Tryptophan-centered metabolic alterations coincides with lipid-mediated fungal response to cold stress

Yonghong Chen; Xiaoyu Yang; Longlong Zhang; Qunfu Wu; Shuhong Li; Jianghui Gou; Jiangbo He; Keqin Zhang; Shenghong Li; Xuemei Niu

doi:10.1016/j.heliyon.2023.e13066

Tryptophan-centered metabolic alterations coincides with lipid-mediated fungal response to cold stress

Heliyon. 2023 Jan 21;9(2):e13066. doi: 10.1016/j.heliyon.2023.e13066. eCollection 2023 Feb.

Authors

Affiliations

¹ State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University, Kunming 650032, China.
² Kunming Key Laboratory of Respiratory Disease, Kunming University, Kunming 650214, China.
³ State Key Laboratory of Phytochemistry and Plant Resources in West China, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650204, China.

Abstract

Tryptophan and its derived metabolites have been assumed to play important roles in the development and survival of organisms. However, the links of tryptophan and its derived metabolites to temperature change remained largely cryptic. Here we presented that a class of prenyl indole alkaloids biosynthesized from tryptophan dramatically accumulated in thermophilic fungus Thermomyces dupontii under cold stress, in which lipid droplets were also highly accumulated and whose conidiophores were highly build-up. Concurrently, disruption of the key NRPS gene involved in the biosynthesis of prenyl indole alkaloids, resulted in decreased lipid and shrunken mitochondria but enlarged vacuoles. Moreover, the Fe³⁺ and superoxide levels in ΔNRPS were significantly increased but the reactive oxygen species lipid peroxidation and autophagy levels decreased. Metabolomics study revealed that most enriched metabolites in ΔNRPS were mainly composed of tryptophan degraded metabolites including well known ROS scavenger kynurenamines, and lipid-inhibitors, anthranilic acid and indoleacetic acid, and free radical reaction suppressor free fatty acids. Transcriptomic analysis suggested that the key gene involved in tryptophan metabolism, coinciding with the lipid metabolic processes and ion transports were most up-regulated in ΔNRPS under stress. Our results confirmed a lipid-mediated fungal response to cold stress and unveiled a link of tryptophan-based metabolic reprogramming to the fungal cold adaption.

Keywords: Cold stress; Lipids; PIAs, prenyl indole alkaloids; Prenylated indole alkaloids; TEM, transmission electron microscope; Thermomyces dupontii; Tryptophan; Tryptophan metabolism.