Cold Adaptation in the Antarctic Archaeon Methanococcoides burtonii Involves Membrane Lipid Unsaturation

Abstract

Direct analysis of membrane lipids by liquid chromatography-electrospray mass spectrometry was used to demonstrate the role of unsaturation in ether lipids in the adaptation of Methanococcoides burtonii to low temperature. A proteomics approach using two-dimensional liquid chromatography-mass spectrometry was used to identify enzymes involved in lipid biosynthesis, and a pathway for lipid biosynthesis was reconstructed from the M. burtonii draft genome sequence. The major phospholipids were archaeol phosphatidylglycerol, archaeol phosphatidylinositol, hydroxyarchaeol phosphatidylglycerol, and hydroxyarchaeol phosphatidylinositol. All phospholipid classes contained a series of unsaturated analogues, with the degree of unsaturation dependent on phospholipid class. The proportion of unsaturated lipids from cells grown at 4°C was significantly higher than for cells grown at 23°C. 3-Hydroxy-3-methylglutaryl coenzyme A synthase, farnesyl diphosphate synthase, and geranylgeranyl diphosphate synthase were identified in the expressed proteome, and most genes involved in the mevalonate pathway and processes leading to the formation of phosphatidylinositol and phosphatidylglycerol were identified in the genome sequence. In addition, M. burtonii encodes CDP-inositol and CDP-glycerol transferases and a number of homologs of the plant geranylgeranyl reductase. It therefore appears that the unsaturation of lipids may be due to incomplete reduction of an archaeol precursor rather than to a desaturase mechanism. This study shows that cold adaptation in M. burtonii involves specific changes in membrane lipid unsaturation. It also demonstrates that global methods of analysis for lipids and proteomics linked to a draft genome sequence can be effectively combined to infer specific mechanisms of key biological processes.

Recent Advances in Structural Research on Ether Lipids from Archaea Including Comparative and Physiological Aspects

“…Nichols et al 37) have also identified unsaturated archaeol-and unsaturated hydroxyarchaeol-based phospholipids with glycerol and inositol as polar head groups by HPLC-MS in a psychrotrophic methanoarchaeon, Methanococcoides burtonii, isolated at Ace Lake in Antarctica. They reported that the unsaturated archaeol core contains one to five double bonds, although the location of the double bonds could not be determined.…”

“…In fact, all of the hyperthermophilic Pyrococcus furiosus (optimum temperature, 98 C), 33) moderately thermophilic Methanothermobacter thermautotrophicus (65 C), 74) mesophilic Methanobacterium formicicum (37 C), 54) and Methanogenium cariaci (23 C) 54) have caldarcheaol-based polar lipids with a smaller amount of archaeol-based lipid. Unsaturated archaeol (geranylgeranyl group-containing archaeol) is present in psychrophilic Methanococcoides burtonii 37) that can grow at 2 C as well as in hyperthermophilic Methanopyrus kandleri (98 C). 34) The same ether lipids of archaea can be utilized at both high and low temperatures because of their liquid crystalline phase and low permeability in a wide range of temperatures.…”

“…77) The content of trans-unsaturation of isoprenoid chain has been reported to decrease with higher growth temperatures in Methanococcoides burtonii., 37) but it is not known what influence these changes in isoprenoid chains exerts on the properties of lipid membranes (e.g., phase behavior, permeability, or rigidity). Archaeal lipid membrane is not required to regulate its hydrocarbon composition to meet the two conditions for adaptation to temperature because the two conditions are realized over a wide range of temperatures.…”

“…On the other hand, phospholipids with the same unsaturated isoprenoid are present in cold-tolerant methanoarchaeon Methanococcoides burtonii cells. 37) This shows that stable ether bonds are not required for life in hot environments. This is not an exceptional example.…”

Terrestrial models for extraterrestrial life: methanogens and halophiles at Martian temperatures

“…Given the abundance and diversity of Archaea in cold environments (Karner et al 2001;Feller & Gerday 2003), especially in the oceans, our understanding of the genetics and physiology of coldadapted Archaea is surprisingly scarce . Some insights have been obtained on the level of protein structure and function (Schleper et al 1997;Thomas et al 2001;Siddiqui et al 2002), gene regulation (Lim et al 2000;DasSarma 2006), tRNA modification (Noon et al 2004), membrane lipid composition (Nichols et al 2004 ;Gibson et al 2005), proteomics (Goodchild et al 2004a(Goodchild et al , b, 2005Saunders et al 2005) and genomics (Saunders et al 2003) by studying coldadapted Archaea.…”