Thermophilic archaeon orchestrates temporal expression of GDGT ring synthases in response to temperature and acidity stress

Yang, Wei1; Chen, Huahui1; Chen, Yufei1; Chen, Aiping1,2; Feng, Xi1; Zhao, Bo1; Zheng, Fengfeng1; Fang, Hongwei1; Zhang, Changyi3; Zeng, Zhirui1,2,4

2022-12-01

10.1111/1462-2920.16301

ENVIRONMENTAL MICROBIOLOGY   Impact Factor & Quartile

1462-2912

1462-2920

Glycerol dibiphytanyl glycerol tetraethers (GDGTs) are unique archaeal membrane-spanning lipids with 0-8 cyclopentane rings on the biphytanyl chains. The cyclization pattern of GDGTs is affected by many environmental factors, such as temperature and pH, but the underlying molecular mechanism remains elusive. Here, we find that the expression regulation of GDGT ring synthase genes grsA and grsB in thermophilic archaeon Sulfolobus acidocaldarius is temperature- and pH-dependent. Moreover, the presence of functional GrsA protein, or more likely its products cyclic GDGTs rather than the accumulation of GrsA protein itself, is required to induce grsB expression, resulting in temporal regulation of grsA and grsB expression. Our findings establish a molecular model of GDGT cyclization regulated by environment factors in a thermophilic ecosystem, which could be also relevant to that in mesophilic marine archaea. Our study will help better understand the biological basis for GDGT-based paleoclimate proxies. Archaea inhabit a wide range of terrestrial and marine environments. In response to environment fluctuations, archaea modulate their unique membrane GDGTs lipid composition with different strategies, in particular GDGTs cyclization significantly alters membrane permeability. However, the regulation details of archaeal GDGTs cyclization in response to different environmental factor changes remain unknown. We demonstrated, for the first time, thermophilic archaea orchestrate the temporal expression of GDGT ring synthases, leading to delicate control of GDGTs cyclization to respond environmental temperature and acidity stress. Our study provides insight into the regulation of archaea membrane plasticity, and the survival strategy of archaea in fluctuating environments.

SCI

English

First ; Corresponding

National Natural Science Foundation of China["92051112","32170041"] ; Science, Technology and Innovation Commission of Shenzhen Municipality[20200925154325002] ; Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou)[K19313901]

Microbiology

Microbiology

WOS:000901758900001

WILEY

ENVIRONMENT/ECOLOGY

Web of Science

1.Southern Univ Sci & Technol, Dept Ocean Sci & Engn, Shenzhen, Peoples R China
2.Southern Marine Sci & Engn Guangdong Lab Guangzhou, Guangzhou, Peoples R China
3.Univ Illinois, Carl R Woese Inst Genom Biol, Urbana, IL USA
4.Southern Univ Sci & Technol, Dept Ocean Sci & Engn, Shenzhen 518055, Peoples R China

Yang, Wei,Chen, Huahui,Chen, Yufei,et al. Thermophilic archaeon orchestrates temporal expression of GDGT ring synthases in response to temperature and acidity stress[J]. ENVIRONMENTAL MICROBIOLOGY,2022.

Yang, Wei.,Chen, Huahui.,Chen, Yufei.,Chen, Aiping.,Feng, Xi.,...&Zeng, Zhirui.(2022).Thermophilic archaeon orchestrates temporal expression of GDGT ring synthases in response to temperature and acidity stress.ENVIRONMENTAL MICROBIOLOGY.

Yang, Wei,et al."Thermophilic archaeon orchestrates temporal expression of GDGT ring synthases in response to temperature and acidity stress".ENVIRONMENTAL MICROBIOLOGY (2022).