Adaptations of archaeal and bacterial membranes to variations in temperature,pH and pressure

The cytoplasmic membrane of a prokaryotic cell consists of a lipid bilayer or a monolayer that shields the cellular content from the environment. In addition, the membrane contains proteins that are responsible for transport of proteins and metabolites as well as for signalling and energy transduction. Maintenance of the functionality of the membrane during changing environmental conditions relies on the cell’s potential to rapidly adjust the lipid composition of its membrane. Despite the fundamental chemical differences between bacterial ester lipids and archaeal ether lipids, both types are functional under a wide range of environmental conditions. We here provide an overview of archaeal and bacterial strategies of changing the lipid compositions of their membranes. Some molecular adjustments are unique for archaea or bacteria, whereas others are shared between the two domains. Strikingly, shared adjustments were predominantly observed near the growth boundaries of bacteria. Here, we demonstrate that the presence of membrane spanning ether-lipids and methyl branches shows a striking relationship with the growth boundaries of archaea and bacteria.

     

Recent advances in structural research on ether lipids from archaea including comparative and physiological aspects

A great number of novel and unique chemical structures of archaeal polar lipids have been reported. Since 1993, when those lipids were reviewed in several review articles, a variety of core lipids and lipids with unique polar groups have been reported successively. We summarize new lipid structures from archaea elucidated after 1993. In addition to lipids from intact archaeal cells, more diverse structures of archaea-related lipids found in environmental samples are also reviewed. These lipids are assumed to be lipids from unidentified or ancient archaea or related organisms. In the second part of this paper, taxonomic and ecological aspects are discussed. Another aspect of archaeal lipid study has to do with its physiological significance, particularly the phase behavior and permeability of archaeal lipid membranes in relation to the thermophily of many archaea. In the last part of this review we discuss this problem.     

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

A great number of novel and unique chemical structures of archaeal polar lipids have been reported. Since 1993, when those lipids were reviewed in several review articles, a variety of core lipids and lipids with unique polar groups have been reported successively. We summarize new lipid structures from archaea elucidated after 1993. In addition to lipids from intact archaeal cells, more diverse structures of archaea-related lipids found in environmental samples are also reviewed. These lipids are assumed to be lipids from unidentified or ancient archaea or related organisms. In the second part of this paper, taxonomic and ecological aspects are discussed. Another aspect of archaeal lipid study has to do with its physiological significance, particularly the phase behavior and permeability of archaeal lipid membranes in relation to the thermophily of many archaea. In the last part of this review we discuss this problem.     

The archaeal cell envelope

At first glance, archaea and bacteria look alike; however, the composition of the archaeal cell envelope is fundamentally different from the bacterial cell envelope. With just one exception, all archaea characterized to date have only a single membrane and most are covered by a paracrystalline protein layer. This Review discusses our current knowledge of the composition of the archaeal cell surface. We describe the wide range of cell wall polymers, O- and N-glycosylated extracellular proteins and other cell surface structures that archaea use to interact with their environment.     

Origins and evolution of isoprenoid lipid biosynthesis in archaea

A characteristic feature of the domain archaea are the lipids forming the hydrophobic core of their cell membrane. These unique lipids are composed of isoprenoid side-chains stereospecifically ether linked to sn-glycerol-1-phosphate. Recently, considerable progress has been made in characterizing the enzymes responsible for the synthesis of archaeal lipids. However, little is known about their evolution. To better understand how this unique biosynthetic apparatus came to be, large-scale database surveys and phylogenetic analyses were performed. All characterized enzymes involved in the biosynthesis of isoprenoid side-chains and the glycerol phosphate backbone along with their assembly in ether lipids were included in these analyses. The sequence data available in public databases was complemented by an in-depth sampling of isoprenoid lipid biosynthesis genes from multiple genera of the archaeal order Halobacteriales, allowing us to look at the evolution of these enzymes on a smaller phylogenetic scale. This investigation of the isoprenoid biosynthesis apparatus of archaea on small and large phylogenetic scales reveals that it evolved through a combination of evolutionary processes, including the co-option of ancestral enzymes, modification of enzymatic specificity, orthologous and non-orthologous gene displacement, integration of components from eukaryotes and bacteria and lateral gene transfer within and between archaeal orders.     

Diversity of archaeal type IV pilin-like structures

Bacterial type IV pili perform important functions in such disparate biological processes as surface adhesion, cell–cell interactions, autoaggregation, conjugation, and twitching motility. Unlike bacteria, archaea use a type IV pilus related structure to drive swimming motility. While this unique flagellum is the best-studied example of an archaeal IV pilus-like structure, recent in silico, in vivo and structural analyses have revealed a highly diverse set of archaeal non-flagellar type IV pilus-like structures. Accumulating evidence suggests that these structures play important diverse roles in archaea.     

Comparative genomic analysis of archaeal genotypic variants in a single population and in two different oceanic provinces.

Planktonic crenarchaeotes are present in high abundance in Antarctic winter surface waters, and they also make up a large proportion of total cell numbers throughout deep ocean waters. To better characterize these uncultivated marine crenarchaeotes, we analyzed large genome fragments from individuals recovered from a single Antarctic picoplankton population and compared them to those from a representative obtained from deeper waters of the temperate North Pacific. Sequencing and analysis of the entire DNA insert from one Antarctic marine archaeon (fosmid 74A4) revealed differences in genome structure and content between Antarctic surface water and temperate deepwater archaea. Analysis of the predicted gene products encoded by the 74A4 sequence and those derived from a temperate, deepwater planktonic crenarchaeote (fosmid 4B7) revealed many typical archaeal proteins but also several proteins that so far have not been detected in archaea. The unique fraction of marine archaeal genes included, among others, those for a predicted RNA-binding protein of the bacterial cold shock family and a eukaryote-type Zn finger protein. Comparison of closely related archaea originating from a single population revealed significant genomic divergence that was not evident from 16S rRNA sequence variation. The data suggest that considerable functional diversity may exist within single populations of coexisting microbial strains, even those with identical 16S rRNA sequences. Our results also demonstrate that genomic approaches can provide high-resolution information relevant to microbial population genetics, ecology, and evolution, even for microbes that have not yet been cultivated.     

Comparative Genomic Analysis of Archaeal Genotypic Variants in a Single Population and in Two Different Oceanic Provinces

Planktonic crenarchaeotes are present in high abundance in Antarctic winter surface waters, and they also make up a large proportion of total cell numbers throughout deep ocean waters. To better characterize these uncultivated marine crenarchaeotes, we analyzed large genome fragments from individuals recovered from a single Antarctic picoplankton population and compared them to those from a representative obtained from deeper waters of the temperate North Pacific. Sequencing and analysis of the entire DNA insert from one Antarctic marine archaeon (fosmid 74A4) revealed differences in genome structure and content between Antarctic surface water and temperate deepwater archaea. Analysis of the predicted gene products encoded by the 74A4 sequence and those derived from a temperate, deepwater planktonic crenarchaeote (fosmid 4B7) revealed many typical archaeal proteins but also several proteins that so far have not been detected in archaea. The unique fraction of marine archaeal genes included, among others, those for a predicted RNA-binding protein of the bacterial cold shock family and a eukaryote-type Zn finger protein. Comparison of closely related archaea originating from a single population revealed significant genomic divergence that was not evident from 16S rRNA sequence variation. The data suggest that considerable functional diversity may exist within single populations of coexisting microbial strains, even those with identical 16S rRNA sequences. Our results also demonstrate that genomic approaches can provide high-resolution information relevant to microbial population genetics, ecology, and evolution, even for microbes that have not yet been cultivated.     

炭疽杆菌S层的研究进展

S层是广泛存在于古细菌和真细菌细胞壁最外层的结构独特、功能特殊的成分,对它的研究具有重要的意义。炭疽杆菌是引起人畜炭疽病的病原体,对其S层的研究将为深入认识该菌的生理特性及致病机制等提供坚实的基础。就近年来对炭疽杆菌S层的结构、功能特点及应用前景等方面的研究进展做一简要的综述。     

The archaeal cell cycle: current issues

The recently discovered structural similarities between the archaeal Orc1/Cdc6 and bacterial DnaA initiator proteins for chromosome replication have exciting implications for cell cycle regulation. Together with current attempts to identify archaeal chromosome replication origins, the information is likely to yield fundamental insights into replication control in both archaea and eukaryotes within the near future. Several proteins that affect, or are likely to affect, chromatin structure and genome segregation in archaea have been described recently, including Sph1 and 2, ScpA and B, Sir2, Alba and Rio1p. Important insights into the properties of the MinD and FtsZ cell division proteins, and of putative cytoskeletal elements, have recently been gained in bacteria. As these proteins also are present among archaea, it is likely that the new information will also be essential for understanding archaeal genome segregation and cell division. A series of interesting cell cycle issues has been brought to light through the discovery of the novel Nanoarchaeota phylum, and these are outlined briefly. Exciting areas for extended cell cycle investigations of archaea are identified, including termination of chromosome replication, application of in situ cytological techniques for localization of cell cycle proteins and the regulatory roles of GTP-binding proteins and small RNAs.     

Ether Lipids of Planktonic Archaea in the Marine Water Column

Acyclic and cyclic biphytanes derived from the membrane ether lipids of archaea were found in water column particulate and sedimentary organic matter from several oxic and anoxic marine environments. Compound-specific isotope analyses of the carbon skeletons suggest that planktonic archaea utilize an isotopically heavy carbon source such as algal carbohydrates and proteins or dissolved bicarbonate. Due to their high preservation potential, these lipids provide a fossil record of planktonic archaea and suggest that they have thrived in marine environments for more than 50 million years.     

PII signaling proteins of cyanobacteria and green algae. New features of conserved proteins

The characteristics of signal PII proteins identified in bacteria, archaea, and plants are presented. Special attention is paid to the properties and functions of PII proteins in microorganisms with oxygenic photosynthesis type: cyanobacteria and unicellular green algae. The structure and regulation of PII proteins are reviewed. The mechanisms of interactions of PII proteins with effectors and cellular targets are analyzed in detail. The conservative properties and unique characteristics of proteins from representatives of pro-and eukaryotic phototrophs are discussed.     

Virion architecture unifies globally distributed pleolipoviruses infecting halophilic archaea

Our understanding of the third domain of life, Archaea, has greatly increased since its establishment some 20 years ago. The increasing information on archaea has also brought their viruses into the limelight. Today, about 100 archaeal viruses are known, which is a low number compared to the numbers of characterized bacterial or eukaryotic viruses. Here, we have performed a comparative biological and structural study of seven pleomorphic viruses infecting extremely halophilic archaea. The pleomorphic nature of this novel virion type was established by sedimentation analysis and cryo-electron microscopy. These nonlytic viruses form virions characterized by a lipid vesicle enclosing the genome, without any nucleoproteins. The viral lipids are unselectively acquired from host cell membranes. The virions contain two to three major structural proteins, which either are embedded in the membrane or form spikes distributed randomly on the external membrane surface. Thus, the most important step during virion assembly is most likely the interaction of the membrane proteins with the genome. The interaction can be driven by single-stranded or double-stranded DNA, resulting in the virions having similar architectures but different genome types. Based on our comparative study, these viruses probably form a novel group, which we define as pleolipoviruses.     

Archaeal phospholipids: Structural properties and biosynthesis

Phospholipids are major components of the cellular membranes present in all living organisms. They typically form a lipid bilayer that embroiders the cell or cellular organelles, constitute a barrier for ions and small solutes and form a matrix that supports the function of membrane proteins. The chemical composition of the membrane phospholipids present in the two prokaryotic domains Archaea and Bacteria are vastly different. Archaeal lipids are composed of highly-methylated isoprenoid chains that are ether-linked to a glycerol-1-phosphate backbone while bacterial phospholipids consist of straight fatty acids bound by ester bonds to the enantiomeric glycerol-3-phosphate backbone. The chemical structure of the archaeal lipids and their compositional diversity ensures the required stability at extreme environmental conditions as many archaea thrive at such conditions including high or low temperature, high salinity and extreme acidic or alkaline pH values. However, not all archaea are extremophiles, and the presence of ether-linked phospholipids is a phylogenetic marker that distinguishes Archaea from other life forms. During the past decade, our understanding of the biosynthesis of archaeal lipids has progressed resulting in the characterization of the main biosynthetic steps of the pathway including the reconstitution of lipid biosynthesis in vitro. Here we describe the chemical and physical properties of archaeal lipids and membranes derived thereof, summarize the existing knowledge about the enzymology of the archaeal lipid biosynthetic pathway and discuss evolutionary theories associated with the “Lipid Divide” that resulted in the differentiation of bacterial and archaeal organisms. This article is part of a Special Issue entitled: Bacterial Lipids edited by Russell E. Bishop.     

S-layers as a tool kit for nanobiotechnological applications

Crystalline bacterial cell surface layers (S-layers) have been identified in a great number of different species of bacteria and represent an almost universal feature of archaea. Isolated native S-layer proteins and S-layer fusion proteins incorporating functional sequences self-assemble into monomolecular crystalline arrays in suspension, on a great variety of solid substrates and on various lipid structures including planar membranes and liposomes. S-layers have proven to be particularly suited as building blocks and patterning elements in a biomolecular construction kit involving all major classes of biological molecules (proteins, lipids, glycans, nucleic acids and combinations of them) enabling innovative approaches for the controlled 'bottom-up' assembly of functional supramolecular structures and devices. Here, we review the basic principles of S-layer proteins and the application potential of S-layers in nanobiotechnology and biomimetics including life and nonlife sciences.     

Murein and pseudomurein cell wall binding domains of bacteria and archaea—a comparative view

The cell wall, a major barrier protecting cells from their environment, is an essential compartment of both bacteria and archaea. It protects the organism from internal turgor pressure and gives a defined shape to the cell. The cell wall serves also as an anchoring surface for various proteins and acts as an adhesion platform for bacteriophages. The walls of bacteria and archaea are mostly composed of murein and pseudomurein, respectively. Cell wall binding domains play a crucial role in the non-covalent attachment of proteins to cell walls. Here, we give an overview of the similarities and differences in the biochemical and functional properties of the two major murein and pseudomurein cell wall binding domains, i.e., the Lysin Motif (LysM) domain (Pfam PF01476) and the pseudomurein binding (PMB) domain (Pfam PF09373) of bacteria and archaea, respectively.     

Structural and physicochemical properties of polar lipids from thermophilic archaea

The essential general features required for lipid membranes of extremophilic archaea to fulfill biological functions are that they are in the liquid crystalline phase and have extremely low permeability of solutes that is much less temperature sensitive due to a lack of lipid-phase transition and highly branched isoprenoid chains. Many accumulated data indicate that the organism’s response to extremely low pH is the opposite of that to high temperature. The high temperature adaptation does not require the tetraether lipids, while the adaptation of thermophiles to acidic environment requires the tetraether polar lipids. The presence of cyclopentane rings and the role of polar heads are not so straightforward regarding the correlations between fluidity and permeability of the lipid membrane. Due to the unique lipid structures and properties of archaeal lipids, they are a valuable resource in the development of novel biotechnological processes. This microreview focuses primarily on structural and physicochemical properties of polar lipids of (hyper)thermophilic archaea.     

Assembly and mechanisms of bacterial type IV secretion machines

Type IV secretion occurs across a wide range of prokaryotic cell envelopes: Gram-negative, Gram-positive, cell wall-less bacteria and some archaea. This diversity is reflected in the heterogeneity of components that constitute the secretion machines. Macromolecules are secreted in an ATP-dependent process using an envelope-spanning multi-protein channel. Similar to the type III systems, this apparatus extends beyond the cell surface as a pilus structure important for direct contact and penetration of the recipient cell surface. Type IV systems are remarkably versatile in that they mobilize a broad range of substrates, including single proteins, protein complexes, DNA and nucleoprotein complexes, across the cell envelope. These machines have broad clinical significance not only for delivering bacterial toxins or effector proteins directly into targeted host cells, but also for direct involvement in phenomena such as biofilm formation and the rapid horizontal spread of antibiotic resistance genes among the microbial community.     

Caveolae: Formation,dynamics, and function

Caveolae are abundant surface pits formed by the assembly of cytoplasmic proteins on a platform generated by caveolin integral membrane proteins and membrane lipids. This membranous assembly can bud off into the cell or can be disassembled releasing the cavin proteins into the cytosol. Disassembly can be triggered by increased membrane tension, or by stress stimuli, such as UV. Here, we discuss recent mechanistic studies showing how caveolae are formed and how their unique properties allow them to function as multifunctional protective and signaling structures.