Genomic, Transcriptomic, and Proteomic Analysis Provide Insights Into the Cold Adaptation Mechanism of the Obligate Psychrophilic Fungus Mrakia psychrophila

Abstract

Mrakia psychrophila is an obligate psychrophilic fungus. The cold adaptation mechanism of psychrophilic fungi remains unknown. Comparative genomics analysis indicated that M. psychrophila had a specific codon usage preference, especially for codons of Gly and Arg and its major facilitator superfamily (MFS) transporter gene family was expanded. Transcriptomic analysis revealed that genes involved in ribosome and energy metabolism were upregulated at 4°, while genes involved in unfolded protein binding, protein processing in the endoplasmic reticulum, proteasome, spliceosome, and mRNA surveillance were upregulated at 20°. In addition, genes related to unfolded protein binding were alternatively spliced. Consistent with other psychrophiles, desaturase and glycerol 3-phosphate dehydrogenase, which are involved in biosynthesis of unsaturated fatty acid and glycerol respectively, were upregulated at 4°. Cold adaptation of M. psychrophila is mediated by synthesizing unsaturated fatty acids to maintain membrane fluidity and accumulating glycerol as a cryoprotectant. The proteomic analysis indicated that the correlations between the dynamic patterns between transcript level changes and protein level changes for some pathways were positive at 4°, but negative at 20°. The death of M. psychrophila above 20° might be caused by an unfolded protein response.

Living strategy of cold-adapted fungi with the reference to several representative species

“…The first integrated study on the genomic, transcriptomic and proteomic perspectives of M. psychrophila provided insights into the cold adaptation mechanism of psychrophilic fungi (Su et al 2016). The comparative genomic analysis with that of other psychrophilic, thermophilic and mesophilic fungi indicated that M. psychrophila had a specific codon usage preference, especially for codons of Gly and Arg and its major facilitator superfamily transporter gene family was expanded.…”

Ice‐binding proteins from the fungus Antarctomyces psychrotrophicus possibly originate from two different bacteria through horizontal gene transfer

“…These microbes have acquired several strategies against freezing that inevitably accompany ice crystal formation and overcome physical damages. An example of such a strategy is the production of cryoprotective substances, such as glycerol , trehalose , and ice‐binding proteins (IBPs) , which inhibit ice crystal growth. Nevertheless, cold‐survival mechanism and phylogenetic relationship of microbial IBPs, especially in fungi, are not well understood.…”

Transcriptomic time-series analysis of cold- and heat-shock response in psychrotrophic lactic acid bacteria

“…Upregulation of multidrug ABC transporter gene during cold temperature was reported for psychrophilic gram-negative bacteria Flavobacterium psychrophilum [45]. Similarly, upregulation of a MFS transporter gene during cold temperature was seen in psychrophilic fungus Mrakia psychrophila [46].…”

“…Both ABC and MFS transporters can play a role in stress resistance, especially in antibiotics resistance [44]. However, previous studies related to psychrophilic organisms also support that ABC and MFS transporters play a role in cold adaptation [45,46]. Upregulation of multidrug ABC transporter gene during cold temperature was reported for psychrophilic gram-negative bacteria Flavobacterium psychrophilum [45].…”