-biol 11:251-260.
71. Souza-Egipsy V, Wierzchos J, Ascaso C, Nealson KH. 2005. Mg-Silica precipitation in fossilization mechanisms of sand tufa endolithic microbial community, Mono Lake (California). Chem Geol 217:77-87.
72. Squyres SW, Grotzinger JP, Arvidson RE, Bell III JF, Calvin W, Christensen PR, Clark BC, Crisp JA, Farrand WH, Herkenhoff KE, Johnson JR, Klingelhöfer G, Knoll AH, McLennan SM, McSween HYJ, Morris RV, Rice JWJ, Rieder R, Soderblom LA. 2004. In situ evidence for and ancient aqueous environment at Meridiani Planum, Mars. Science 306:1709-1714.
73. Squyres SW, Knoll AH. 2005. Sedimentary rocks at Meridiani Planum: origin, diagenesis, and implications for life on Mars. Earth Planet Sci Lett 240:1-10.
74. Squyres SW, Knoll AH, Arvidson RE, Clark BC, Grotzinger JP, Jolliff BL, McLennan SM, Tosca NJ, Bell III JF, Calvin WM, Farrand WH, Glotch TD, Golombek MP, Herkenhoff KE, Johnson JR, Klingelhöfer G, McSween HY, Yen AS. 2006. Two years at Meridiani Planum: results from the Opportunity Rover. Science 313:1403-1407.
75. Sumner DY. 2004. Poor preservation potential of organics in Meridiani Planum hematite bearing sedimentary rocks. J GeophysRes 109 (E12007):1-8. doi:10.1029/2004JE002321
76. Tosca NJ, McLennan SM, Clark BC, Grotzinger JP, Hurowitz JA, Knoll AH, Schröder C, Squyres SW. 2005. Geochemical modelling of evaporation processes on Mars: insight from the sedimentary record at Meridianum Planum. Earth Planet Sci Lett 240:122-148.
77. Vasconcelos C, Warthmann R, McKenzie JA, Visscher PT, Bittermann AG, van Lith Y. 2006. Lithifying microbial mats in Lagoa Vermelha, Brazil: Modern Precambrian relics? Sediment Geol 185:175-183.
78. Walker JL, Spear JR, Pace NR. 2005. Geobiology of a microbial endolithic community in the Yellowstone geothermal environment. Nature 434:1011-1014.
79. Warren LA, Ferris FG. 1998. Continuum between sorption and precipitation of Fe(III) on microbial surfaces. Environ Sci Technol 32:2331-2337.
80. Wierzchos J, Ascaso C. 1994. Application of back-scattered electron imaging to the study of the lichen-rock interface. J Microsc 175:54-59.