Multiple environmental parameters impact lipid cyclization in Sulfolobus acidocaldarius

Abstract

Adaptation of lipid membrane composition is an important component of archaeal homeostatic response. Historically, the number of cyclopentyl and cyclohexyl rings in the glycerol dibiphytanyl glycerol tetraether (GDGT) Archaeal lipids has been linked to variation in environmental temperature. However, recent work with GDGT-making archaea highlight the roles of other factors, such as pH or energy availability, in influencing the degree of GDGT cyclization. To better understand the role of multiple variables in a consistent experimental framework and organism, we cultivated the model Crenarchaeon Sulfolobus acidocaldarius DSM639 at different combinations of temperature, pH, oxygen flux, or agitation speed. We quantified responses in growth rate, biomass yield, and core lipid compositions, specifically the degree of core GDGT cyclization. The degree of GDGT cyclization correlated with growth rate under most conditions. The results suggest the degree of cyclization in archaeal lipids records a universal response to energy availability at the cellular level, both in thermoacidophiles, and in other recent findings in the mesoneutrophilic Thaumarchaea. Although we isolated the effects of key individual parameters, there remains a need for multi-factor experiments (e.g., pH + temperature + redox) in order to more robustly establish a framework to better understand homeostatic membrane responses.

Physiological Characterization of Sulfolobus acidocaldarius in a Controlled Bioreactor Environment

“…While there is broad consensus on the optimal growth temperature of S. acidocaldarius being at 75 °C [ 7 , 8 , 9 , 10 , 33 ] the described optimal cultivation pH still varies [ 5 , 6 , 7 , 8 , 9 , 10 ]. Our study determined a pH optimum of 3.0 in regards to the cell density during continuous cultivation ( Figure 2 ), contradicting the recent publication by Cobban et al [ 11 ], in which higher biomass yields were observed at pH 2.0 and 4.0 compared to pH 3.0. A possible reason for the differences could be the used cultivation temperature for their experiments of 70 °C and that cultivations were performed in batch mode using a different medium.…”

“…Since the pH optimum of this organism is still disputed in literature and recently Cobban et al [ 11 ] showed data conflicting with the broad consensus of the optimal pH of 3 to 3.5 [ 5 , 6 , 7 , 8 , 9 , 10 ], we determined the pH optimum by shifting the pH from 2.0 to 4.0 in increments of 0.5 pH units at a constant growth temperature of 75 °C and dilution rate of 0.03 h −1 .…”

“…The organism thrives in a temperature range of 65 to 85 °C and at a pH ranging from pH 2.0 to 5.5 [ 4 ], while under laboratory conditions it is generally cultivated at temperatures of 70 to 75 °C and at a pH of 2.25 to 3.5 [ 5 , 6 , 7 , 8 , 9 , 10 ]. Most research with this organism is performed in batch cultivations using shake flasks as culture vessels [ 5 , 7 , 11 ]. However, a continuous cultivation in a stirred-tank reactor (CSTR) with the possibility to monitor and control pH, temperature and dissolved oxygen content (dO 2 ) is the basis for stable growth conditions, thereby allowing the acquisition of reliable and reproducible process data [ 12 ].…”

Disrupted Coherence Between Upwelling Strength and Redox Conditions Reflects Source Water Change in Santa Barbara Basin During the 20th Century

“…The degree of cyclization in GDGTs has successfully been used for reconstruction of sea surface temperature (SST), expressed in various SST proxies (Kim et al., 2010; Schouten et al., 2002; Wörmer et al., 2014). However, even though the sensitivity to temperature variations has been confirmed in pure culture experiments (Elling et al., 2015; Wuchter et al., 2004), studies investigating the effect of nutrient availability (Cobban et al., 2020; Evans et al., 2018; Hurley et al., 2016) and oxygen concentration (Cobban et al., 2020; Qin et al., 2015) also showed a strong response of the degree of cyclization. Additionally, the potential input of GDGTs from a second archeal clade, the Euryarchaeota of Marine Group II (MG II), possibly affects the GDGT signal exported to sediments.…”

The production of diverse brGDGTs by an Acidobacterium allows a direct test of temperature and pH controls on their distribution

“…The degree of cyclization in isoGDGTs is a key strategy for archaea to adapt to extreme environments, with more cyclopentyl moieties generally produced by archaea growing at a higher temperature or a lower pH (47)(48)(49). Molecular modeling suggests that an increase in isoGDGT cyclization degree leads to tighter membrane packing that enhances membrane thermal stability and reduces overall membrane permeability (50,51).…”