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

Jayme Feyhl-Buska,Chuanlun L Zhang,Jin-Xiang Wang,Chengling Jia,Yufei Chen,Eric S Boyd

doi:10.3389/fmicb.2016.01323

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.

Highlights

Archaea are known to populate nearly every niche inhabited by Bacteria (Cavicchioli, 2011)
Influence of Growth Phase on Tetraether Lipid Abundance and Composition. Both glycerol dibiphytanyl glycerol tetraether (GDGT) and glycerol tribiphytanyl glycerol tetraether (GTGT) were detected in the core and the polar lipid fractions of P. torridus cells harvested at all stages of growth when incubated at 58◦C in medium with a pH of 0.7
The abundance of core GDGTs ranged from 2.2 ± 0.3 to 35.6 ± 10.0 fg cell−1 during the growth cycle (Supplementary Table 1), with the highest abundance per cell detected during lag and early stationary phase grown cultures and the lowest abundance detected during log phase growth (Figure 2A)

Summary

Introduction

Archaea are known to populate nearly every niche inhabited by Bacteria (Cavicchioli, 2011). Disproportionate abundances of Archaea relative to Bacteria have been reported in a number of “extreme” environments, including those characterized by elevated salt, temperature, and acidity (Valentine, 2007). Archaea synthesize a variety of membrane lipids including glycerol dibiphytanyl glycerol tetraethers (GDGTs; De Rosa et al, 1980, 1986; De Rosa and Gambacorta, 1988; Macalady et al, 2004) which consist of two ether-linked C40 polyisoprenoid chains with zero to as many as four cyclopentyl rings and zero or one cyclohexyl ring [i.e., crenarchaeol (Sinninghe Damsté et al, 2002)] on each chain (Schouten et al, 2000, 2003; Figure 1). GTGTs have previously been proposed as an intermediate in the biosynthesis of a GDGT that contains zero cyclopentyl rings (i.e., GDGT-0) from two C40 diether core lipids (i.e., archaeol; Koga and Morii, 2007) while other authors have proposed GTGTs as a terminal biosynthetic product (Villanueva et al, 2014)

Methods

Results

Discussion

Conclusion