Subzero, saline incubations of Colwellia psychrerythraea reveal strategies and biomarkers for sustained life in extreme icy environments

Abstract

Colwellia psychrerythraea is a marine psychrophilic bacterium known for its remarkable ability to maintain activity during long-term exposure to extreme subzero temperatures and correspondingly high salinities in sea ice. These microorganisms must have adaptations to both high salinity and low temperature to survive, be metabolically active, or grow in the ice. Here, we report on an experimental design that allowed us to monitor culturability, cell abundance, activity and proteomic signatures of C. psychrerythraea strain 34H (Cp34H) in subzero brines and supercooled sea water through long-term incubations under eight conditions with varying subzero temperatures, salinities and nutrient additions. Shotgun proteomics found novel metabolic strategies used to maintain culturability in response to each independent experimental variable, particularly in pathways regulating carbon, nitrogen and fatty acid metabolism. Statistical analysis of abundances of proteins uniquely identified in isolated conditions provide metabolism-specific protein biosignatures indicative of growth or survival in either increased salinity, decreased temperature, or nutrient limitation. Additionally, to aid in the search for extant life on other icy worlds, analysis of detected short peptides in −10 C incubations after 4 months identified over 500 potential biosignatures that could indicate the presence of terrestrial-like cold-active or halophilic metabolisms on other icy worlds.

The transcriptome analysis of Escherichia coli responding to tellurite

“…The top ve downregulated genes were hC, hD, gH, iS and iE, encoding proteins FlhC, FlhD, FlgH, FliS and FliE respectively. FlhCD is a transcription activator responsible for the transcriptional activation of gene iA and involved in the regulation of the agella synthesis (Mudge et al 2021;Fitzgerald et al 2014). FlgH is the component of the L-ring located on the outer membrane layer, forming a molecular tube with the Pring (Akiba et al 1991;Minamino et al 2015).…”

Astrobiology of life on Earth

“…and at temperatures as low as −12 C. As such, and because its genome and many unusual biochemical features are already known, C. psychrerythraea has risen to become a model marine psychrophile for the study of carbon cycling in cold marine sediments, and a relevant subject for assessing growth and survivability under simulated Martian conditions. Using radiotracer methods, previous studies of this bacterium revealed protein synthesis in unamended cell suspensions at −20 C and in those supplemented with additional extracellular polymeric substances at −80 C. Mudge et al (2021) now utilize proteomic tools to reveal metabolic pathway-specific proteins produced by C. psychrerythraea in response to variations in temperature, salinity and nutrient status. In addition, useful new tools emerge from their research including a novel approach for life detection that identifies over 500 very short peptides whose sequences could be determined by either lander-based or in-orbit mass spectrometers and used as potential biosignatures of cold-or hypersaline metabolisms.…”

“…This indicates that extreme cold is not an insurmountable barrier for terrestrial (and presumably extraterrestrial) life. The special issue article by Mudge et al (2021) probes physiological features of Colwellia psychrerythraea, a polyextremophilic bacterium isolated from subzero marine sediments that can grow at a salinity up to 18% (wt./vol.) and at temperatures as low as −12 C. As such, and because its genome and many unusual biochemical features are already known, C. psychrerythraea has risen to become a model marine psychrophile for the study of carbon cycling in cold marine sediments, and a relevant subject for assessing growth and survivability under simulated Martian conditions.…”

“…A number of the special issue articles focus on life at low temperatures in the Arctic or Antarctic (Coleine et al . 2021; Mudge et al ., 2021; Pavankumar et al ., 2021; Magnuson et al ., 2021). These habitats are typically polyextreme due to combinations of extreme cold, low water‐activity, long‐term desiccation and freezing, salt(s), ultraviolet radiation, low‐nutrient conditions, and/or events that can be traumatic for the cell such as desiccation–rehydration (in some cases, caused by salt deliquescence–efflorescence) and freeze–thaw cycles (Hallsworth, 2018).…”

Biolocomotion and Premelting in Ice

“…It is important to emphasize that factors such as surface adhesion, salinity, the segregation of impurities of all types from the ice lattice, among other factors [67,69,71,72], make our treatment of chemotaxis a simplified starting point. However, field samples and laboratory experiments have shown that cell motility is influenced by chemotaxis at low temperature [40,73,74]. Thus, although there are many complicated interactions that provide scope for future work, the basic role of chemotaxis in the distribution of biota in ice must start with a self-consistent framework, which is the focus of our work.…”