Proteomics of Colwellia psychrerythraea at subzero temperatures – a life with limited movement, flexible membranes and vital DNA repair

Abstract

The mechanisms that allow psychrophilic bacteria to remain metabolically active at subzero temperatures result from form and function of their proteins. We present first proteomic evidence of physiological changes of the marine psychrophile Colwellia psychrerythraea 34H (Cp34H) after exposure to subzero temperatures (-1, and -10°C in ice) through 8 weeks. Protein abundance was compared between different treatments to understand the effects of temperature and time, independently and jointly, within cells transitioning to, and being maintained in ice. Parallel [3H]-leucine and [3H]-thymidine incubations indicated active protein and DNA synthesis to -10°C. Mass spectrometry-based proteomics identified 1763 proteins across four experimental treatments. Proteins involved in osmolyte regulation and polymer secretion were found constitutively present across all treatments, suggesting that they are required for metabolic success below 0°C. Differentially abundant protein groups indicated a reallocation of resources from DNA binding to DNA repair and from motility to chemo-taxis and sensing. Changes to iron and nitrogen metabolism, cellular membrane structures, and protein synthesis and folding were also revealed. By elucidating vital strategies during life in ice, this study provides novel insight into the extensive molecular adaptations that occur in cold-adapted marine organisms to sustain cellular function in their habitat.

A Proteomic Perspective on the Bacterial Adaptation to Cold: Integrating OMICs Data of the Psychrotrophic Bacterium Exiguobacterium antarcticum B7

“…Applying the log 2 FC (log base 2 Fold Change) of the transcriptome in the calculated model, the fluxome was modified and the metabolic pathway of E. antarcticum B7 started to produce short-chain fatty acids. This metabolic behavior has been experimentally documented for other cold-adapted bacteria [23,25]. …”

“…In a genomic study of Colwellia psychrerytharea the proteins involved in the synthesis, ramification, and cis-isomerization of polyunsaturated fatty acids were described [22]. Subsequently, the authors identified differentially expressed genes of polyunsaturated fatty acid synthases ( pfaC , pfaA , and pfaD ) [23]. To date, these synthase enzymes have been described only in marine bacteria [23,24].…”

“…Subsequently, the authors identified differentially expressed genes of polyunsaturated fatty acid synthases ( pfaC , pfaA , and pfaD ) [23]. To date, these synthase enzymes have been described only in marine bacteria [23,24]. In Sphingopyxis alaskensis , the enzymes involved in the de novo synthesis of fatty acids were described using quantitative proteomic approaches [25].…”

Mechanisms of subzero growth in the cryophile Planococcus halocryophilus determined through proteomic analysis

“…Endonuclease IV, the enzyme responsible for recognition and priming of the damaged site for repair in numerous bacteria (Hosfield et al ., ), is increased almost threefold in the two stressed conditions compared to 23°C (Table ). Several proteins involved in DNA repair were also detected at −10°C in Colwellia psychrerythraea (Nunn et al ., ). In addition to potential increases in DNA damage, low temperatures and stress conditions can induce changes to DNA supercoiling, and since DNA topology has a substantial impact on gene expression (Pruss and Drlica, ), mediating these changes would be expected.…”

“…halocryophilus . This work is only the second proteomic study performed at such a low temperature (–10°C) (Nunn et al ., ) and the first at −10°C for an organism isolated from permafrost. Given its wide growth range and ability to grow at subzero temperatures, gaining a better understanding of the mechanisms used by this bacterium for subzero growth is particularly interesting.…”