Dunaliellacells in fluid inclusions in halite: Significance for long-term survival of prokaryotes

Geomicrobiology Journal

Volumn 27, Issue 1, 2010, Pages 61-75

  Schubert, Brian A ^a   Timofeeff, Michael N ^a   Lowenstein, Tim K ^a   Polle, Jürgen E W ^b  

^a BINGHAMTON UNIVERSITY   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

carotene; Death valley; Dunaliella; Fluid inclusions; Glycerol; Halite; Saline valley; Survival

Indexed keywords

FLUID INCLUSION; GREEN ALGA; HALITE; PROKARYOTE; SURVIVAL;

CALIFORNIA; DEATH VALLEY; UNITED STATES;

ALGAE; ARCHAEA; DUNALIELLA; PROKARYOTA;

EID: 74549157676     PISSN: 01490451     EISSN: 15210529     Source Type: Journal    
DOI: 10.1080/01490450903232207     Document Type: Article

References (80)

1. Aasen AJ, Eimhjellen KE, Liaaen-Jensen S. 1969. An extreme source of β-carotene. Acta Chem Scand 23:2544-2545.
2. Adamski JC, Roberts JA, Goldstein RH. 2006. Entrapment of bacteria in fluid inclusions in laboratory-grown halite. Astrobiology 6:552-562.
3. Amy PS, Durham C, Hall D, Haldeman DL. 1993. Starvation-survival of deep subsurface isolates. Curr Microbiol 26:345-352.
4. Amy PS, Morita RY. 1983. Starvation-survival patterns of sixteen freshly isolated open-ocean bacteria. Appl Environ Microbiol 45:1109-1115.
5. Avron M. 1992. Osmoregulation, in Ben-Amotz A, Avron M, editors. Dunaliella: Physiology, Biochemistry, Biotechnology. Boca Raton, FL: CRC Press. P 135-164.
6. Bass CJ, Davey RA, Lappin-Scott HM. 1998. Long-term starvation survival of a thermophilic sulfidogen consortium. Geomicrobiol J 15:29-36.
7. Ben-Amotz A. 1996. Effect of low temperature on the stereoisomer composition of β-carotene in the halotolerant alga Dunaliella bardawil (Chlorophyta). J Phycol 32:272-275.
8. Ben-Amotz A. 1999. Dunaliella β-carotene: from science to commerce. In Seckbach J, editor. Enigmatic Microorganisms and Life in Extreme Environments. Dordrecht: Kluwer Academic Publishers. P 401-410.
9. Ben-Amotz A, Avron M. 1982. The potential use of Dunaliella for the production of glycerol, β-carotene and high-protein feed. In San Pietro A, editor. Biosaline Research: A Look to the Future. New York: Plenum Publishing Group. P 207-214.
10. Ben-Amotz A, Katz A, Avron M. 1982. Accumulation of β-carotene in halotolerant algae: Purification and characterization of β carotene-rich globules from Dunaliella bardawil (Chlorophyceae). J Phycol 18:529-537.
11. Ben-Amotz A, Shaish A, Avron M. 1989. Mode of action of the massively accumulated β-carotene of Dunaliella bardawil in protecting the alga against damage by excess irradiation. Plant Physiol 91:1040-1043.
12. B́erub́e KA, Dodge JD, Ford TW. 1999. Effects of chronic salt stress on the ultrastructure of Dunaliella bioculata (Chlorophyta, Volvocales): mechanisms of response and recovery. Euro J Phycol 34:117-123.
13. Borowitzka LJ. 1981. The microflora: Adaptations to life in extremely saline lakes. Hydrobiologia 81:33-46.
14. Borowitzka LJ, Borowitzka MA. 1989. β-carotene (provitamin A) production with algae. In Vandamme EJ, editor. Biotechnology of Vitamins, Pigments, and Growth Factors. New York: Elsevier Applied Science. P 15-26.
15. Borowitzka MA, Borowitzka LJ. 1988. Dunaliella in Borowitzka MA, Borowitzka LJ, editors. Micro-algal Biotechnology. Cambridge: Cambridge University Press. P 27-58.
16. Borowitzka MA, Huisman JM. 1993. The ecology of Dunaliella salina (Chlorophyceae, Volvocales): Effect of environmental conditions on aplanospore formation. Botanica Marina 36:233-243.
17. Borowitzka MA, Siva CJ. 2007. The taxonomy of the genus Dunaliella (Chlorophyta, Dunaliellales) with emphasis on the marine and halophilic species. J Appl Phycol 19:567-590.
18. Chapman D, Cherry RJ, Morrison A. 1967. Spectroscopic and electrical studies of all-trans β-carotene crystals. Proc Roy Soc Lond Ser A, Math Phys Sci 301:173-193.
19. Craft NE, Soares JH. 1992. Relative solubility, stability, and absorptivity of lutein and β-carotene in organic solvents. J Agri Food Chem 40:431-434.
20. Dana ES, Ford WE. 1922. A Text-book of Mineralogy: With an Extended Treatise on Crystallography and Physical Mineralogy. New York: JohnWiley & Sons, Inc.
21. Del Campo JA, Garćia-Gonźalez M, Guerrero MG. 2007. Outdoor cultivation of microalgae for carotenoid production: current state and perspectives. Appl Microbiol Biotechnol 74:1163-1174.
22. Dombrowski H. 1963. Bacteria from Paleozoic salt deposits. Ann NY Acad Sci 108:453-460.
23. Elevi Bardavid R, Khristo P, Oren A. 2008. Interrelationships between Dunaliella and halophilic prokaryotes in saltern crystallizer ponds. Extremophiles 12:5-14.
24. Falb M, M̈uller K, K̈onigsmaier L, Oberwinkler T, Horn P, von Gronau S, Gonzalez O, Pfeiffer F, Bornberg-Bauer E, Oesterhelt D.2008. Metabolism f halophilic archaea. Extremophiles 12:177-196.
25. Fendrihan S, Legat A, Pfaffenhuemer M, Gruber C, Weidler G, Gerbl F, Stan-Lotter H. 2006. Extremely halophilic archaea and the ssue of long-term icrobial survival. Rev Environ Sci Biotechnol 5:203-218.
26. Fendrihan S, Stan-Lotter H. 2004. Survival of halobacteria in fluid inclusions as a model of possible biotic survival in Martian halite. In Teodorescu HN, Griebel HS, editors. Mars and Planetary Science and Technology. Iasi, Romania: Performantica Press. P 9-18.
27. Fredrickson JK, Chandler DP, Onstott TC. 1997. Potential for preservation of halobacteria and their macromolecular constituents in brine inclusions from bedded salt deposits. Proceedings of SPIE (The International Society for Optical Engineers) 3111:318-329.
28. Ginzburg M. 1987. Dunaliella: a green alga adapted to salt. Adv Botan Res 14:93-180.
29. Gochnauer MB, Kushwaha SC, Kates M, Kushner DJ. 1972. Nutritional control of pigment and isoprenoid compound formation in extremely halophilic bacteria. Archiv f̈ur Mikrobiologie 84:339-349.
30. Goldstein RH, Reynolds TJ. 1994. Systematics of Fluid Inclusions in Diagenetic Minerals Tulsa: Society of Economic Paleontologists and Mineralogists. 184 p.
31. Gonźalez-Pastor JE, Hobbs EC, Losick R. 2003. Cannibalism by sporulating bacteria. Science 301:510-513.
32. Grant WD, Gemmell RT, McGenity TJ. 1998. Halobacteria: the evidence for longevity. Extremophiles 2:279-287.
33. Gruber C, Legat A, Pfaffenhuemer M, Radax C, Weidler G, Busse H-J, Stan-Lotter H. 2004. Halobacterium noricense sp. nov., an archaeal isolate from a bore core of an alpine Permian salt deposit, classification of Halobacterium sp. NRC-1 as a strain of H. salinarum and emended description of H. salinarum. Extremophiles 8:431-439.
34. Hamburger, C. 1905. Zur Kenntnis der Dunaliella salina und einer Am̈obe aus Salinenwasser von Cagliari. Archiv f̈ur Protistenkunde 6:111-131.
35. Hardie LA. 1968. The origin of the recent non-marine evaporite deposit of Saline Valley, Inyo County, California. Geochim Cosmochim Acta 32: 1279-1301.
36. Javor BJ. 1984. Growth potential of halophilic bacteria isolated from solar salt environments: Carbon sources and salt requirements. Appl EnvironMicrobiol 48:352-360.
37. Johnson SS, Hebsgaard MB, Christensen TR, Mastepanov M, Nielsen R, Munch K, Brand T, Gilbert MT, Zuber MT, Bunce M, Ronn R, Gilichinsky D, Froese D, Willerslev E. 2007. Ancient bacteria show evidence of DNA repair. Proc Natl Acad Sci USA 104:14401-14405.
38. Kjelleberg S, Hermansson M. 1984. Starvation-induced effects on bacterial surface characteristics. Appl Environ Microbiol 48:497-503.
39. Kjelleberg S, Humphrey BA, Marshall KC. 1983. Initial phases of starvation and activity of bacteria at surfaces. Appl Environ Microbiol 46: 978-984.
40. Ku TL, Luo S, Lowenstein TK, Li J, Spencer RJ. 1998. U-Series chronology of lacustrine deposits in Death Valley, California. Quater Res 50:261-275.
41. Leonardi PI, Ćaceres EJ. 1997. Light and electron microscope observations of the life cycle of Dunaliella salina (Polyblepharidaceae, Chlorophyceae). Nova Hedwigia 64:621-633.
42. Lerche W. Untersuchungen̈uber Entwicklung und Fortpflanzung in derGattung Dunaliella. Archiv f̈ur Protistenkunde 88:236-268.
43. Li J, Lowenstein TK, Brown CB, Ku TL, Luo S. 1996. A 100 ka record of water tables and paleoclimates from salt cores, Death Valley, California. Palaeogeogr Palaeoclimatol Palaeoecol 123:179-203.
44. Loeblich LA. 1969. Aplanospores of Dunaliella salina (Chlorophyta). J Protozool 16:22-23.
45. Loeblich LA. 1982. Photosynthesis and pigments influenced by light intensity and salinity in the halophile Dunaliella salina (Chlorophyta). J Mar BiolAsso UK 62:493-508.
46. Lowenstein T. 2008. Ancient microorganisms in salt. In Weil J, Blumel D, Malmoli S, Netting J, editors. McGraw-Hill Yearbook of Science and Technology. New York: McGraw-Hill. P 13-15.
47. Lowenstein TK, Brennan ST. 2001. Fluid inclusions in paleolimnological studies of chemical sediments. In Last WM, Smol JP, editors. Tracking Environmental Change Using Lake Sediments: Physical and Geochemical Methods (Volume 2). Dordrecht, Netherlands: Kluwer Academic Publishers. P 189-216.
48. Lowenstein TK, Hardie LA. 1985. Criteria for the recognition of salt-pan evaporites. Sedimentology 32:627-644.
49. Lowenstein TK, Li J, Brown C, Roberts SM, Ku T-L, Luo S, Yang W. 1999. 200 k.y. paleoclimate record from Death Valley salt core. Geology 27:3-6.
50. McGenity TJ, Gemmell RT, Grant WD, Stan-Lotter H. 2000. Origins of halophilic microorganisms in ancient salt deposits. Environ Microbiol 2:243-250.
51. Morita RY. 1982. Starvation-survival of heterotrophs in themarine environment. Adv Microb Ecol 6:171-198.
52. Mormile MR, Biesen MA, Gutierrez MC, Ventosa A, Pavlovich JB, Onstott TC, Fredrickson JK. 2003. Isolation of Halobacterium salinarum retrieved directly from halite brine inclusions. Environ Microbiol 5:1094-1102.
53. Moyer CL, Morita RY. 1989. Effect of growth rate and starvation-survival on the viability and stability of a psychrophilic marine bacterium. Appl Environ Microbiol 55:1122-1127.
54. Nandy SK, Bapat PM, Venkatesh KV. 2007. Sporulating bacteria prefers predation to cannibalism in mixed cultures. FEBS Lett 581:151-156.
55. Nesse WD. 2000. Introduction to Mineralogy. New York Oxford University Press.
56. Norton CF, Grant WD. 1988. Survival of halobacteria within fluid inclusions in salt crystals. J Gen Microbiol 134:1365-1373.
57. Norton CF, McGenity TJ, Grant WD. 1993. Archaeal halophiles (halobacteria) from two British salt mines. J Gen Microbiol 139:1077-1081.
58. Novitsky JA, Morita RY. 1976. Morphological characterization of small cells resulting from nutrient starvation of a psychrophilic marine vibrio. Appl Environ Microbiol 32:617-622.
59. Oren A. 1993a. Availability, uptake and turnover of glycerol in hypersaline environments. FEMS Microbiol Ecol 12:15-23.
60. Oren A.1993b. The Dead Sea-alive again. Experientia 49:518-522.
61. Oren A.1995. The role of glycerol in the nutrition of halophilic archaeal communities: a study of respiratory electron transport. FEBS Microbiol Ecol 16:281-289.
62. Oren A. 2005. A hundred years of Dunaliella research: 1905-2005. Saline Systems 1:2.
63. Oren A, Gurevich P, Anati DA, Barkan E, Luz B. 1995. A bloom of Dunaliella parva in the Dead Sea in 1992: biological and biogeochemical aspects. Hydrobiologia 297:173-185.
64. Pick U, Karni L, Avron M. 1986. Determination of ion content and ion fluxes in the halotolerant alga Dunaliella salina. Plant Physiol 81:92-96.
65. Price PB, and Sowers T. 2004. Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc Natl Acad Sci USA 101:4631-4636.
66. Raja R, Hema Iswarya S, Balasubramanyam D, Rengasamy R. 2007. PCRidentification of Dunaliella salina (Volvocales, Chlorophyta) and its growth characteristics. Microbiol Res 162:168-176.
67. Rawal N, Kelkar SM, Altekar W. 1988. Alternative routes of carbohydrate metabolism in halophilic Archaebacteria. Ind J Biochem Biophys 25:674-686.
68. Reiser R, Tasch P. 1960. Investigation of the viability of osmophile bacteria of great geological age. Trans Kansas Acad Sci 63:31-34.
69. Rodriguez-Valera F, Ruiz-Berraquero F, Ramos-Cormenzana A. 1980. Isolation of extremely halophilic bacteria able to grow in defined inorganic media with single carbon sources. J Gen Microbiol 119:535-538.
70. Roedder E. 1984. The fluids in salt. Amer Mineral 69:413-439.
71. Schubert BA, Lowenstein TK, Timofeeff MN. 2009a.Microscopic identification of prokaryotes in modern and ancient halite, Saline Valley and Death Valley, California. Astrobiology 9:467-482.
72. Schubert BA, Lowenstein TK, Timofeeff MN, Parker MA. 2009b. Halophilic Archaea cultured from ancient halite, Death Valley, California. Environ Microbiol.
73. Schubert BA, Lowenstein TK, Timofeeff MN, Parker MA. 2009c. How do prokaryotes survive in fluid inclusions in halite for 30 k.y.? Geology 37:1059-1062.
74. Setlow P. 1995. Mechanisms for the prevention of damage to DNA in spores of Bacillus species. Ann Rev Microbiol 49:29-54.
75. Stan-Lotter H, McGenity TJ, Legat A, Denner EBM, Glaser K, Stetter KO, Wanner G. 1999. Very similar strains of Halococcus salifodinae are found in geographically separated Permo-Triassic salt deposits. Microbiology 145:3565-3574.
76. Stan-Lotter H, Pfaffenhuemer M, Legat A, Busse H-J, Radax C, Gruber C. 2002. Halococcus dombrowskii sp. nov., an archaeal isolate from a Permian alpine salt deposit. Inter J System Evolution Microbiol 52:1807-1814.
77. Vreeland RH, Jones J, Monson A, Rosenzweig WD, Lowenstein TK, Timofeeff M, Satterfield C, Cho BC, Park JS, Wallace A, Grant WD. 2007. Isolation of live Cretaceous (121-112 Million Years Old) halophilic Archaea from primary salt crystals. Geomicrobiol J 24:275-282.
78. Vreeland RH, Rosenzweig WD, Powers DW. 2000. Isolation of a 250 millionyear old halotolerant bacterium from a primary salt crystal. Nature 407:897-900.
79. Whitman WB, Coleman DC, Wiebe WJ. 1998. Prokaryotes: The unseen majority. Proc Natl Acad Sci USA 95:6578-6583.
80. Zscheile FP, White Jr JW. 1940. Microscope hot stage for determination of melting points: application to carotenoid pigments. Indust Eng Chem 12:436-438.