Orginal Article

Reviews on Ancient Halophilic Microbes in Halite Fluid in Clusions

  • Jiuyi Wang ,
  • Chenglin Liu
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  • MLR Key Laboratory of Metallogeny and Mineral Assessment, Institute of Mineral Resources,Chinese Academy of Geological Sciences, Beijing 100037,China

First author:Wang Jiuyi(1983-), male, Nanyang City, He’nan Province, Assistant professor. Research areas include evaporites and paleoclimate.E-mail:wjyhlx@163.com

Received date: 2016-08-16

  Revised date: 2016-10-21

  Online published: 2016-12-20

Supported by

Project supported by the National Natural Science Foundation of China “Aridification in Asian interior recorded by lithofacies feature of saline lake sediments in western Qaidam Basin”(No.41302133);the State Key Development Program for Basic Research of China “Mineralization regularity and prediction of potash deposits of marine basins in Chinese microplate”(No.2011CB403007)

Copyright

地球科学进展 编辑部, 2016,

Abstract

Fluid inclusions trapped in ancient evaporites can contain a community of halophilic prokaryotes and eukaryotes that inhabited the surface brines from which the minerals formed. Entombed in the fluid inclusions in evaporites, some of these halophilic microbes remain viable for at least tens of thousands of years and possibly for hundreds of millions of years, even under high salinity, low oxygen, high radiation, low nutrient concentration. This review presents the scientific history of discovery, isolation, and culture of ancient halophilic microbes in halite fluid inclusions. We elucidated the controversy associated with the ancient halophilic microbes between geologists and geomicrobiologists. Major concerns and future perspectives on halophiles research were proposed. We emphasized that lithofacies analysis and depositional environment determination on evaporites are prerequisites before any microbiological survey, and rigorous biological protocol must be obeyed at all retrieval procedures for ancient microorganisms. We suggested that future study related to ancient halophilic microbes should focus on other evaporites such as gypsum, glauberite, and trona, characterize and identify older halophiles; clarify metabolic mechanism for longevity of ancient microorganisms.

Cite this article

Jiuyi Wang , Chenglin Liu . Reviews on Ancient Halophilic Microbes in Halite Fluid in Clusions[J]. Advances in Earth Science, 2016 , 31(12) : 1220 -1227 . DOI: 10.11867/j.issn.1001-8166.2016.12.1220

References

[1] Goldstein R H, Reynolds T J.Systematics of Fluid Inclusions in Diagenetic Minerals. SEPM Short Course 31[M]. Tulsa: SEPM, 1994.
[2] Griffith J D, Willcox S, Powers D W,et al.Discovery of abundant cellulose microfibers encased in 250 Ma Permian halite: A macromolecular target in the search for life on other planets[J]. Astrobiology,2008, 8(2): 215-228.
[3] Stan-Lotter H, McGenity T J, Legat A,et al. Very similar strains of Halococcus salifodinae are found in geographically separated Permo-Triassic salt deposits[J]. Microbiology,1999, 145(12): 3 565-3 574.
[4] Stan-Lotter H, Pfaffenhuemer M, Legat A,et al.Halococcus dombrowskii sp. nov., an archaeal isolate from a Permian alpine salt deposit[J]. International Journal of Systematic and Evolutionary Microbiology,2002, 52(5): 1 807-1 814.
[5] Vreeland R H, Jones J, Monson A,et al.Isolation of live Cretaceous (121-112 million years old) halophilic Archaea from primary salt crystals[J]. Geomicrobiology Journal,2007, 24: 275-282,doi:10.1080/01490450701456917.
[6] Vreeland R H, Rosenzweig W D, Powers D W.Isolation of a 250 million-year-old halotolerant bacterium from a primary salt crystal[J].Nature,2000, 407(6 806): 897-900.
[7] Mormile M R, Biesen M A, Gutierrez M C,et al.Isolation of Halobacterium salinarum retrieved directly from halite brine inclusions[J]. Environmental Microbiology,2003, 5(11):1 094-1 102.
[8] Gruber C, Legat A, Pfaffenhuemer M,et al.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[J]. Extremophiles,2004, 8(6): 431-439.
[9] Schubert B A, Lowenstein T K, Timofeeff M N.Microscopic identification of prokaryotes in modern and ancient halite, Saline Valley and Death Valley, California[J].Astrobiology,2009, 9(5): 467-482.
[10] Schubert B A, Lowenstein T K, Timofeeff M N,et al.How do prokaryotes survive in fluid inclusions in halite for 30 ky?[J]. Geology,2009, 37(12): 1 059-1 062.
[11] Schubert B A, Lowenstein T K, Timofeeff M N,et al.Halophilic archaea cultured from ancient halite, Death Valley, California[J]. Environmental Microbiology,2010, 12(2): 440-454.
[12] Schubert B A, Timofeeff M N, Lowenstein T K,et al.Dunaliella cells in fluid inclusions in halite: Significance for long-term survival of prokaryotes[J]. Geomicrobiology Journal,2010, 27(1): 61-75.
[13] Gramain A, Díaz G C, Demergasso C,et al.Archaeal diversity along a subterranean salt core from the Salar Grande (Chile)[J]. Environmental Microbiology,2011, 13(8): 2 105-2 121.
[14] Wang J, Lowenstein T K, Fang X.Microbial habitability and pleistocene aridification of the Asian Interior[J].Astrobiology,2016, 16(6): 379-388.
[15] Radax C, Gruber C, Stan-Lotter H.Novel haloarchaeal 16S rRNA gene sequences from Alpine Permo-Triassic rock salt[J].Extremophiles,2001,5(4):221-228.
[16] Fish S A, Shepherd T J, McGenity T J,et al. Recovery of 16S ribosomal RNA gene fragments from ancient halite[J]. Nature,2002, 417(6 887): 432-436.
[17] Park J S, Vreeland R H, Cho B C,et al.Haloarchaeal diversity in 23, 121 and 419 MYA salts[J]. Geobiology,2009, 7(5): 515-523.
[18] Sankaranarayanan K, Lowenstein T K, Timofeeff M N,et al.Characterization of ancient DNA supports long-term survival of haloarchaea[J]. Astrobiology,2014, 14(7): 553-560.
[19] Sankaranarayanan K, Timofeeff M N, Spathis R,et al.Ancient microbes from halite fluid inclusions: Optimized surface sterilization and DNA extraction[J]. PLoS One,2011, 6(6): e20683,doi:10.1371/journal.pone.0020683.
[20] Lowenstein T K, Schubert B A, Timofeeff M N.Microbial communities in fluid inclusions and long-term survival in halite[J].GSA Today,2011, 21(1): 4-9.
[21] Winters Y D, Lowenstein T, Timofeeff M.Identification of carotenoids in ancient salt from death valley, saline valley, and Searles Lake, California, using laser raman spectroscopy[J].Astrobiology,2013, 13(11): 1 065-1 080.
[22] Winters Y D, Lowenstein T K, Timofeeff M N.Starvation-survival in haloarchaea[J].Life,2015, 5(4): 1 587-1 609.
[23] McGenity T J, Gemmell R T, Grant W D,et al. Origins of halophilic microorganisms in ancient salt deposits[J]. Environmental Microbiology,2000, 2(3): 243-250.
[24] Roedder E.The fluids in salt[J]. American Mineralogist,1984, 69(5):413-439.
[25] Lowenstein T, Brennan S T.Fluid inclusions in paleolimnological studies of chemical sediments[M]∥Last W M, Smol J P, eds. Tracking Environmental Change Using Lake Sediments. New York: Kluwer Academic Publishers, 2002: 189-216.
[26] Dombrowski H J.Balneobiologische untersuchungen der nauheimer quellen[J].Zentralbl Bakteriol Parasitenkd Infektionskr Hygiene,1960, 178: 83-90.
[27] Reiser R, Tasch P.Investigation of the viability of osmophile bacteria of great geological age[J].Transactions of the Kansas Academy of Science,1960, 63: 31-34.
[28] Dombrowski H.Bacteria from Paleozoic salt deposits[J].Annals of the New York Academy of Sciences,1963, 108(2): 453-460.
[29] Dombrowski H J.Geological problems in the question of living bacteria in Paleozoic salt deposits[M]∥Rau J L, ed. Second Symposium on Salt. Cleveland. Ohio: Northern Ohio Geological Society, 1966: 215-219.
[30] Bibo F, Söngen R, Fresenius R.Vermehrungsfähige mikroorganismen in steinsalz aus primären lagerstätten[J].Kali und Steinsalz,1983, 8: 367-373.
[31] Norton C F, Grant W D.Survival of halobacteria within fluid inclusions in salt crystals[J].Journal of General Microbiology,1988, 134(5): 1 365-1 373.
[32] Norton C F, McGenity T J, Grant W D. Archaeal halophiles (halobacteria) from two British salt mines[J]. Journal of General Microbiology,1993, 139(5): 1 077-1 081.
[33] Grant W D, Gemmell R T, McGenity T J. Halobacteria: The evidence for longevity[J]. Extremophiles,1998, 2(3): 279-287.
[34] Vreeland R H, Rosenzweig W D.Survival of halophilic bacteria in ancient salts: Possibilities and potentials[M]∥Seckbach J, ed. Enigmatic Microorganisms and Life in Extreme Environments. The Netherlands: Kluwer Academic Publishers, 1999: 387-398.
[35] Fredrickson J K, Chandler D P, Onstott T C.Potential for preservation of halobacteria and their macromolecular constituents in brine inclusions from bedded salt deposits[C]∥SPIE Proceedings, 1997.
[36] Fendrihan S, Stan-Lotter H.Survival of halobacteria in fluid inclusions as a model of possible biotic survival in Martian halite[M]∥Teodorescu H, Griebel H, eds. Mars and Planetary Science and Technolgy. Iasi, Romania: Performantica Press, 2004: 9-18.
[37] Fendrihan S, Legat A, Pfaffenhuemer M,et al.Extremely halophilic archaea and the issue of long-term microbial survival[J]. Reviews in Environmental Science Biotechnology,2006, 5(2/3): 203-218.
[38] Adamski J C, Roberts J A, Goldstein R H.Entrapment of bacteria in fluid inclusions in laboratory-grown halite[J].Astrobiology,2006, 6(4): 552-562.
[39] Hazen R M, Roedder E.How old are bacteria from the Permian age[J].Nature,2001, 411(6 834): 155-156.
[40] Graur D, Pupko T.The Permian bacterium that isn’t[J].Molecular Biology and Evolution,2001, 18(6): 1 143-1 146.
[41] Nickle D C, Learn G H, Rain M W,et al.Curiously modern DNA for a ‘250 Million-Year-Old’ bacterium[J]. Journal of Molecular Evolution,2002, 54(1): 134-137.
[42] Hebsgaard M B, Phillips M J, Willerslev E.Geologically ancient DNA: Fact or artefact?[J].Trends in Microbiology,2005, 13(5): 212-220.
[43] Willerslev E, Hansen A J, Rønn R,et al.Long-term persistence of bacterial DNA[J]. Current Biology,2004, 14(1): R9-R10.
[44] Willerslev E, Cooper A.Ancient DNA[J].Proceedings of the Royal Society of London B: Biological Sciences,2005, 272(1 558): 3-16.
[45] Satterfield C L, Lowenstein T K, Vreeland R H,et al.New evidence for 250 Ma age of halotolerant bacterium from a Permian salt crystal[J]. Geology,2005, 33(4): 265-268.
[46] Lowenstein T K, Hardie L A.Criteria for the recognition of salt-pan evaporites[J].Sedimentology,1985, 32(5): 627-644.
[47] Arthurton R S.Experimentally produced halite compared with Triassic layered halite-rock from Cheshire, England[J]. Sedimentology,1973, 20(1): 145-160.
[48] Wardlaw N, Schwerdtner W.Halite-anhydrite seasonal layers in the middle Devonian Prairie evaporite formation, Saskatchewan, Canada[J].Geological Society of America Bulletin,1966, 77(4): 331-342.
[49] Panieri G, Lugli S, Manzi V,et al.Microbial communities in Messinian evaporite deposits of the Vena del Gesso (northern Apennines, Italy)[J]. Stratigraphy,2008, 5(34): 343-352.
[50] Panieri G, Lugli S, Manzi V,et al.Ribosomal RNA gene fragments from fossilized cyanobacteria identified in primary gypsum from the late Miocene, Italy[J]. Geobiology,2010, 8(2): 101-111.
[51] Schopf J W, Farmer J D, Foster I S,et al.Gypsum-permineralized microfossils and their relevance to the search for life on Mars[J]. Astrobiology,2012, 12(7): 619-633.
[52] Benison K C, Karmanocky F J.Could microorganisms be preserved in Mars gypsum? Insights from terrestrial examples[J].Geology,2014, 42(7): 615-618.
[53] Roveri M, Flecker R, Krijgsman W,et al.The messinian salinity crisis: Past and future of a great challenge for marine sciences[J]. Marine Geology,2014, 352: 25-58,doi:10.1016/j.margeo.2014.02.002.
[54] Bishop J L, Dyar M D, Lane M D,et al.Spectral identification of hydrated sulfates on Mars and comparison with acidic environments on Earth[J]. International Journal of Astrobiology,2004, 3(4): 275-285.
[55] Clark B C, Morris R V, McLennan S M,et al. Chemistry and mineralogy of outcrops at Meridiani Planum[J]. Earth and Planetary Science Letters,2005, 240(1): 73-94.
[56] Gendrin A, Mangold N, Bibring J-P,et al.Sulfates in martian layered terrains: The OMEGA/Mars express view[J]. Science,2005, 307(5 715): 1 587-1 591.
[57] Squyres S W, Arvidson R E, Bell J,et al.Ancient impact and aqueous processes at Endeavour Crater, Mars[J]. Science,2012, 336(6 081): 570-576.
[58] Davis L E.An Astrobiological Study of an Alkaline-saline Hydrothermal Environment, Relevant to Understanding the Habitability of Mars[D]. London: University College London, 2012.
[59] Novitsky J A, Morita R Y.Morphological characterization of small cells resulting from nutrient starvation of a psychrophilic marine vibrio[J].Applied and Environmental Microbiology,1976, 32(4): 617-622.
[60] Kjelleberg S, Humphrey B A, Marshall K C.Initial phases of starvation and activity of bacteria at surfaces[J].Applied and Environmental Microbiology,1983, 46(5): 978-984.
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