Independent metabolism of oligosaccharides is the keystone of synchronous utilization of cellulose and hemicellulose in Myceliophthora

Jia Liu; Meixin Chen; Shuying Gu; Rui Fan; Zhen Zhao; Wenliang Sun; Yonghong Yao; Jingen Li; Chaoguang Tian

doi:10.1093/pnasnexus/pgae053

Independent metabolism of oligosaccharides is the keystone of synchronous utilization of cellulose and hemicellulose in Myceliophthora

PNAS Nexus. 2024 Feb 6;3(2):pgae053. doi: 10.1093/pnasnexus/pgae053. eCollection 2024 Feb.

Authors

Jia Liu^{1

2}, Meixin Chen^{1

2}, Shuying Gu^{1

2}, Rui Fan^{1

2}, Zhen Zhao^{1

2}, Wenliang Sun^{1

2}, Yonghong Yao^{1

2}, Jingen Li^{1

2}, Chaoguang Tian^{1

2}

Affiliations

¹ Key Laboratory of Engineering Biology for Low-carbon Manufacturing, Tianjin Institute of Industrial Biotechnology, Chinese Academy of Sciences, Tianjin 300308, China.
² National Technology Innovation Center of Synthetic Biology, Tianjin 300308, China.

Abstract

The effective utilization of cellulose and hemicellulose, the main components of plant biomass, is a key technical obstacle that needs to be overcome for the economic viability of lignocellulosic biorefineries. Here, we firstly demonstrated that the thermophilic cellulolytic fungus Myceliophthora thermophila can simultaneously utilize cellulose and hemicellulose, as evidenced by the independent uptake and intracellular metabolism of cellodextrin and xylodextrin. When plant biomass serviced as carbon source, we detected the cellodextrin and xylodextrin both in cells and in the culture medium, as well as high enzyme activities related to extracellular oligosaccharide formation and intracellular oligosaccharide hydrolysis. Sugar consumption assay revealed that in contrast to inhibitory effect of glucose on xylose and cellodextrin/xylodextrin consumption in mixed-carbon media, cellodextrin and xylodextrin were synchronously utilized in this fungus. Transcriptomic analysis also indicated simultaneous induction of the genes involved in cellodextrin and xylodextrin metabolic pathway, suggesting carbon catabolite repression (CCR) is triggered by extracellular glucose and can be eliminated by the intracellular hydrolysis and metabolism of oligosaccharides. The xylodextrin transporter MtCDT-2 was observed to preferentially transport xylobiose and tolerate high cellobiose concentrations, which helps to bypass the inhibition of xylobiose uptake. Furthermore, the expression of cellulase and hemicellulase genes was independently induced by their corresponding inducers, which enabled this strain to synchronously utilize cellulose and hemicellulose. Taken together, the data presented herein will further elucidate the degradation of plant biomass by fungi, with implications for the development of consolidated bioprocessing-based lignocellulosic biorefinery.

Keywords: Myceliophthora thermophila; carbon catabolite repression; cellulose and hemicellulose; fungal biotechnology; independent utilization.