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Biological Context for Exploring Subglacial Lake Environments

Biological Context for Exploring Subglacial Lake Environments. Brent Christner, Department of Biological Sciences xner@lsu.edu; http://brent.xner.net/ 3 rd SCAR SALE Meeting, 6 - 7 June 2007 Big Sky, Montana. OUTLINE. Limnological conditions in surface waters of Subglacial Lake Vostok.

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Biological Context for Exploring Subglacial Lake Environments

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  1. Biological Context for Exploring Subglacial Lake Environments Brent Christner, Department of Biological Sciencesxner@lsu.edu; http://brent.xner.net/ 3rd SCAR SALE Meeting, 6 - 7 June 2007Big Sky, Montana

  2. OUTLINE • Limnological conditions in surface waters of Subglacial Lake Vostok. • Predicting the biogeochemical contributions and physiology of microbes in subglacial lakes. • Adaptations of microorganisms to life in ice and extreme cold. • Genetic relationships between bacteria from global subglacial environments.

  3. Rationale for Ice Core Decontamination Protocol final sample [parameter] [parameter] 5 mm removedby melting 5 mm removed by washing 5 mmscraped core diameter removed core diameter removed Christner et al. 2005, Icarus, 174:572-584

  4. CONCENTRATION OF CELLS ON THE EXTERIOR AND INTERIOR OF ICE SAMPLES FROM THE BOTTOM ~100 M OF THE VOSTOK 5G ICE CORE 500 3520 B A Core exterior (outer 0.5 cm) Core interior (1.5 cm removed) 400 3540 3560 300 Cells mL-1 on core interior Depth (m) 3580 200 3600 100 3620 0 0 1e+5 2e+5 3e+5 4e+5 1e+1 1e+2 1e+3 1e+4 1e+5 1e+6 -1 Cells mL-1 on core exterior Cells mL Cell densities on the inside versus the outside of the ice core are statistically different (r = 0.016) and the data do not co-vary with depth (paired t-test, p < 0.050) Christner et al. in press; In: Psychrophiles: From Biodiversity to Biotechology, Springer

  5. 0 500 1000 1500 Depth (meters below the surface) 2000 2500 3000 3500 0 200 400 0 500 1000 1500 -50 -30 -10 Cells mL-1 Total organic carbon(ppb) Borehole Temperature (oC) VOSTOK 5G ICE CORE (VOSTOK STATION, ANTARCTICA) Christner et al. 2006, L&O 51:2485-2501

  6. SYBR Gold(DNA-containing) SYTO 9(LIVE) Propidium Iodide(DEAD) ACCRETION ICE I Significantly higher(p < 0.001) than cell densities >3,572 m ACCRETION ICE II Cells mL-1 of melt water 0 100 200 300 400 500 600 3510 3520 GLACIAL ICE(>420,000 years-old) 3530 3540 3550 3560 Depth in Vostok core (m) 3570 3580 3590 3600 3610 3620 Christner et al. 2006L&O, 51:2485-2501

  7. NONPURGEABLE ORGANIC CARBON AND TOTAL AMINO ACID CONCENTRATIONS IN THE ACCRETION ICE AAs represent 0.01% to 2% of the NPOC; AAs and NPOC concentrations were correlated in the accretion ice Christner et al. 2006, L&O 51:2485-2501

  8. 3200 m 3310 m 3539 m 3623 m 3750 m 3609 m Ice-water glacier ice shear layer (deformed) up Type I(particle inclusions) Type II(few inclusions) Christner et al. 2006

  9. Biogeochemical conditions in the surface waters of Lake Vostok †Partitioning coefficients based on ice & water chemistry of L. Bonney, Antarctica Christner et al. 2006, L&O, 51:2485-2501.

  10. MOLECULAR IDENTIFICATION OF BACTERIAL DNA SEQUENCES IN LAKE VOSTOK ACCRETION ICE • Major bacterial lineages: Proteobacteria (a, b, g and d),Firmicutes, Actinobacteria, and Bacteroidetes(Priscu et al. 1999; Christner et al. 2001, 2006; Bulat et al. 2004) • Thermophile-related phylotypesRubrobacterHydrogenophilus • Phylotypes related to chemolithoautotrophsHydrogenophilus Thiobacillus/Acidithiobacillus • Other notable bacterial phylotypes: Metal-reducing anaerobes? Methylotrophs? THESE DATA PROVIDE THE RATIONALE TO GENERATE HYPOTHESES ON MICROBIAL LIFESTYLES IN THE LAKE, BUT DO NOT CONFIRM PHYSIOLOGY

  11. Christner et al. in press; In: Psychrophiles: From Biodiversity to Biotechology, Springer

  12. PHYSIOLOGY, SURVIVAL STRATEGIES, AND EVOLUTION OF MICROBES IN SALEs • Can cells survive for extended periods in glacier ice and provide viable inoculi to SALEs? • How do microbes offset macromolecular damage incurred during transport through the ice? • Are there genotypic features which allow microbes to overcome the effects of low temperature? • Have microbes adapted to the high pressure and gas concentrations in SALEs? • Do cosmopolitan or endemic microbial species exist in subglacial environments?

  13. Reports of Viable Microorganisms Revived from Ancient Geological Samples

  14. Geochemical Anomalies Attributable to Microbial Activity? • Souchez et al. (1995) Very low oxygen concentration in the basal ice from Summit, Greenland, Geophys. Res. Lett., 22: 2001-2004. • Sowers (2001) The N2O record spanning the penultimate deglaciation from the Vostok ice core, J. Geograph. Res., 106:31903-31914. • Campen et al. (2003) Evidence of microbial consortia metabolizing within a low latitude mountain glacier, Geology, 31:231-234. • Flǜckiger et al. (2004) N2O and CH4variations during the last glacial epoch: Insight into global processes. Global Biogeoch. Cycles Vol 18. • Ahn et al. (2004) A record of atmosphericCO2 during the last 40,000 years from the Siple Dome, Antarctica ice core. J. Geophys. Res., 199, D13305. • Tung et al. (2005) Microbial origin of excess methane in glacial ice and implications for life on Mars. PNAS, 102:18292-18296. • Spahni et al. (2005) Atmospheric methane and nitrous oxide of the late Pleistocene from Antarctic ice cores. Science, 310:1317-21.

  15. OPTIMUM: enzymatic reactions occurring at maximal possible rate MAXIMUM: protein denaturation; collapse of the cytoplasmic membrane; thermal lysis MINIMUM: membrane gelling; transport processes so slow that growth cannot occur Growth rate Temperature In contrast to the high temperature maximum for growth, determining the low temperature limit can be experimentally difficult (e.g. 104-year doubling times of cryptoendoliths†) and it is usually extrapolated. Figure adapted from Brock Biology of Microorganisms 11e; †Sun and Friedmann (1999) Geomicrobiol. J. 16:193-202

  16. Bakermans et al. 2003 Carpenter et al. 2000 Breezee et al. 2004 * Sowers 2001 -40o -20o -15o -10o Christner 2002 Junge et al. 2006 * Tison et al. 1998 Panikov et al. 2006 Jakosky et al. 2003 Rivkina et al. 2000; * Campen et al. 2003 * Calculated from ice core gas data; not a direct measurement of microbial activity Liquid conditions Frozen conditions

  17. “Microbial habitat consisting of solid ice grains bounded by liquid veins. Two microbes are depicted as living in the vein of diameter dveinsurrounding a single grain of diameter D.” Price, P.B. (2000) A habitat for psychrophiles in deep Antarctic ice PNAS 97:1247-1251.

  18. [3H]THYMIDINE INCORPORATION BY ARTHROBACTER G200-C1 AT -15 oC n = 3 Bulk ion concentration 20 nmol L-1 Christner 2002, AEM 68:6435-6438

  19. DNA synthesis Protein synthesis METABOLISM UNDER FROZEN CONDITIONS (-5 oC) BY YEAST ISOLATED FROM 179 M IN VOSTOK 5G 40 Live cells 30 Dpm x 1000 20 n = 3 10 Dead cells 0 5 10 15 20 Days Amato and Christner, unpublished data

  20. IDENTIFICATION OF AN ICE ACTIVE PROTEIN FROM A CHRYSEOBACTERIUM SPECIES ISOLATED FROM 3519 M ~0.5 mm Kilodaltons 20 15 10 3 9.3 pH No activity Ice-pitting activity The pits form because the IBP binds to the crystal faces, interfering with their growth. IBPs in other species appear to have a cryoprotective function. Peptide sequence from trypsin fragment:VSS(I/L)STDSQ(I/L)SD No match to other IBPs and antifreezes that have been identified thus far! Christner and Raymond, unpublished data

  21. Low Temperature High Pressure ARE THERE PIEZOPHILES† IN DEEP ICE AND SALEs? Pressure units:1,000 atmospheres ≈ 101 MPa Most microbes show reduced growth rates at just a few hundred atmospheres Cell membranes becomes waxy and relatively impermeable at low temperature and high pressure Doug Bartlett, Scripps Institution of Oceanography†Display optimal growth at a pressure above atmospheric pressure

  22. Clone from deep-sea sediment 0.1 fixed substitutions per nucleotide position Phylogenetic analysis of Alphaproteobacteria from glacier environments using maximum likelihood1220-nucleotides of the 16s rRNA gene sequence Methylobacterium sp. UMB 3 Methylobacterium sp. UMB 26 Methylobacterium sp. V3 Methylobacterium sp. GIC 46 Methylobacteriumadhaesivum Methylobacterium sp. UMB 28 Methylobacteriumorganophilum Methylobacterium sp. zf-IVRht8 Methylobacterium sp. IS11 Methylobacteriumrhodinum Methylobacterium sp. G296-15 Methylobacterium sp. TD4 Red = permanently cold or frozen environmentsRed Bold = from glacier/basal iceBlue = from Lake Vostok accretion ice Methylobacterium sp. GIC52 Methylobacteriumextorquens Methylobacteriumzatmanii Methylobacterium sp. zf-IVRht11 Methylobacterium sp. G296-5 Methylobacteriumradiotolerans Methylobacteriumfujisawaense Methylobacteriumfujisawaense Sphingomonas sp. Arctic Sphingomonas sp. Antarctic Sphingomonas sp. G296-3 Sphingomonas sp. Muzt-J22 Sphingomonas sp. SIA181-1A1 Sphingomonas sp. SO3-7r Sphingomonaspaucimobilis Sphingomonas sp. CanClear1 Sphingomonassanguis Sphingomonas sp. M3C1.8k-TD1 Sphingomonasparapaucimobilis Sphingomonasechinoides Sphingomonas sp. FXS25 Sphingomonas sp. V1 Sphingomonas sp. G296-14 Sphingomonasanadarae Clone from deep-sea octacoral Sphingomonas sp. TSBY 64 Sphingomonas sp. TSBY 38 Sphingomonas sp. eh2 Sphingomonasaurantiaca Sphingomonasaerolata Sphingomonasaerolata Sphingomonasaerolata Sphingomonas sp. UMB 19 Sphingomonas sp. J05 Clone from Antarctic soil Sphingomonas sp. TSBY-61 Sphingomonas faeni Clone from subsurface aquifer Christner et al. in pressIn: Psychrophiles: From Biodiversity to Biotechology, Springer Sphingomonas sp. Antarctic IS01 Proteobacterialoutgroups Sphingomonas sp. TSBY-49

  23. Clone from deep-sea sediment 0.1 fixed substitutions per nucleotide position Phylogenetic analysis of Alphaproteobacteria from glacier environments using maximum likelihood1220-nucleotides of the 16s rRNA gene sequence Methylobacterium sp. UMB 3 Methylobacterium sp. UMB 26 Methylobacterium sp. V3 Methylobacterium sp. GIC 46 Methylobacteriumadhaesivum Methylobacterium sp. UMB 28 Methylobacteriumorganophilum Methylobacterium sp. zf-IVRht8 Methylobacterium sp. IS11 Methylobacteriumrhodinum Purple = Greenland (GISP2)Orange = Antarctica (Vostok, Siple, Taylor Dome, Taylor Valley)Green = HimalayanBlue = New Zealand Methylobacterium sp. G296-15 Methylobacterium sp. TD4 Methylobacterium sp. GIC52 Methylobacteriumextorquens Methylobacteriumzatmanii Methylobacterium sp. zf-IVRht11 Methylobacterium sp. G296-5 Methylobacteriumradiotolerans Methylobacteriumfujisawaense Methylobacteriumfujisawaense Sphingomonas sp. Arctic Glacier ice samples collected without the use of a drilling fluid Sphingomonas sp. Antarctic Sphingomonas sp. G296-3 Sphingomonas sp. Muzt-J22 Sphingomonas sp. SIA181-1A1 Sphingomonas sp. SO3-7r Sphingomonaspaucimobilis Sphingomonas sp. CanClear1 Sphingomonassanguis Sphingomonas sp. M3C1.8k-TD1 Sphingomonasparapaucimobilis Sphingomonasechinoides Sphingomonas sp. FXS25 Sphingomonas sp. V1 Sphingomonas sp. G296-14 Sphingomonasanadarae Clone from deep-sea octacoral Sphingomonas sp. TSBY 64 Sphingomonas sp. TSBY 38 Sphingomonas sp. eh2 Sphingomonasaurantiaca Sphingomonasaerolata Sphingomonasaerolata Sphingomonasaerolata Sphingomonas sp. UMB 19 Sphingomonas sp. J05 Clone from Antarctic soil Sphingomonas sp. TSBY-61 Sphingomonas faeni Clone from subsurface aquifer Christner et al. in pressIn: Psychrophiles: From Biodiversity to Biotechology, Springer Sphingomonas sp. Antarctic IS01 Proteobacterialoutgroups Sphingomonas sp. TSBY-49

  24. CONCLUSIONS • The accreted ice is a proxy to estimate biogeochemical conditions in surface waters of Subglacial Lake Vostok. • Variation in the accretion ice implies that ecological conditions are not spatially or temporally uniform in SLV. • The search for viable microbial ecosystems in SALEs need not be exclusive to those with thermotectonic or hydrothermal activity. • The low temperature limit for metabolic activity is probably lower than -40 oC. • Territory for further microbiological studies: How do microbes deal with the high pressure, extreme cold, low nutrient, and potentially high O2 concentrations? $National Science Foundation: EAR and OPP$

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