Chemical structure of the cell wall polymer of methanosarcina

Kreisl, Peter; Kandler, Otto

doi:10.1016/s0723-2020(86)80022-4

Cited by 81 publications

(33 citation statements)

References 32 publications

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“…When grown on freshwater medium, this species grows as large multicellular aggregates embedded in a heteropolysaccharide matrix (Fig. 1A) composed primarily of D-galactosamine and D-glucuronic acid, termed methanochondroitin (24), whereas in marine medium these species grow as individual cells surrounded only by a protein cell surface layer (S layer) (38). This isolate has been one of the methanosarcinal strains most frequently studied for the physiology, biochemistry, and bioenergetics of methanogenesis (39).…”

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The Methanosarcina barkeri Genome: Comparative Analysis with Methanosarcina acetivorans and Methanosarcina mazei Reveals Extensive Rearrangement within Methanosarcinal Genomes

et al. 2006

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We report here a comparative analysis of the genome sequence of Methanosarcina barkeri with those of Methanosarcina acetivorans and Methanosarcina mazei. The genome of M. barkeri is distinguished by having an organization that is well conserved with respect to the other Methanosarcina spp. in the region proximal to the origin of replication, with interspecies gene similarities as high as 95%. However, it is disordered and marked by increased transposase frequency and decreased gene synteny and gene density in the distal semigenome. Of the 3,680 open reading frames (ORFs) in M. barkeri, 746 had homologs with better than 80% identity to both M. acetivorans and M. mazei, while 128 nonhypothetical ORFs were unique (nonorthologous) among these species, including a complete formate dehydrogenase operon, genes required for N-acetylmuramic acid synthesis, a 14-gene gas vesicle cluster, and a bacterial-like P450-specific ferredoxin reductase cluster not previously observed or characterized for this genus. A cryptic 36-kbp plasmid sequence that contains an orc1 gene flanked by a presumptive origin of replication consisting of 38 tandem repeats of a 143-nucleotide motif was detected in M. barkeri. Three-way comparison of these genomes reveals differing mechanisms for the accrual of changes. Elongation of the relatively large M. acetivorans genome is the result of uniformly distributed multiple gene scale insertions and duplications, while the M. barkeri genome is characterized by localized inversions associated with the loss of gene content. In contrast, the short M. mazei genome most closely approximates the putative ancestral organizational state of these species.Biological methanogenesis by the methane-producing archaea has a significant role in the global carbon cycle. This process is one of several anaerobic degradative processes that complement aerobic degradation by utilizing alternative electron acceptors in habitats where O 2 is not available (39). The efficiency of this microbial process is directly dependent upon the interaction of three metabolically distinct groups of microorganisms: the fermentative and acetogenic bacteria and the methanogenic archaea. The methanogenic archaea have two pivotal roles in methanogenic consortia (28). By consuming hydrogen for methanogenesis and effectively lowering its partial pressure by the process of interspecies hydrogen exchange, the methanogens provide a thermodynamically favorable environment for the fermentative and acetogenic species to utilize protons as electron acceptors. This interaction enables fermenters to conserve more energy by producing a more oxidized product, acetate, which is also a substrate for methanogenesis. The second role of the methanogens is the fermentation of acetate, which accounts for 70% of the global methane produced by biological methane production (28). The net effect of these microbial interactions is the diversion of protons to hydrogen and carbon to acetate, which ultimately yields methane and carbon dioxide via methanogenesis.The genus M...

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The Methanosarcina barkeri Genome: Comparative Analysis with Methanosarcina acetivorans and Methanosarcina mazei Reveals Extensive Rearrangement within Methanosarcinal Genomes

et al. 2006

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“…The latter are globular structures with zonal heterogeneity and intercellular connective material that extends the outer surface of the packets and wraps the cells together. This connective material is composed chiefly of a heteropolysaccharide (14,16) which confers to the packets resistance to traumas of various types: mechanical, physical (e.g., heat), and chemical (unpublished observations). This resistance is in contrast to the relative fragility of lamina (25) and especially to the fragility of single cells (9).…”

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Archaeal grpE: transcription in two different morphologic stages of Methanosarcina mazei and comparison with dnaK and dnaJ

1995

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Transcription of the heat shock gene grpE was studied in two different morphologic stages of the archaeon Methanosarcina mazei S-6 that differ in resistance to physical and chemical traumas: single cells and packets. While single cells are directly exposed to environmental changes, such as temperature elevations, cells in packets are surrounded by intercellular and peripheral material that keeps them together in a globular structure which can reach several millimeters in diameter. grpE transcript levels determined by Northern (RNA) blotting peaked after a 15-min heat shock in single cells. In contrast, the highest transcript levels in packets were observed after the longest heat shock tested, 60 min. The same response profiles were demonstrated by primer extension experiments and S1 nuclease analysis. A comparison of the grpE response to heat shock with those of dnaK and dnaJ showed that the grpE transcript level was the most increased, closely followed by that of the dnaK transcript, with that of the dnaJ gene being the least augmented. Transcription of grpE started at the same site under normal and heat shock temperatures, and the transcript was consistently ϳ700 bases long. Codon usage patterns revealed that the three archaeal genes use most codons and have the same codon preference for 61% of the amino acids.A gene encoding a GrpE homolog has recently been cloned from the genome of the archaeon Methanosarcina mazei S-6 and sequenced (6). It is the first example of a grpE heat shock gene found within the domain Archaea. The Archaea are organisms phylogenetically distinct from Bacteria (eubacteria) and Eucarya (eucaryotes) (41). However, Archaea resemble eucaryotes in several molecular biological features more than they resemble bacteria and are closer to eucaryotes than bacteria (15,28,30,31,41). A case in point is gene regulation, since there are data indicating that Archaea use a transcription regulation machinery similar to that of eucaryotes (10,24,28,33). Whether this is the case also for archaeal heat shock genes has not been established. To address this question, it is necessary to first determine the expression pattern of the known archaeal heat shock genes and then proceed to analyze the regulation mechanisms at the molecular level.Among the Archaea, M. mazei is particularly interesting because it is one of a small group of organisms, the methanosarcinae (22,23), that undergo a growth cycle with morphologic conversions (3,25,32,42). The cycle includes a unicellular form or stage, named single cells, and two multicellular forms, called lamina and packets. The latter are globular structures with zonal heterogeneity and intercellular connective material that extends the outer surface of the packets and wraps the cells together. This connective material is composed chiefly of a heteropolysaccharide (14, 16) which confers to the packets resistance to traumas of various types: mechanical, physical (e.g., heat), and chemical (unpublished observations). This resistance is in contrast to the relative fragilit...

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“…There are other features of methanosarcinae that remind one of higher organisms, such as the cell wall polymer methanochondroitin, which closely resembles eukaryotic chondroitin (14,15). Also, Methanosarcina gene organization, although typically prokaryotic, shows conserved molecules involved in replication, transcription, and translation with a higher degree of homology to those of eukaryotes than to those of eubacteria (4,33,37).…”

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Lamina, a novel multicellular form of Methanosarcina mazei S-6

Mayerhofer

Macario

1992

J Bacteriol

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A novel multicellular form of Methanosarcina mazei S-6 is described. It was termed lamina, and it formed during the exponential growth phase when packets or single cells were grown in 40 mM trimethylamine and a total concentration of 8.3 to 15.6 mM Ca2`and/or Mg2+, in cultures that were not shaken. A distinct molecular event represented by the increment in expression and a spatial redistribution of an antigen during lamina formation is documented.Methanosarcinae are the only members of the archaebacterial domain, Archaea (33, 34), for which uni-and multicellular forms have been observed (20,26,29,31), suggesting an underlying complexity in gene regulation not hitherto observed in other archaebacteria. There are other features of methanosarcinae that remind one of higher organisms, such as the cell wall polymer methanochondroitin, which closely resembles eukaryotic chondroitin (14, 15). Also, Methanosarcina gene organization, although typically prokaryotic, shows conserved molecules involved in replication, transcription, and translation with a higher degree of homology to those of eukaryotes than to those of eubacteria (4,33,37).Among methanosarcinae, Methanosarcina mazei S-6 (20, 21) is one of the better-studied species in pure culture concerning different morphologies-i.e., single cells and small and large packets (1,12,26,27,35). These morphologies have also been observed in complex ecosystems like anaerobic bioreactors (18). Different morphologies allow analysis from various perspectives. Packets of M. mazei S-6 can easily be monitored in different types of anaerobic bioreactors (18,19), whereas single cells facilitate molecular biologic studies (12). In addition, the multicellular structures in M. mazei S-6 afford the opportunity to examine cell-cell interaction in archaebacteria.The use of monoclonal antibodies has proven to be a powerful tool for examining developmentally regulated antigens in both prokaryotic and eukaryotic systems (5, 10). Investigations of the cell surface's architecture and antigenic mosaic of methanosarcinae have revealed antigens whose expression is associated with morphology (22, 23), and thus these antigens can be useful as markers in the study of temporal gene expression during morphologic changes. A multicellular form of M. mazei S-6, which we have termed lamina, and the temporal variations of a cell surface antigen (AgIc) paralleling the morphological rearrangements involved in lamina formation are described here. The word lamina best illustrates the structure's distinctive morphologic feature, i.e., its flat shape observed macro-and microscopically, its thickness being minimal in comparison with its length and width. Monoclonal antibody IC (MAbIC) generated and characterized as described previously (9, 17) was used for immunologic assays. The presence of antigen (AgIc) in sections of M. mazei S-6 was detected with MAbIC by immunohistochemistry and indirect immunofluorescence (6,7,13 (Fig. la). These packets were inoculated into medium containing 40

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Chemical structure of the cell wall polymer of methanosarcina

Cited by 81 publications

References 32 publications

The Methanosarcina barkeri Genome: Comparative Analysis with Methanosarcina acetivorans and Methanosarcina mazei Reveals Extensive Rearrangement within Methanosarcinal Genomes

The Methanosarcina barkeri Genome: Comparative Analysis with Methanosarcina acetivorans and Methanosarcina mazei Reveals Extensive Rearrangement within Methanosarcinal Genomes

Archaeal grpE: transcription in two different morphologic stages of Methanosarcina mazei and comparison with dnaK and dnaJ

Lamina, a novel multicellular form of Methanosarcina mazei S-6

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