Highlighted Text:
Show |
Hide
Full text loading...
Chapter 12 : Low-Temperature Limits of Microbial Growth and Metabolism
Author:
P. Buford Price1
VIEW AFFILIATIONS
HIDE AFFILIATIONS
Affiliations:
1: Physics Department, University of California, Berkeley, CA 94720
Content Type: Monograph
Publication Year:
2012
Category: Environmental Microbiology
Book DOI:
10.1128/9781555817183
Chapter DOI:
10.1128/9781555817183.ch12
MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
Preview this chapter:
Low-Temperature Limits of Microbial Growth and Metabolism, Page 1 of 2
< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555817183/9781555816049_Chap12-1.gif /docserver/preview/fulltext/10.1128/9781555817183/9781555816049_Chap12-2.gif
Abstract:
Depending on wind speed and direction, microbes are swept up from diverse terrestrial and oceanic environments and blown onto glacial ice. The activation energy for survival metabolism turns out to be ~110 kJ, but with an ~106-fold smaller preexponential factor than for unlimited growth. The arrival rates of bacteria and nonmicrobial dust blown from African desert sources to an air collector on Barbados showed similar patterns of seasonal and daily. In seeking to interpret the rapid decrease in fluorescence intensities of tryptophan (Trp) in the top 120 m of ice and the flattening of intensity values at greater depth, researchers carried out ground-truth measurements of cell concentrations in ice from several sites in Antarctica and Greenland. The main conclusion is that the depth dependence of cell concentration seen with epifluorescence microscopy is far weaker than the ~20-fold decrease with depth of the chlorophyll (Chl) and Trp fluorescence shown. The weak decrease in microbial concentration with depth suggests that both psychrophiles and nonpsychrophiles are equally able to adapt to the lower temperatures, lower nutrient availability, and immobility in ice than in oceans and soil. By using new techniques of single-cell genomics, it should be possible to track changes in their genome as a function of depth in the ice and thus to infer their mutation rates in the ocean before they reached the ice.
Citation:
Price P.
2012.
Low-Temperature Limits of Microbial Growth and Metabolism,
p 243-264.
In
Miller R, Whyte L (ed),
Polar Microbiology: Life in a Deep Freeze.
ASM Press, Washington, DC.
doi: 10.1128/9781555817183.ch12
Key Concept Ranking
- Bacteria and Archaea
- 1.0135151
- Viruses
- 0.5211195
- Chemicals
- 0.47878346
- Epifluorescence Microscopy
- 0.47114906
- Microbial Communities in Environment
- 0.46426177
1.0135151
Figures
Low-Temperature Limits of Microbial Growth and Metabolism
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555817183.chap12-1,webId=/content/author/10.1128/9781555817183.chap12-1,properties={foaf_givenname=P. Buford, foaf_name=P. Buford Price, foaf_surname=Price, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555817183.chap12-aff1]]}]]
Citation:
Price P.
2012.
Low-Temperature Limits of Microbial Growth and Metabolism,
p 243-264.
In
Miller R, Whyte L (ed),
Polar Microbiology: Life in a Deep Freeze.
ASM Press, Washington, DC.
doi: 10.1128/9781555817183.ch12
/content/10.1128/9781555817183.chap12.fig12-1
FIGURE 1
Size distributions of biotic (left) and abiotic (middle) particles in WAIS Divide ice. (Right) Dwarf cells on 0.2-µm filter. (Left and middle panels courtesy of John Priscu, reproduced with permission. Right image reprinted from Miteva and Brenchley [2005] , with permission of the publisher.)
10.1128/9781555817183/fig12-1_thmb.gif
10.1128/9781555817183/fig12-1.gif
FIGURE 1
Size distributions of biotic (left) and abiotic (middle) particles in WAIS Divide ice. (Right) Dwarf cells on 0.2-µm filter. (Left and middle panels courtesy of John Priscu, reproduced with permission. Right image reprinted from Miteva and Brenchley [2005] , with permission of the publisher.)
Citation:
Price P.
2012.
Low-Temperature Limits of Microbial Growth and Metabolism,
p 243-264.
In
Miller R, Whyte L (ed),
Polar Microbiology: Life in a Deep Freeze.
ASM Press, Washington, DC.
doi: 10.1128/9781555817183.ch12
/content/10.1128/9781555817183.chap12.fig12-2
FIGURE 2
Sketch of microbes confined to liquid veins in glacial ice. (Reprinted from Price [2000] with permission.) (Copyright 2000, National Academy of Sciences, U.S.A.)
10.1128/9781555817183/fig12-2_thmb.gif
10.1128/9781555817183/fig12-2.gif
FIGURE 2
Sketch of microbes confined to liquid veins in glacial ice. (Reprinted from Price [2000] with permission.) (Copyright 2000, National Academy of Sciences, U.S.A.)
Citation:
Price P.
2012.
Low-Temperature Limits of Microbial Growth and Metabolism,
p 243-264.
In
Miller R, Whyte L (ed),
Polar Microbiology: Life in a Deep Freeze.
ASM Press, Washington, DC.
doi: 10.1128/9781555817183.ch12
/content/10.1128/9781555817183.chap12.fig12-3
FIGURE 3
(Left) Linear fits to diameter (or perimeter) instead of area imply that cells on clay grains get access to their food at edges. (Right) Fe(III) reduction via a shuttle molecule that transports an electron to one of three locations with access to an Fe(III) ion (large black discs in octahedral planes). Dashed lines show examples of paths of shuttle molecules; dotted lines show paths of electrons. Several cells might be attached to outer surfaces of clay grains within a coating of unfrozen water. (Reprinted from Astrobiology, Tung et al. [2006] , with permission of the publisher.)
10.1128/9781555817183/fig12-3_thmb.gif
10.1128/9781555817183/fig12-3.gif
FIGURE 3
(Left) Linear fits to diameter (or perimeter) instead of area imply that cells on clay grains get access to their food at edges. (Right) Fe(III) reduction via a shuttle molecule that transports an electron to one of three locations with access to an Fe(III) ion (large black discs in octahedral planes). Dashed lines show examples of paths of shuttle molecules; dotted lines show paths of electrons. Several cells might be attached to outer surfaces of clay grains within a coating of unfrozen water. (Reprinted from Astrobiology, Tung et al. [2006] , with permission of the publisher.)
Citation:
Price P.
2012.
Low-Temperature Limits of Microbial Growth and Metabolism,
p 243-264.
In
Miller R, Whyte L (ed),
Polar Microbiology: Life in a Deep Freeze.
ASM Press, Washington, DC.
doi: 10.1128/9781555817183.ch12
/content/10.1128/9781555817183.chap12.fig12-4
FIGURE 4
Arrhenius plot showing data on microbial metabolism. See text for explanation. (Reprinted from Price and Sowers [2004] and augmented by points from Tung et al. [2005] , both with permission of the publisher.) (Copyright 2004, 2005, National Academy of Sciences, U.S.A.)
10.1128/9781555817183/fig12-4_thmb.gif
10.1128/9781555817183/fig12-4.gif
FIGURE 4
Arrhenius plot showing data on microbial metabolism. See text for explanation. (Reprinted from Price and Sowers [2004] and augmented by points from Tung et al. [2005] , both with permission of the publisher.) (Copyright 2004, 2005, National Academy of Sciences, U.S.A.)
Citation:
Price P.
2012.
Low-Temperature Limits of Microbial Growth and Metabolism,
p 243-264.
In
Miller R, Whyte L (ed),
Polar Microbiology: Life in a Deep Freeze.
ASM Press, Washington, DC.
doi: 10.1128/9781555817183.ch12
/content/10.1128/9781555817183.chap12.fig12-5
FIGURE 5
Berkeley Fluorescence Spectrometer showing vertical laser surrounded by seven photon counters just above an ice core on the moving translation stage in a dark lab at –20°C at NICL. The student in the middle is removing an ice core that was previously scanned.
10.1128/9781555817183/fig12-5_thmb.gif
10.1128/9781555817183/fig12-5.gif
FIGURE 5
Berkeley Fluorescence Spectrometer showing vertical laser surrounded by seven photon counters just above an ice core on the moving translation stage in a dark lab at –20°C at NICL. The student in the middle is removing an ice core that was previously scanned.
Citation:
Price P.
2012.
Low-Temperature Limits of Microbial Growth and Metabolism,
p 243-264.
In
Miller R, Whyte L (ed),
Polar Microbiology: Life in a Deep Freeze.
ASM Press, Washington, DC.
doi: 10.1128/9781555817183.ch12
/content/10.1128/9781555817183.chap12.fig12-6
FIGURE 6
Measurements with the BFS of Chl and Trp fluorescence intensity versus depth in ice cores from five sites in Antarctica and one site in Greenland. See text for explanation. (Data from R. A. Rohde, R. Bay, P. B. Price, and D. Tosi [unpublished].)
10.1128/9781555817183/fig12-6_thmb.gif
10.1128/9781555817183/fig12-6.gif
FIGURE 6
Measurements with the BFS of Chl and Trp fluorescence intensity versus depth in ice cores from five sites in Antarctica and one site in Greenland. See text for explanation. (Data from R. A. Rohde, R. Bay, P. B. Price, and D. Tosi [unpublished].)
Citation:
Price P.
2012.
Low-Temperature Limits of Microbial Growth and Metabolism,
p 243-264.
In
Miller R, Whyte L (ed),
Polar Microbiology: Life in a Deep Freeze.
ASM Press, Washington, DC.
doi: 10.1128/9781555817183.ch12
/content/10.1128/9781555817183.chap12.fig12-7
FIGURE 7
Cell concentrations in glacial ice from Greenland and Antarctica that was melted under various conditions and measured with epifluorescence microscopy via their NADH autofluorescence (unstained) and with SYBR Gold staining. See text for explanation. (Data from Liu and Price [unpublished].)
10.1128/9781555817183/fig12-7_thmb.gif
10.1128/9781555817183/fig12-7.gif
FIGURE 7
Cell concentrations in glacial ice from Greenland and Antarctica that was melted under various conditions and measured with epifluorescence microscopy via their NADH autofluorescence (unstained) and with SYBR Gold staining. See text for explanation. (Data from Liu and Price [unpublished].)
Citation:
Price P.
2012.
Low-Temperature Limits of Microbial Growth and Metabolism,
p 243-264.
In
Miller R, Whyte L (ed),
Polar Microbiology: Life in a Deep Freeze.
ASM Press, Washington, DC.
doi: 10.1128/9781555817183.ch12
/content/10.1128/9781555817183.chap12.fig12-8
FIGURE 8
Cell concentrations in GISP2 and Vostok ice. Some of the large scatter may be due to different techniques and criteria used in cell identification. (Some data points have been taken from the following references: a, Abyzov et al. [1998b] ; b, Abyzov et al. [2007] ; c, Abyzov [2004] ; d, Christner et al. [2006] ; e, Abyzov et al. [2004] ; f, Miteva et al. [2009] ; g, Yung et al. [2007] ; h, Tung et al. [2005]. )
10.1128/9781555817183/fig12-8_thmb.gif
10.1128/9781555817183/fig12-8.gif
FIGURE 8
Cell concentrations in GISP2 and Vostok ice. Some of the large scatter may be due to different techniques and criteria used in cell identification. (Some data points have been taken from the following references: a, Abyzov et al. [1998b] ; b, Abyzov et al. [2007] ; c, Abyzov [2004] ; d, Christner et al. [2006] ; e, Abyzov et al. [2004] ; f, Miteva et al. [2009] ; g, Yung et al. [2007] ; h, Tung et al. [2005]. )
Citation:
Price P.
2012.
Low-Temperature Limits of Microbial Growth and Metabolism,
p 243-264.
In
Miller R, Whyte L (ed),
Polar Microbiology: Life in a Deep Freeze.
ASM Press, Washington, DC.
doi: 10.1128/9781555817183.ch12
/content/10.1128/9781555817183.chap12.fig12-9
FIGURE 9
(Top) Annual modulation of both Chl and Trp from BFS data in WAIS Divide core ice over 4 years. (Bottom) Agreement of phases of annual modulation of Chl (BFS data) and SO4 2–. (BFS data from Price and Bay [unpublished]; SO4 2– data provided by Cole-Dai and Ferris at WAIS Divide Science Meeting, 2007.)
10.1128/9781555817183/fig12-9_thmb.gif
10.1128/9781555817183/fig12-9.gif
FIGURE 9
(Top) Annual modulation of both Chl and Trp from BFS data in WAIS Divide core ice over 4 years. (Bottom) Agreement of phases of annual modulation of Chl (BFS data) and SO4 2–. (BFS data from Price and Bay [unpublished]; SO4 2– data provided by Cole-Dai and Ferris at WAIS Divide Science Meeting, 2007.)
Citation:
Price P.
2012.
Low-Temperature Limits of Microbial Growth and Metabolism,
p 243-264.
In
Miller R, Whyte L (ed),
Polar Microbiology: Life in a Deep Freeze.
ASM Press, Washington, DC.
doi: 10.1128/9781555817183.ch12
/content/10.1128/9781555817183.chap12.fig12-10
FIGURE 10
Flow cytograms of autofluorescence of Chl and PE in melted ice from Greenland GISP (on the divide) and D4 (west of the divide), West Antarctica (WAIS Divide [WDC] and Siple Dome), and East Antarctica (Dome C and along a U.S.-Norway traverse). Rectangular boxes denote Prochlorococcus (high-Chl and low-Chl); inclined boxes denote Synechococcus (at Greenland D4, two likely strains are found).
10.1128/9781555817183/fig12-10_thmb.gif
10.1128/9781555817183/fig12-10.gif
FIGURE 10
Flow cytograms of autofluorescence of Chl and PE in melted ice from Greenland GISP (on the divide) and D4 (west of the divide), West Antarctica (WAIS Divide [WDC] and Siple Dome), and East Antarctica (Dome C and along a U.S.-Norway traverse). Rectangular boxes denote Prochlorococcus (high-Chl and low-Chl); inclined boxes denote Synechococcus (at Greenland D4, two likely strains are found).
Citation:
Price P.
2012.
Low-Temperature Limits of Microbial Growth and Metabolism,
p 243-264.
In
Miller R, Whyte L (ed),
Polar Microbiology: Life in a Deep Freeze.
ASM Press, Washington, DC.
doi: 10.1128/9781555817183.ch12
References
/content/book/10.1128/9781555817183.chap12
1.
Abbott, M. R.,, J. R. Richman,, R. M. Letelier,, and J. S. Bartlett. 2000. The spring bloom in the Antarctic Polar Frontal Zone as observed from a mesoscale array of bio-optical sensors. Deep Sea Res. Part 2 Top. Stud. Oceanogr. 47: 3285– 3314.
2.
Abyzov, S. S. 2004. Use of different methods for discovery of ice-entrapped microorganisms in ancient layers of the Antarctic glacier. Adv. Space Res. 33: 1222– 1230.
3.
Abyzov, S.,, M. Fukuchi,, S. Imura,, H. Kanda,, I. Mitskevich,, T. Naganuma,, M. Poglazova,, L. Savatyugin,, and M. Ivanov. 2004. Biological investigations of the Antarctic ice sheet: review, problems and prospects. Polar Biosci. 17: 106– 116.
4.
Abyzov, S. S.,, I. N. Mitskevich,, and M. Ivanov,. 2007. Microbiology of the Antarctic glacier above the Lake Vostok, p. 11– 39. In S. Abyzov, and D. Perovich (ed.), Climate Change and Polar Research. Luso-American Development Foundation, Lisbon, Portugal.
5.
Abyzov, S. S.,, I. N. Mitskevich,, and M. N. Poglazova. 1998a. Microflora of the deep glacier horizons of central Antarctica. Microbiology 67: 547– 555.
6.
Abyzov, S. S.,, I. N. Mitskevich,, M. N. Poglazova,, N. I. Barkov,, V. Y. Lipenkov,, N. E. Bobin,, B. B. Koudryashov,, and V. M. Pashkevich. 1998b. Antarctic ice sheet as a model in search of life on other planets. Adv. Space Res. 22: 363– 368.
7.
Albertano, P.,, D. DiSomma,, and E. Capucci. 1997. Cyanobacterial picoplankton from the Central Baltic Sea: cell size classification by image-analyzed fluorescence microscopy. J. Plankton Res. 19: 1405– 1416.
8.
Benner, S. A.,, K. G. Devine,, L. N. Matveeva,, and D. H. Powell. 2000. The missing organic molecules on Mars. Proc. Natl. Acad. Sci. USA 97: 2425– 2430.
9.
Bidle, K. D.,, S. H. Lee,, D. R. Marchant,, and P. G. Falkowski. 2007. Fossil genes and microbes in the oldest ice on Earth. Proc. Natl. Acad. Sci. USA 104: 13455– 13460.
10.
Bramall, N. E. 2007. The remote sensing of microorganisms. Ph.D. thesis. University of California—Berkeley, Berkeley, CA.
11.
Brinton, K. K. F.,, A. I. Tsapin,, D. Gilichinsky,, and G. D. McDonald. 2002. Aspartic acid racemization and age-depth relationships for organic carbon in Siberian permafrost. Astrobiology 2: 77– 82.
12.
Brook, E. J.,, T. Sowers,, and J. Orchardo. 1996. Rapid variations in atmospheric methane concentrations during the past 110,000 years. Science 273: 1087– 1091.
13.
Chance, B. 1991. Optical method. Annu. Rev. Biophys. Biophys. Chem. 20: 1– 28.
14.
Chisholm, S. W.,, R. J. Olson,, E. R. Zettler,, R. Goericke,, J. B. Waterbury,, and N. A. Welschmeyer. 1988. A novel free-living prochlorophyte occurs at high cell concentrations in the oceanic euphotic zone. Nature 334: 340– 343.
15.
Christner, B. C.,, G. Royston-Bishop,, C. M. Foreman,, B. R. Arnold,, M. Tranter,, K. A. Welch,, W. B. Lyons,, A. I. Tsapin,, M. Studinger,, and J. C. Priscu. 2006. Limnological conditions in subglacial Lake Vostok, Antarctica. Limnol. Oceanogr. 51: 2485– 2501.
16.
Christner, B. C.,, M. L. Skidmore,, J. C. Priscu,, M. Tranter,, and C. M. Foreman,. 2008. Bacteria in subglacial environments, p. 51– 71. In R. Margesin,, F. Schinner,, J.-C. Marx,, and C. Gerday (ed.), Psychrophiles: from Biodiversity to Biotechnology. Springer, Berlin, Germany.
17.
Clarke, S. 2003. Aging as war between chemical and biochemical processes: protein methylation and the recognition of age-damaged proteins for repair. Ageing Res. Rev. 2: 263– 285.
18.
Cleaves, H. J.,, K. E. Nelson,, and S. L. Miller. 2006. The prebiotic synthesis of pyrimidines in frozen solution. Naturwissenschaften 93: 228– 231.
19.
D'Elia, T.,, R. Veerapaneni,, and S. O. Rogers. 2008. Isolation of microbes from Lake Vostok accretion ice. Appl. Environ. Microbiol. 74: 4962– 4965.
20.
D'Elia, T.,, R. Veerapaneni,, V. Theraisnathan,, and S. O. Rogers. 2009. Isolation of fungi from Lake Vostok accretion ice. Mycologia 101: 751– 763.
21.
Dufresne, A.,, M. Salanoubat,, F. Partensky,, F. Artiguenave,, I. M. Axmann,, V. Barbe,, S. Duprat,, M. Y. Galperin,, E. V. Koonin,, F. Le Gall,, K. S. Makarova,, M. Ostrowski,, S. Oztas,, C. Robert,, I. B. Rogozin,, D. J. Scanlan,, N. Tandeau de Marsac,, J. Weissenbach,, P. Wincker,, Y. I. Wolf,, and W. R. Hess. 2003. Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc. Natl. Acad. Sci. USA 100: 10020– 10025.
22.
Estes, C.,, A. Duncan,, B. Wade,, C. Lloyd,, W. Ellis,, and L. Powers. 2003. Reagentless detection of microorganisms by intrinsic fluorescence. Biosens. Bioelectron. 18: 511– 519.
23.
Gregg, W. W. 2008. Assimilation of SeaWiFS ocean chlorophyll data into a three-dimensional global ocean model. J. Mar. Syst. 69: 205– 225.
24.
Jaenicke, R. 1980. Atmospheric aerosols and global climate. J. Aerosol Sci. 11: 577– 588.
25.
Johnson, S. S.,, M. B. Hebsgaard,, T. R. Christensen,, M. Mastepanov,, R. Nielsen,, K. Munch,, T. Brand,, M. T. P. Gilbert,, M. T. Zuber,, M. Bunce,, R. Rønn,, D. Gilichinsky,, D. Froese,, and E. Willerslev. 2007. Ancient bacteria show evidence of DNA repair. Proc. Natl. Acad. Sci. USA 104: 14401– 14405.
26.
Kirschvink, J. L.,, B. P. Weiss,, and N. J. Beukes. 2006. Boron, ribose, and a Martian origin for terrestrial life. Geochim. Cosmochim. Acta 70: S320.
27.
Larralde, R.,, M. P. Robertson,, and S. L. Miller. 1995. Rates of decomposition of ribose and other sugars: implications for chemical evolution. Proc. Natl. Acad. Sci. USA 92: 8158– 8160.
28.
Lazcano, A.,, and S. L. Miller. 1994. How long did it take for life to begin and evolve to cyanobacteria? J. Mol. Evol. 39: 546– 554.
29.
Leck, C.,, and E. K. Bigg. 2005. Biogenic particles in the surface microlayer and overlaying atmosphere in the central Arctic Ocean during summer. Tellus B Chem. Phys. Meteorol. 57: 305– 316.
30.
Levy, M.,, and S. L. Miller. 1998. The stability of the RNA bases: implications for the origin of life. Proc. Natl. Acad. Sci. USA 95: 7933– 7938.
31.
Lindahl, T.,, and N. Nyberg. 1972. Rate of depurination of native deoxyribonucleic acid. Biochemistry 11: 3610– 3618.
32.
Martins, Z.,, O. Botta,, M. L. Fogel,, M. A. Sephton,, D. P. Glavin,, J. S. Watson,, J. P. Dworkin,, A. W. Schwartz,, and P. Ehrenfreund. 2008. Extraterrestrial nucleobases in the Murchison meteorite. Earth Planet. Sci. Lett. 270: 130– 136.
33.
Miller, S. L.,, and L. E. Orgel. 1974. The Origins of Life on the Earth. Prentice-Hall, Princeton, NJ.
34.
Miteva, V. I.,, and J. E. Brenchley. 2005. Detection and isolation of ultrasmall microorganisms from a 120,000-year-old Greenland glacier ice core. Appl. Environ. Microbiol. 71: 7806– 7818.
35.
Miteva, V.,, T. Sowers,, and J. Brenchley. 2007. Production of N 2O by ammonia-oxidizing bacteria at subfreezing temperatures as a model for assessing the N 2O anomalies in the Vostok ice core. Geomicrobiol. J. 24: 451– 459.
36.
Miteva, V.,, T. Sowers,, C. Olsen,, and J. E. Brenchley. 2006. Geochemical and molecular data support a biogenic origin of methane in the basal Greenland ice, p. 371. In Proceedings of the 11th International Symposium on Microbial Ecology (ISME 11), Vienna, Austria, 20-25 August 2006. ISME Society, Wageningen, The Netherlands.
37.
Miteva, V.,, C. Teacher,, T. Sowers,, and J. Brenchley. 2009. Comparison of the microbial diversity at different depths of the GISP2 Greenland ice core in relationship to deposition climates. Environ. Microbiol. 11: 640– 656.
38.
Miyakawa, S.,, H. I. Cleaves,, and S. L. Miller. 2002. Cold origin of life: B. Implications based on pyrimidines and purines produced from frozen ammonium cyanide solutions. Orig. Life Evol. Biosph. 32: 209– 218.
39.
Moore, J. K.,, and M. R. Abbott. 2002. Surface chorophyll concentrations in relation to the Antarctic Polar Front: seasonal and spatial patterns from satellite observations. J. Mar. Syst. 37: 69– 86.
40.
Perron, J. T.,, J. X. Mitrovica,, M. Manga,, I. Matsuyama,, and M. A. Richards. 2007. Evidence for an ancient martian ocean in the topography of deformed shorelines. Nature 447: 840– 843.
41.
Price, P. B. 2000. A habitat for psychrophiles in deep Antarctic ice. Proc. Natl. Acad. Sci. USA 97: 1247– 1251.
42.
Price, P. B. 2009. Microbial genesis, life and death in glacial ice. Can. J. Microbiol. 55: 1– 11.
43.
Price, P. B.,, and T. Sowers. 2004. Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc. Natl. Acad. Sci. USA 101: 4631– 4636.
44.
Prospero, J. M.,, E. Blades,, G. Mathison,, and R. Naidu. 2005. Interhemispheric transport of viable fungi and bacteria from Africa to the Caribbean with soil dust. Aerobiologia 12: 1– 19.
45.
Ricardo, A.,, M. A. Carrigan,, A. N. Olcott,, and S. A. Benner. 2004. Borate minerals stabilize ribose. Science 303: 196.
46.
Rocap, G.,, D. L. Distel,, J. B. Waterbury,, and S. W. Chisholm. 2002. Resolution of Prochlorococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Appl. Environ. Microbiol. 68: 1180– 1191.
47.
Rohde, R. A. 2010. The development and use of the Berkeley Fluorescence Spectrometer to characterize microbial content and detect volcanic ash in glacial ice. Ph.D. thesis. University of California—Berkeley, Berkeley, CA.
48.
Rohde, R. A.,, and P. B. Price. 2007. Diffusion-controlled metabolism for long-term survival of single isolated microorganisms trapped within ice crystals. Proc. Natl. Acad. Sci. USA 104: 16592– 16597.
49.
Rohde, R. A.,, P. B. Price,, R. C. Bay,, and N. E. Bramall. 2008. In situ microbial metabolism as a cause of gas artifacts in ice. Proc. Natl. Acad. Sci. USA 105: 8667– 8672.
50.
Sanchez. R.,, J. Ferris,, and L. Orgel. 1966. Conditions for purine synthesis: did prebiotic synthesis occur at low temperatures? Science 153: 72– 73.
51.
Sheridan, P. P.,, V. I. Miteva,, and J. E. Brenchley. 2003. Phylogenetic analysis of anaerobic psychrophilic enrichment cultures obtained from a Greenland glacier ice core. Appl. Environ. Microbiol. 69: 2153– 2160.
52.
Sleep, N. H.,, and K. Zahnle. 1998. Refugia from asteroid impacts on early Mars and the early Earth. J. Geophys. Res. 103: 28529– 28544.
53.
Smith, J. J.,, J. P. Howington,, and G. A. McFeters. 1994. Survival, physiological response, and recovery of enteric bacteria exposed to a polar marine environment. Appl. Environ. Microbiol. 60: 2977– 2984.
54.
Sowers, T. 2001. N 2O record spanning the penultimate deglaciation from the Vostok ice core. J. Geophys. Res. 106: 31903– 31914.
55.
Sowers, T.,, R. B. Alley,, and J. Jubenville. 2003. Ice core records of atmospheric N 2O covering the last 106,000 years. Science 301: 945– 948.
56.
Tison, J.-L.,, R. Souchez,, E. W. Wolff,, J. C. Moore,, M. R. Legrand,, and J. de Angelis. 1998. Is a periglacial biota responsible for enhanced dielectric response in basal ice from the Greenland Ice Core Project ice core? J. Geophys. Res. 103: 18885– 18894.
57.
Trinks, H.,, W. Schröder,, and C. K. Biebricher. 2005. Ice and the origin of life. Orig. Life Evol. Biosph. 35: 429– 445.
58.
Tung, C.,, N. E. Bramall,, and P. B. Price. 2005. Microbial origin of excess methane in glacial ice and implications for life on Mars. Proc. Natl. Acad. Sci. USA 102: 18292– 18296.
59.
Tung, C.,, P. B. Price,, N. E. Bramall,, and G. Vrdoljak. 2006. Microorganisms metabolizing on clay grains in 3-km-deep Greenland basal ice. Astrobiology 6: 69– 86.
60.
Wettlaufer, J. S. 1999. Impurity effects in the premelting of ice. Phys. Rev. Lett. 82: 2516– 2519.
61.
Yung, P. T.,, H. S. Shafaat,, S. A. Connon,, and A. Ponce. 2007. Quantification of viable spores from a Greenland ice core. FEMS Microbiol. Ecol. 59: 300– 306.