A comparative transcriptomic analysis provides insights into the cold-adaptation mechanisms of a psychrophilic yeast, Glaciozyma antarctica PI12
- 36 Downloads
Glaciozyma antarctica PI12, a psychrophilic yeast from Antarctica, grows well at low temperatures. However, it is not clear how it responds and adapts to cold and freeze stresses. Hence, this project was set out to determine the cold-adaptation strategies and mechanisms of G. antarctica PI12 using a transcriptomic analysis approach. G. antarctica PI12 cells, grown in rich medium at 12 °C, were exposed to freeze stress at 0 and − 12 °C for 6 h and 24 h. Their transcriptomes were sequenced and analyzed. A hundred and sixty-eight genes were differentially expressed. The yeast gene expression patterns were found to be dependent on the severity of the cold with more genes being differentially expressed at − 12 °C than at 0 °C. Glaciozyma antarctica PI12 was found to share some common adaptation strategies with other yeasts, Saccharomyces cerevisiae and Mrakia spp., but at the same time, found to have some of its own unique strategies and mechanisms. Among the unique mechanisms was the production of antifreeze protein to prevent ice-crystallization inside and outside the cell. In addition, several molecular chaperones, detoxifiers of reactive oxygen species (ROS), and transcription and translation genes were constitutively expressed in G. antarctica PI12 to enable the cells to endure the fluctuating freezing temperatures. Interestingly, G. antarctica PI12 used nitrite as an alternative terminal acceptor of electrons when the oxygen level was low to minimize disruption of energy production in the cell. These mechanisms coupled with several other common mechanisms ensured that G. antarctica PI12 adapted well to the cold temperatures.
KeywordsRNA-sequencing Differentially expressed gene (DEG) RT-qPCR Cold adaptation Antarctica
The funding supports from the Ministry of Science, Technology, and Innovation (MOSTI), Malaysia, under the Antarctica Flagship Programme (Sub-Project 1: FP1213E036) and Science Fund Project No: 08–05-MGI-GMB001 are gratefully acknowledged. We would also like to thank Miss Teoh Chui Peng for helping us to deposit the transcriptomic data to the NCBI GeneBank, and Michelle Wong for checking and editing the language in the final draft of the manuscript.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Albertyn J, Hohmann S, Thevelein JM, Prior BA (1994) GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high osmolarity glycerol response pathway. Mol Cell Biol 14:4135–4144CrossRefGoogle Scholar
- Ayala-del-Río HL, Chain PS, Grzymski JJ, Ponder MA, Ivanova N, Bergholz PW, Di Bartolo G, Hauser L, Land M, Bakermans C, Rodrigues D, Klappenbach J, Zarka D, Larimer F, Richardson P, Murray A, Thomashow M, Tiedje JM (2010) The genome sequence of Psychrobacter arcticus 273–4, a psychroactive Siberian permafrost bacterium, reveals mechanisms for adaptation to low-temperature growth. Appl Environ Microbiol 76:2304–2312CrossRefGoogle Scholar
- Firdaus-Raih M, Hashim NHF, Bharudin I, Abu Bakar MF, Huang KK, Alias H, Lee BKB, Mat Isa MN, Mat-Sharani S, Sulaiman S, Tay LJ, Zolkefli R, Muhammad Noor Y, Law DSN, Abdul Rahman SH, Md-Illias R, Abu Bakar FD, Najimudin N, Abdul Murad AM, Mahadi NM (2018) The Glaciozyma antarctica genome reveals an array of systems that provide sustained responses towards temperature variations in a persistently cold habitat. PLoS ONE. https://doi.org/10.1371/journal.pone.0189947 Google Scholar
- Fujita J (1999) Cold-shock response in mammalian cells. J Mol Microbiol Biotechnol 1:243–255Google Scholar
- Gupta KJ, Igamberdiev AU (2016) Reactive nitrogen species in mitochondria and their implications in plant energy status and hypoxic stress tolerance. Front Plant Sci 7:369Google Scholar
- Hébraud M, Potier P (1999) Cold-shock response and low-temperature adaptation in psychrotrophic bacteria. J Mol Microbiol Biotechnol 1:211–219Google Scholar
- Moriyama M, Abe J, Yoshida M, Tsurumi Y, Nakayama S (1995) Seasonal changes in freezing tolerance, moisture content and dry weight of three temperate grasses. Grassl Sci 41:21–25Google Scholar
- Su Y, Jiang X, Wu W, Wang M, Hamid MI, Xiang M, Liu X (2016) Genomic, transcriptomic, and proteomic analysis provide insights into the cold adaptation mechanism of the obligate psychrophilic fungus Mrakia psychrophila. G3 (Bethesda) 6:3603–3613Google Scholar
- Tsuji M (2018) Cold-stress responses in the Antarctic basidiomycetous yeast Mrakia blollopis. R Soc Open Sci 6:160106Google Scholar
- Yamano N, Higashida N, Endo C, Sakata N, Fujishima S, Maruyama A, Higashihara T (2000) Purification and characterization of N-Acetylglucosamine-6-phosphate deacetylase from a psychrotrophic marine bacterium, Alteromonas Species. Mar Biotechnol 2:57–64Google Scholar