Characterization of potential stress responses in ancient Siberian permafrost psychroactive bacteria

Abstract

Past studies of cold-acclimated bacteria have focused primarily on organisms not capable of sub-zero growth. Siberian permafrost isolates Exiguobacterium sp. 255-15 and Psychrobacter sp. 273-4, which grow at subzero temperatures, were used to study cold-acclimated physiology. Changes in membrane composition and exopolysaccharides were defined as a function of growth at 24, 4 and -2.5 degrees C in the presence and absence of 5% NaCl. As expected, there was a decrease in fatty acid saturation and chain length at the colder temperatures and a further decrease in the degree of saturation at higher osmolarity. A shift in carbon source utilization and antibiotic resistance occurred at 4 versus 24 degrees C growth, perhaps due to changes in the membrane transport. Some carbon substrates were used uniquely at 4 degrees C and, in general, increased antibiotic sensitivity was observed at 4 degrees C. All the permafrost strains tested were resistant to long-term freezing (1 year) and were not particularly unique in their UVC tolerance. Most of the tested isolates had moderate ice nucleation activity, and particularly interesting was the fact that the Gram-positive Exiguobacterium showed some soluble ice nucleation activity. In general the features measured suggest that the Siberian organisms have adapted to the conditions of long-term freezing at least for the temperatures of the Kolyma region which are -10 to -12 degrees C where intracellular water is likely not frozen.

Bacterial genome replication at subzero temperatures in permafrost

“…Increases in both the production of extracellular polymeric substances (acting as cryoprotectants) and in bacterial abundance under similar subzero temperature conditions have been observed in brine channels from sea ice and frost flowers (Krembs et al, 2002;Collins et al, 2008;Meiners et al, 2008;Bowman and Deming 2010;Krembs et al, 2011). This hypothesis is further supported by recent evidence that permafrost isolates have thermohaline-dependent responses for both polysaccharide and fatty acid composition (Ponder et al, 2005) as well as for gene expression patterns (Mykytczuk et al, 2013). Alternatively, the activity of hypo-psychrophilic bacteria may represent a shift in competition for resources, where opportunistic psychrophiles that are adept at garnering nearly all the organic carbon at near freezing temperatures are inactive below À 6 1C.…”

Cultivation of a novel cold-adapted nitrite oxidizing betaproteobacterium from the Siberian Arctic

“…Our results suggested the existence of one so far unknown lowtemperature-adapted nitrite oxidizer. The adaptation is obviously realized by increasing the percentage of 16:1 cis 9 with decreasing temperature (Table 1), which is a strategy already described for ammonia oxidizing bacteria (Jones and Prahl, 1985) and bacterial isolates from permafrost soils (Ponder et al, 2005). Further enrichment cultures 6679, 6680 and 6681 incubated at 41C, 101C or 171C resulted in this typical pattern for Betaproteobacteria with 16:0 and 16:1 cis 9 as dominating compounds, too (not shown).…”

Biogeography of two cold-adapted genera: Psychrobacter and Exiguobacterium

“…can grow with additional NaCl in their medium (Romanenko et al, 2004;Shivaji et al, 2005;Rodrigues et al, 2006;Crapart et al, 2007). This evidence suggests that these genera are adapted to salinity, which would explain the strong correlation of the abundance of these genera to moderate to high salinity habitats, that is, Antarctic marine sediments, the Puerto Rican mangroves and the Siberian permafrost, the latter due to its limited but salty liquid phase (low water activity) (Ponder et al, 2005).…”

“…Studies with Psychrobacter and Exiguobacterium spp. isolated from the Siberian permafrost have shown that these genera can tolerate increased osmolarity and show associated changes in membrane composition, cell morphology and size (Ponder et al, 2005). Furthermore, all isolates from Exiguobacterium spp.…”

“…In addition to Siberian permafrost, species of Exiguobacterium and Psychrobacter have also been isolated from several other cold environments such as Antarctica soil, sea ice and Himalayan mountain soil (Bowman et al, 1997;Shivaji et al, 2005;Chaturvedi and Shivaji, 2006;Shravage et al, 2007). The fact that members of these genera seem to be successful in cold environments, yet have very distinct physiologies as one is Gram-positive (Exiguobacterium) (Ponder et al, 2005;Rodrigues et al, 2008) and the other is Gram-negative (Psychrobacter) (Bergholz et al, 2009), make them good candidates to test Baas Becking's statement 'everything is everywhere, the environment selects' for cold-adapted microorganisms. Results suggest that these cold-adapted microorganisms are not restricted to cold environments but are also found in temperate and tropical soils, although Psychrobacter especially is only marginally successful in the nonpolar habitats.…”