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

Abstract

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.

Unraveling the multiplicity of geranylgeranyl reductases in Archaea: potential roles in saturation of terpenoids

“…2 ) (Sasaki et al 2011 ). This cysteine is speculated to be involved in electron transfer or modulation of the reactivity of flavin (Xu et al 2010 ). The ligand-binding domain of archaeal GGRs consists of two tunnels: A and B (Sasaki et al 2011 ; Xu et al 2010 ).…”

“…This cysteine is speculated to be involved in electron transfer or modulation of the reactivity of flavin (Xu et al 2010 ). The ligand-binding domain of archaeal GGRs consists of two tunnels: A and B (Sasaki et al 2011 ; Xu et al 2010 ). Tunnel A is narrow and restrictive, whereas tunnel B is more permissive in its size (Sasaki et al 2011 ; Xu et al 2010 ) (Fig.…”

Tetraether archaeal lipids promote long‐term survival in extreme conditions

“…The unique, domain‐specific, isoprenoid‐based lipid membranes generated by all Archaea (Koga, 2014) are thought to assist but cannot completely resolve rationales for survival in the extremes. Beyond compositional and structural differences, the dynamic response of archaeal lipid membranes to changes in growth phase, growth rate, and temperature supports adaptive responses to rapid and often dramatic stimuli in highly volatile environments (Elling et al., 2014; Hurley et al., 2016; Qin et al., 2015; Yang et al., 2023; Zhou et al., 2020).…”

Membrane Adaptations and Cellular Responses of Sulfolobus acidocaldarius to the Allylamine Terbinafine

“…These proteins belong to the rSAM family. GrsA and GrsB introduce rings at the C-7 or C-3 position in GDGTs, and their expression is regulated by pH or temperature [ 11 , 12 ]. These GDGTs can be modified by the addition of headgroups.…”