4.8 Article

Functional compartmentalization and metabolic separation in a prokaryotic cell

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.2022114118

Keywords

Archaea; compartmentalization; CO2 fixation; immunogold labeling

Funding

  1. Deutsche Forschungsgemeinschaft [HU703/2]

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Prokaryotic cells are more complex than traditionally believed, with various microcompartments encapsulating metabolic enzymes or pathways. The hyperthermophilic Crenarchaeon Ignicoccus hospitalis possesses unique structures like two membranes and an unknown intermembrane compartment. The compartmentalization of metabolic pathways and information processes in this organism represents a unique example in the prokaryotic world.
The prokaryotic cell is traditionally seen as a bag of enzymes, yet its organization is much more complex than in this simplified view. By now, various microcompartments encapsulating metabolic enzymes or pathways are known for Bacteria. These microcompartments are usually small, encapsulating and concentrating only a few enzymes, thus protecting the cell from toxic intermediates or preventing unwanted side reactions. The hyperthermophilic, strictly anaerobic Crenarchaeon Ignicoccus hospitalis is an extraordinary organism possessing two membranes, an inner and an energized outer membrane. The outer membrane (termed here outer cytoplasmic membrane) harbors enzymes involved in proton gradient generation and ATP synthesis. These two membranes are separated by an intermembrane compartment, whose function is unknown. Major information processes like DNA replication, RNA synthesis, and protein biosynthesis are located inside the cytoplasm or central cytoplasmic compartment. Here, we show by immunogold labeling of ultrathin sections that enzymes involved in autotrophic CO2 assimilation are located in the intermembrane compartment that we name (now) a peripheric cytoplasmic compartment. This separation may protect DNA and RNA from reactive aldehydes arising in the I. hospitalis carbon metabolism. This compartmentalization of metabolic pathways and information processes is unprecedented in the prokaryotic world, representing a unique example of spatiofunctional compartmentalization in the second domain of life.

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