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Bacterial genome replication at subzero temperatures in permafrost.

ABSTRACT: Microbial metabolic activity occurs at subzero temperatures in permafrost, an environment representing ?25% of the global soil organic matter. Although much of the observed subzero microbial activity may be due to basal metabolism or macromolecular repair, there is also ample evidence for cellular growth. Unfortunately, most metabolic measurements or culture-based laboratory experiments cannot elucidate the specific microorganisms responsible for metabolic activities in native permafrost, nor, can bulk approaches determine whether different members of the microbial community modulate their responses as a function of changing subzero temperatures. Here, we report on the use of stable isotope probing with (13)C-acetate to demonstrate bacterial genome replication in Alaskan permafrost at temperatures of 0 to -20?°C. We found that the majority (80%) of operational taxonomic units detected in permafrost microcosms were active and could synthesize (13)C-labeled DNA when supplemented with (13)C-acetate at temperatures of 0 to -20?°C during a 6-month incubation. The data indicated that some members of the bacterial community were active across all of the experimental temperatures, whereas many others only synthesized DNA within a narrow subzero temperature range. Phylogenetic analysis of (13)C-labeled 16S rRNA genes revealed that the subzero active bacteria were members of the Acidobacteria, Actinobacteria, Chloroflexi, Gemmatimonadetes and Proteobacteria phyla and were distantly related to currently cultivated psychrophiles. These results imply that small subzero temperature changes may lead to changes in the active microbial community, which could have consequences for biogeochemical cycling in permanently frozen systems.

SUBMITTER: Tuorto SJ

PROVIDER: S-EPMC3869017 | biostudies-literature | 2014 Jan

REPOSITORIES: biostudies-literature

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Bacterial genome replication at subzero temperatures in permafrost.

Tuorto Steven J SJ Darias Phillip P McGuinness Lora R LR Panikov Nicolai N Zhang Tingjun T Häggblom Max M MM Kerkhof Lee J LJ

The ISME journal 20130829 1

Microbial metabolic activity occurs at subzero temperatures in permafrost, an environment representing ∼25% of the global soil organic matter. Although much of the observed subzero microbial activity may be due to basal metabolism or macromolecular repair, there is also ample evidence for cellular growth. Unfortunately, most metabolic measurements or culture-based laboratory experiments cannot elucidate the specific microorganisms responsible for metabolic activities in native permafrost, nor, c ...[more]

PMID: 23985750

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Project description:ObjectivePreservation of biological materials at subzero Centigrade temperatures, cryopreservation, is important for the field of tissue engineering and organ transplantation. Our group is studying the use of isochoric (constant volume) systems of aqueous solution for cryopreservation. Previous studies measured the pressure-temperature relations in aqueous isochoric systems in the temperature range from 0°C to - 20°C. The goal of this study is to expand the pressure-temperature measurement beyond the range reported in previous publications.Materials and methodsTo expand the pressure-temperature measurements beyond the previous range, we have developed a new isochoric device capable of withstanding liquid nitrogen temperatures and pressures of up to 413 MPa. The device is instrumented with a pressure transducer than can monitor and record the pressures in the isochoric chamber in real time. Measurements were made in a temperature range from - 5°C to liquid nitrogen temperatures for various solutions of pure water and Me2SO (a chemical additive used for protection of biological materials in a frozen state and for vitrification (glass formation) of biological matter). Undissolved gaseous are is carefully removed from the system.ResultsTemperature-pressure data from - 5°C to liquid nitrogen temperature for pure water and other solutions are presented in this study. Following are examples of some, temperature-pressure values, that were measured in an isochoric system containing pure water: (- 20°C, 187 MPa); (-25°C, 216 MPa); (- 30°C, 242.3 MPa); (-180°C, 124 MPa). The data is consistent with the literature, which reports that the pressure and temperature at the triple point, between ice I, ice III and water is, - 21.993°C and 209.9 MPa, respectively. It was surprising to find that the pressure in the isochoric system increases at temperatures below the triple point and remains high to liquid nitrogen temperatures. Measurements of pressure-temperature relations in solutions of pure water and Me2SO in different concentrations show that, for concentrations in which vitrification is predicted, no increase in pressure was measured during rapid cooling to liquid nitrogen temperatures. However, ice formation either during cooling or warming to and from liquid nitrogen temperatures produced an increase in pressure.ConclusionsThe data obtained in this study can be used to aid in the design of isochoric cryopreservation protocols. The results suggest that the pressure measurement is important in the design of "constant volume" systems and can provide a simple means to gain information on the occurrence of vitrification and devitrification during cryopreservation processes of aqueous solutions in an isochoric system.

Project description:Cryopeg brines are isolated volumes of hypersaline water in subzero permafrost. The cryopeg system at Utqiaġvik, Alaska, is estimated to date back to 40 ka BP or earlier, a remnant of a late Pleistocene Ocean. Surprisingly, the cryopeg brines contain high concentrations of organic carbon, including extracellular polysaccharides, and high densities of bacteria. How can these physiologically extreme, old, and geologically isolated systems support such an ecosystem? This study addresses this question by examining the energetics of the Utqiaġvik cryopeg brine ecosystem. Using literature-derived assumptions and new measurements on archived borehole materials, we first estimated the quantity of organic carbon when the system formed. We then considered two bacterial growth trajectories to calculate the lower and upper bounds of the cell-specific metabolic rate of these communities. These bounds represent the first community estimates of metabolic rate in a subzero hypersaline environment. To assess the plausibility of the different growth trajectories, we developed a model of the organic carbon cycle and applied it to three borehole scenarios. We also used dissolved inorganic carbon and nitrogen measurements to independently estimate the metabolic rate. The model reconstructs the growth trajectory of the microbial community and predicts the present-day cell density and organic carbon content. Model input included measured rates of the in-situ enzymatic conversion of particulate to dissolved organic carbon under subzero brine conditions. A sensitivity analysis of model parameters was performed, revealing an interplay between growth rate, cell-specific metabolic rate, and extracellular enzyme activity. This approach allowed us to identify plausible growth trajectories consistent with the observed bacterial densities in the cryopeg brines. We found that the cell-specific metabolic rate in this system is relatively high compared to marine sediments. We attribute this finding to the need to invest energy in the production of extracellular enzymes, for generating bioavailable carbon from particulate organic carbon, and the production of extracellular polysaccharides for cryoprotection and osmoprotection. These results may be relevant to other isolated systems in the polar regions of Earth and to possible ice-bound brines on worlds such as Europa, Enceladus, and Mars.

Dataset Information

Bacterial genome replication at subzero temperatures in permafrost.

Publications

Bacterial genome replication at subzero temperatures in permafrost.

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