Relationship of critical temperature to macromolecular synthesis and growth yield in Psychrobacter cryopegella

Abstract

Most microorganisms isolated from low-temperature environments (below 4 degrees C) are eury-, not steno-, psychrophiles. While psychrophiles maximize or maintain growth yield at low temperatures to compensate for low growth rate, the mechanisms involved remain unknown, as does the strategy used by eurypsychrophiles to survive wide ranges of temperatures that include subzero temperatures. Our studies involve the eurypsychrophilic bacterium Psychrobacter cryopegella, which was isolated from a briny water lens within Siberian permafrost, where the temperature is -12 degrees C. P. cryopegella is capable of reproducing from -10 to 28 degrees C, with its maximum growth rate at 22 degrees C. We examined the temperature dependence of growth rate, growth yield, and macromolecular (DNA, RNA, and protein) synthesis rates for P. cryopegella. Below 22 degrees C, the growth of P. cryopegella was separated into two domains at the critical temperature (T(critical) = 4 degrees C). RNA, protein, and DNA synthesis rates decreased exponentially with decreasing temperatures. Only the temperature dependence of the DNA synthesis rate changed at T(critical). When normalized to growth rate, RNA and protein synthesis reached a minimum at T(critical), while DNA synthesis remained constant over the entire temperature range. Growth yield peaked at about T(critical) and declined rapidly as temperature decreased further. Similar to some stenopsychrophiles, P. cryopegella maximized growth yield at low temperatures and did so by streamlining growth processes at T(critical). Identifying the specific processes which result in T(critical) will be vital to understanding both low-temperature growth and growth over a wide range of temperatures.

FIG. 1.

Temperature dependence of P. cryopegella growth rate. Each point represents the average of two to four replicates. Standard deviations are shown. Note that the y axis is a log scale, and lines of best fit are shown.

FIG. 2.

Temperature dependence of P. cryopegella growth yield. Each point represents the average of triplicate samples (except for −10 and −4°C, which represent two and one sample, respectively). Standard deviations are shown.

FIG. 3.

(A) Temperature dependence of P. cryopegella macromolecular synthesis rates. Each point represents the slope of the linear portion of the tritium uptake versus time curve for two samples minus killed controls. Standard errors of the slopes are shown. Note that the y axis is a log scale, and lines of best fit are shown. (B) Temperature dependence of P. cryopegella normalized macromolecular synthesis rates. (1 zmol = 10⁻²¹ mol.)

FIG. 4.

Analogous data for the mesophile S. oneidensis MR-1. (A) Temperature dependence of macromolecular synthesis and growth rates. Each point represents the slope of the linear portion of the tritium uptake versus time curve for two samples minus killed controls (for growth rate, each point represents the average of two to four samples). Lines of best fit are shown for DNA synthesis and growth rates. The standard error (synthesis rates) or standard deviation (growth rate) is shown. Note that the y axis is a log scale. (1 zmol = 10⁻²¹ mol.) (B) Temperature dependence of normalized macromolecular synthesis rates. (C) Yield versus temperature. Cell yield was measured as the number of cells present at the beginning of stationary phase at each temperature. Each point represents the average of at least three samples; standard deviations are shown.

FIG. 4.

Analogous data for the mesophile S. oneidensis MR-1. (A) Temperature dependence of macromolecular synthesis and growth rates. Each point represents the slope of the linear portion of the tritium uptake versus time curve for two samples minus killed controls (for growth rate, each point represents the average of two to four samples). Lines of best fit are shown for DNA synthesis and growth rates. The standard error (synthesis rates) or standard deviation (growth rate) is shown. Note that the y axis is a log scale. (1 zmol = 10⁻²¹ mol.) (B) Temperature dependence of normalized macromolecular synthesis rates. (C) Yield versus temperature. Cell yield was measured as the number of cells present at the beginning of stationary phase at each temperature. Each point represents the average of at least three samples; standard deviations are shown.

FIG. 4.

Analogous data for the mesophile S. oneidensis MR-1. (A) Temperature dependence of macromolecular synthesis and growth rates. Each point represents the slope of the linear portion of the tritium uptake versus time curve for two samples minus killed controls (for growth rate, each point represents the average of two to four samples). Lines of best fit are shown for DNA synthesis and growth rates. The standard error (synthesis rates) or standard deviation (growth rate) is shown. Note that the y axis is a log scale. (1 zmol = 10⁻²¹ mol.) (B) Temperature dependence of normalized macromolecular synthesis rates. (C) Yield versus temperature. Cell yield was measured as the number of cells present at the beginning of stationary phase at each temperature. Each point represents the average of at least three samples; standard deviations are shown.