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Chapter 12 : Low-Temperature Limits of Microbial Growth and Metabolism
Author:
P. Buford Price1
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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
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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
Figures
Low-Temperature Limits of Microbial Growth and Metabolism
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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
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