Important roles for membrane lipids in haloarchaeal bioenergetics

Abstract

Recent advances in lipidomic analysis in combination with various physiological experiments set the stage for deciphering the structure-function of haloarchaeal membrane lipids. Here we focused primarily on changes in lipid composition of Haloferax volcanii, but also performed a comparative analysis with four other haloarchaeal species (Halobacterium salinarum, Halorubrum lacusprofundi, Halorubrum sodomense and Haloplanus natans) all representing distinctive cell morphologies and behaviors (i.e., rod shape vs. pleomorphic behavior). Common to all five haloarchaea, our data reveal an extraordinary high level of menaquinone, reaching up to 72% of the total lipids. This ubiquity suggests that menaquinones may function beyond their ordinary role as electron and proton transporter, acting simultaneously as ion permeability barriers and as powerful shield against oxidative stress. In addition, we aimed at understanding the role of cations interacting with the characteristic negatively charged surface of haloarchaeal membranes. We propose for instance that by bridging the negative charges of adjacent anionic phospholipids, Mg acts as surrogate for cardiolipin, a molecule that is known to control curvature stress of membranes. This study further provides a bioenergetic perspective as to how haloarchaea evolved following oxygenation of Earth's atmosphere. The success of the aerobic lifestyle of haloarchaea includes multiple membrane-based strategies that successfully balance the need for a robust bilayer structure with the need for high rates of electron transport - collectively representing the molecular basis to inhabit hypersaline water bodies around the planet.

Lipid Anchoring of Archaeosortase Substrates and Midcell Growth in Haloarchaea

“…Such a mechanism would directly result in a covalently modified protein C terminus. While an archaetidylethanolamine lipid was reported to be absent from Halobacterium salinarum or Haloarcula marismortui (25), it is present in H. volcanii and several other haloarchaea, albeit at various abundances (26).…”

Heat Stress Dictates Microbial Lipid Composition along a Thermal Gradient in Marine Sediments

“…Thus, we propose that unsaturated tetraethers do not likely reflect an archaeal membrane adaptation to extreme high temperatures, as suggested recently ( Bauersachs et al, 2015 ). Conversely, unsaturation might be critical for motion of the rigid isoprenoidal membranes ( Kellermann et al, 2016a ). Supporting the idea that unsaturation of isoprenoids may not directly represent a thermal adaptation, unsaturated diethers are observed in several archaea ranging from psychrophilic to hyperthermophilic ( Gonthier et al, 2001 ; Nishihara et al, 2002 ; Nichols et al, 2004 ; Gibson et al, 2005 ; Kellermann et al, 2016a ).…”

“…That is, although considerable changes in microbial community composition are expected along this thermal gradient, we predict that any given living cell must adjust its cell membranes to in situ temperature conditions. We thus tested the concept that membrane lipids dictate the thermodynamic ecology of bacteria and archaea in stressful conditions ( Valentine, 2007 ; Valentine and Valentine, 2009 ; Kellermann et al, 2016a ). The general strategy of this paper features a detailed lipidomics approach with the focus on membrane lipid structure-function based on experimental data from the literature (e.g., pure culture experiments and/or molecular dynamics simulations).…”

Whole‐genome comparison between the type strain of Halobacterium salinarum (DSM 3754T) and the laboratory strains R1 and NRC‐1

“…It has been extensively studied as a model archaeal extremophile, resulting in numerous discoveries and insights into archaeal biology and the adaptations required to live at saturating salt concentrations (see reviews by Beer, Wurtmann, Pinel, & Baliga, ; Soppa, ) and the references within). Examples include prokaryotic glycoproteins (Mescher & Strominger, ), archaeal isoprenoid lipids and membranes (Kellermann, Yoshinaga, Valentine, Wormer, & Valentine, ), rhodopsins (Grote & O'Malley, ), resistance to UV‐induced DNA damage (Jones & Baxter, ), gene transcription and regulation (Yoon et al, ), motility via archaella (Kinosita, Uchida, Nakane, & Nishizaka, ), biofilm formation (Fröls, Dyall‐Smith, & Pfeifer, ), halovirus biology (Stolt & Zillig, ), and even astrobiology (Leuko, Domingos, Parpart, Reitz, & Rettberg, ). Unusual features of this species are the high level of genetic variation, due mainly to the presence and activity of numerous ISH elements (Brugger et al, ), and the high GC content of the main chromosome (~68%) compared to their plasmids (57%–60% G + C) (Grant et al, ; Ng et al, ; Pfeiffer, Schuster, et al, ).…”