Influence of Growth Phase, pH, and Temperature on the Abundance and Composition of Tetraether Lipids in the Thermoacidophile Picrophilus torridus

Abstract

The abundance and composition of glycerol dibiphytanyl glycerol tetraether (GDGT) and glycerol tribiphytanyl glycerol tetraether (GTGT) lipids were determined as a function of growth phase as a proxy for nutrient availability, the pH of growth medium, and incubation temperature in cultures of the thermoacidophile Picrophilus torridus. Regardless of the cultivation condition, the abundance of GDGTs and GTGTs was greater in the polar than core fraction, with a marked decrease in core GDGTs in cultures harvested during log phase growth. These data are consistent with previous suggestions indicating that core GDGTs are re-functionalized during polar lipid synthesis. Under all conditions examined, polar lipids were enriched in a GDGT with 2 cyclopentyl rings (GDGT-2), indicating GDGT-2 is the preferred lipid in this taxon. However, lag or stationary phase grown cells or cells subjected to pH or thermal stress were enriched in GDGTs with 4, 5, or 6 rings and depleted in GDGTs with 1, 2, 3, rings relative to log phase cells grown under optimal conditions. Variation in the composition of polar GDGT lipids in cells harvested during various growth phases tended to be greater than in cells cultivated over a pH range of 0.3–1.1 and a temperature range of 53–63°C. These results suggest that the growth phase, the pH of growth medium, and incubation temperature are all important factors that shape the composition of tetraether lipids in Picrophilus. The similarity in enrichment of GDGTs with more rings in cultures undergoing nutrient, pH, and thermal stress points to GDGT cyclization as a generalized physiological response to stress in this taxon.

Multiple environmental parameters impact core lipid cyclization in Sulfolobus acidocaldarius

“…When pH deviated from the optimum pH of ∼3 for DSM639, cyclization decreased. Whereas prior thermoacidophile studies showed that cyclization primarily decreased with increases in pH (10, 11, 25), we observed decreased cyclization when the pH was both above and below optimal. Despite the similarity in RI values at pH 2 and pH 4, the composition of GDGTs at each pH also was distinct (Figure 2, Figure 5).…”

“…Growth rate and ring index broadly covary, independent of which variable is causing this forcing (Figure 4). The temperature, pH and shaking speed experiments show inverse trends between growth rate and RI, consistent with batch experiments in the existing Thaumarchaeota (Figure S1) and Crenarchaeota (Figure S2) literature (11, 12, 29). However, these trends directly oppose results from other experiments characterizing GDGT response to pH in thermoacidophiles (11).…”

“…The temperature, pH and shaking speed experiments show inverse trends between growth rate and RI, consistent with batch experiments in the existing Thaumarchaeota (Figure S1) and Crenarchaeota (Figure S2) literature (11, 12, 29). However, these trends directly oppose results from other experiments characterizing GDGT response to pH in thermoacidophiles (11). It is possible that the fastest growth conditions in batch culture are those with high environmental or energetic stress (high temperature/shaking speed), and this increase in stress necessitates generally higher cyclization for the cells to maintain homeostasis.…”

Chemotaxonomic characterisation of the thaumarchaeal lipidome

“…The high abundances of GTGTs in HWCG-III Thaumarchaeota are unprecedented among cultivated archaea (Table 2; cf. De Rosa and Gambacorta, 1988;Knappy et al, 2011;Feyhl-Buska et al, 2016) and have previously been interpreted to reflect sub-optimal growth conditions of Ca. N. yellowstonii (cf.…”

Living at the Extremes: Extremophiles and the Limits of Life in a Planetary Context

“…The lowest pHmin -0.06 was observed for two hyperacidophilic Archaea known as Picrophilus oshimae and P. torridus (pHopt 0.7), isolated from a solfataric hot spring in Noboribetsu (Hokkaido, Japan) (Schleper et al, 1996). These heterotrophic and aerobic polyextremophiles can also withstand temperatures of up to 65ºC (Topt = 60ºC, Tmin = 47ºC), potentially through increased cyclization of their tetraether membrane lipids as a generalized response to pH, temperature, and nutrient stress (Feyhl-Buska et al, 2016). In comparison to extreme acidophily, the highest pHmax of 12.5 was observed for an alkaliphilic, aerobic, mesophilic bacterium known as Serpentinomonas sp.…”