Dataset Information

Structure of the surface layer of the methanogenic archaean Methanosarcina acetivorans.

ABSTRACT: Archaea have a self-assembling proteinaceous surface (S-) layer as the primary and outermost boundary of their cell envelopes. The S-layer maintains structural rigidity, protects the organism from adverse environmental elements, and yet provides access to all essential nutrients. We have determined the crystal structure of one of the two "homologous" tandem polypeptide repeats that comprise the Methanosarcina acetivorans S-layer protein and propose a high-resolution model for a microbial S-layer. The molecular features of our hexameric S-layer model recapitulate those visualized by medium resolution electron microscopy studies of microbial S-layers and greatly expand our molecular view of S-layer dimensions, porosity, and symmetry. The S-layer model reveals a negatively charged molecular sieve that presents both a charge and size barrier to restrict access to the cell periplasmic-like space. The ?-sandwich folds of the S-layer protein are structurally homologous to eukaryotic virus envelope proteins, suggesting that Archaea and viruses have arrived at a common solution for protective envelope structures. These results provide insight into the evolutionary origins of primitive cell envelope structures, of which the S-layer is considered to be among the most primitive: it also provides a platform for the development of self-assembling nanomaterials with diverse functional and structural properties.

SUBMITTER: Arbing MA

PROVIDER: S-EPMC3406845 | biostudies-literature | 2012 Jul

REPOSITORIES: biostudies-literature

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Structure of the surface layer of the methanogenic archaean Methanosarcina acetivorans.

Arbing Mark A MA Chan Sum S Shin Annie A Phan Tung T Ahn Christine J CJ Rohlin Lars L Gunsalus Robert P RP

Proceedings of the National Academy of Sciences of the United States of America 20120702 29

Archaea have a self-assembling proteinaceous surface (S-) layer as the primary and outermost boundary of their cell envelopes. The S-layer maintains structural rigidity, protects the organism from adverse environmental elements, and yet provides access to all essential nutrients. We have determined the crystal structure of one of the two "homologous" tandem polypeptide repeats that comprise the Methanosarcina acetivorans S-layer protein and propose a high-resolution model for a microbial S-layer ...[more]

PMID: 22753492

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Project description:UnlabelledResults are presented supporting a regulatory role for the product of the MA3302 gene locus (designated MreA) previously annotated as a hypothetical protein in the methanogenic species Methanosarcina acetivorans of the domain Archaea. Sequence analysis of MreA revealed identity to the TrmB family of transcription factors, albeit the sequence is lacking the sensor domain analogous to TrmBL2, abundant in nonmethanogenic species of the domain Archaea. Transcription of mreA was highly upregulated during growth on acetate versus methylotrophic substrates, and an mreA deletion (?mreA) strain was impaired for growth with acetate in contrast to normal growth with methylotrophic substrates. Transcriptional profiling of acetate-grown cells identified 280 genes with altered expression in the ?mreA strain versus the wild-type strain. Expression of genes unique to the acetate pathway decreased whereas expression of genes unique to methylotrophic metabolism increased in the ?mreA strain relative to the wild type, results indicative of a dual role for MreA in either the direct or indirect activation of acetate-specific genes and repression of methylotrophic-specific genes. Gel shift experiments revealed specific binding of MreA to promoter regions of regulated genes. Homologs of MreA were identified in M. acetivorans and other Methanosarcina species for which expression patterns indicate roles in regulating methylotrophic pathways.ImportanceSpecies in the domain Archaea utilize basal transcription machinery resembling that of the domain Eukarya, raising questions addressing the role of numerous putative transcription factors identified in sequenced archaeal genomes. Species in the genus Methanosarcina are ideally suited for investigating principles of archaeal transcription through analysis of the capacity to utilize a diversity of substrates for growth and methanogenesis. Methanosarcina species switch pathways in response to the most energetically favorable substrate, metabolizing methylotrophic substrates in preference to acetate marked by substantial regulation of gene expression. Although conversion of the methyl group of acetate accounts for most of the methane produced in Earth's biosphere, no proteins involved in the regulation of genes in the acetate pathway have been reported. The results presented here establish that MreA participates in the global regulation of diverse methanogenic pathways in the genus Methanosarcina. Finally, the results contribute to a broader understanding of transcriptional regulation in the domain Archaea.

Dataset Information

Structure of the surface layer of the methanogenic archaean Methanosarcina acetivorans.

Publications

Structure of the surface layer of the methanogenic archaean Methanosarcina acetivorans.

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