Anaerobic glucose consumption is accelerated at non-proliferating elevated temperatures through upregulation of a glucose transporter gene in Corynebacterium glutamicum

• Published in: Applied microbiology and biotechnology Vol. 104; no. 15; pp. 6719 - 6729
• Main Authors: Uchikura, Hiroto, Toyoda, Koichi, Matsuzawa, Hiroki, Mizuno, Hikaru, Ninomiya, Kazuaki, Takahashi, Kenji, Inui, Masayuki, Tsuge, Yota
• Format: Journal Article
• Language: English
• Published: Berlin/Heidelberg Springer Berlin Heidelberg 01.08.2020; Springer; Springer Nature B.V
• Subjects: Aerobic conditions; Anaerobic conditions; Anaerobiosis; Analysis; Applied Microbial and Cell Physiology; Biological Transport; Biomedical and Life Sciences; Biotechnology; Cell growth; Cell proliferation; Complementation; Consumption; Corynebacterium glutamicum; Corynebacterium glutamicum - genetics; Corynebacterium glutamicum - metabolism; Dextrose; Enzymes; Gene Expression; Gene Expression Profiling; Genetic aspects; Genetic research; Genetic transcription; Glucose; Glucose - metabolism; Glucose transport; Glucose Transport Proteins, Facilitative - genetics; Glucose Transport Proteins, Facilitative - metabolism; Glucose transporter; Glycolysis; High temperature; Hot Temperature; Life Sciences; Metabolic Networks and Pathways; Metabolic pathways; Metabolism; Microbial Genetics and Genomics; Microbiology; Scientific equipment and supplies industry; Temperature; Tricarboxylic acid cycle; Up-Regulation; United States; Japan; Glycolysis; Temperature; Glucose consumption; Transcriptome; Anaerobic; Corynebacterium glutamicum
• ISSN: 0175-7598; 1432-0614
• DOI: 10.1007/s00253-020-10739-0

Cell proliferation is achieved through numerous enzyme reactions. Temperature governs the activity of each enzyme, ultimately determining the optimal growth temperature. The synthesis of useful chemicals and fuels utilizes a fraction of available metabolic pathways, primarily central metabolic pathways including glycolysis and the tricarboxylic acid cycle. However, it remains unclear whether the optimal temperature for these pathways is correlated with that for cell proliferation. Here, we found that wild-type Corynebacterium glutamicum displayed increased glycolytic activity under non-growing anaerobic conditions at 42.5 °C, at which cells do not proliferate under aerobic conditions. At this temperature, glucose consumption was not inhibited and increased by 28% compared with that at the optimal growth temperature of 30 °C. Transcriptional analysis revealed that a gene encoding glucose transporter ( iolT2 ) was upregulated by 12.3-fold compared with that at 30 °C, with concomitant upregulation of NCgl2954 encoding the iolT2 -regulating transcription factor. Deletion of iolT2 decreased glucose consumption rate at 42.5 °C by 28%. Complementation of iolT2 restored glucose consumption rate, highlighting the involvement of iolT2 in the accelerating glucose consumption at an elevated temperature. This study shows that the optimal temperature for glucose metabolism in C. glutamicum under anaerobic conditions differs greatly from that for cell growth under aerobic conditions, being beyond the upper limit of the growth temperature. This is beneficial for fuel and chemical production not only in terms of increasing productivity but also for saving cooling costs. Key points • C. glutamicum accelerated anaerobic glucose consumption at elevated temperature. • The optimal temperature for glucose consumption was above the upper limit for growth. • Gene expression involved in glucose transport was upregulated at elevated temperature. Graphical abstract