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Formation and function of bacterial organelles

Abstract

Advances in imaging technologies have revealed that many bacteria possess organelles with a proteomically defined lumen and a macromolecular boundary. Some are bound by a lipid bilayer (such as thylakoids, magnetosomes and anammoxosomes), whereas others are defined by a lipid monolayer (such as lipid bodies), a proteinaceous coat (such as carboxysomes) or have a phase-defined boundary (such as nucleolus-like compartments). These diverse organelles have various metabolic and physiological functions, facilitating adaptation to different environments and driving the evolution of cellular complexity. This Review highlights that, despite the diversity of reported organelles, some unifying concepts underlie their formation, structure and function. Bacteria have fundamental mechanisms of organelle formation, through which conserved processes can form distinct organelles in different species depending on the proteins recruited to the luminal space and the boundary of the organelle. These complex subcellular compartments provide evolutionary advantages as well as enabling metabolic specialization, biogeochemical processes and biotechnological advances. Growing evidence suggests that the presence of organelles is the rule, rather than the exception, in bacterial cells.

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Fig. 1: Structural and functional diversity of bacterial organelles.
Fig. 2: Formation of membrane-bound organelles.
Fig. 3

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Acknowledgements

Work in the authors’ labs is supported by NHMRC EL2 Fellowship 1178715 (to C.G.) and NHMRC Program Grant 1092262 (to T.L.). The authors thank Christopher Stubenrauch and Chaille Webb for critical comments on the manuscript and Rhys Grinter for assistance with figure preparation.

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Glossary

Phase-defined

In cases of high concentration of nucleic acids (or specific proteins) a phase separation can be observed in the cytoplasm that results in a partitioning of specific proteins that either prefer or disfavour the conditions of each phase. A notable example is the nucleolus in eukaryotes and the ribonucleoprotein granules found in bacteria such as Caulobacter crescentus.

Carboxysomes

Anabolic bacterial microcompartments that have a polyhedral protein shell and a lumen filled with the CO2-fixing enzyme RuBisCO. Examples include the β-carboxysomes of the phototroph Synechococcus elongatus and the α-carboxysomes of the lithotroph Acidithiobacillus spp.

Thylakoids

Membrane-bound organelle that mediates light-harvesting and energy transduction in photosynthetic cyanobacteria. Through evolutionary links, thylakoids are also one of the three membrane systems found in the chloroplasts of eukaryotes.

Metabolosomes

Catabolic bacterial microcompartments bound by polyhedral protein shells and housing enzymes to oxidize a specific metabolite. Notable examples include the organelles that metabolize propanediol or ethanolamine in various bacteria and archaea, including Salmonella enterica.

Acidocalcisomes

First identified in single-celled eukaryotes, these organelles have a single membrane boundary. A pH gradient across the membrane is generated by a proton-translocating pyrophosphatase, providing an acidic, phosphate-rich lumen that can accommodate excess cellular calcium. Typical examples are found in Alphaproteobacteria such as Agrobacterium tumefaciens.

Mitochondria

Eukaryotic organelles with two membrane systems that primarily mediate ATP synthesis through aerobic respiration. Derived through endosymbiosis of an alphaproteobacterial cell.

Chloroplasts

Plastids are organelles with three membrane systems found in eukaryotes, with the chloroplast being defined as a type of plastid mediating oxygenic photosynthesis in plants and algae. Derived through endosymbiosis of a cyanobacterial cell.

Magnetosomes

Membrane-bound organelles that contain a lumen filled with magnetic iron oxide or iron sulfide crystals, which enable bacteria, such as Magnetospirillum gryphiswaldense, to orient towards magnetic fields and, in turn, mediate aerotaxis.

Chromatophores

Membrane-bound organelles that function in light harvesting and energy transduction during anoxygenic photosynthesis. Examples are found in Alphaproteobacteria such as Rhodobacter sphaeroides.

Anammoxosomes

Large membrane-bound organelles containing enzymes for anaerobic ammonium oxidation in the lumen and associated energy transduction in the membrane. Exclusively found in anammox Planctomycetes such as Kuenenia stuttgartiensis.

Nucleoid

Region within bacterial cells defined by the compacted genome. These regions are often phase-separated from the surrounding cytoplasm and therefore contain a distinct population of proteins.

Nitrate vacuoles

Giant membrane-bound organelles that store the anaerobic electron acceptor nitrate and found in various sulfur-oxidizing, nitrate-reducing Gammaproteobacteria such as Thioploca araucae.

Ferrosomes

A recently discovered group of small membrane-bound organelles that store iron, including in iron-reducing bacteria such as Shewanella putrefaciens.

Mitosomes

Organelles with two membrane systems found in some single-celled eukaryotes, notably in the genera Giardia and Entamoeba, containing luminal enzymes required for the biosynthesis of iron–sulfur clusters. These organelles are functionally specialized derivatives of mitochondria.

Hydrogenosomes

Organelles with two membrane systems found in some anaerobic protists, fungi and animals. They contain luminal enzymes that produce ATP via fermentation, resulting in the production of end products such as hydrogen gas. These organelles are functionally specialized derivatives of mitochondria.

Peroxisomes

Organelles found in many animals and fungi, containing luminal enzymes required for oxidative reactions such as lipid biosynthesis and detoxification reactions. These single-membrane-bound organelles are evolutionarily related to glycosomes and glyoxysomes.

Glycosomes

Organelles found in trypanosomes and other single-celled eukaryotes, containing enzymes required for glycolysis in their lumen. These single-membrane-bound organelles are functionally specialized derivatives of peroxisomes.

Glyoxysomes

Organelles found in many plants and some other eukaryotes, containing in the lumen the enzymes required for the glyoxylate cycle. These single-membrane-bound organelles are functionally specialized derivatives of peroxisomes.

Nanocompartments

Minimalistic organelles containing a polyhedral shell made of the protein encapsulin and a lumen containing targeted cargo proteins. These organelles are widespread in bacteria and archaea, for example, supporting oxidative stress responses in Mycobacterium tuberculosis.

Gas vesicles

Protein-bound compartments that function in buoyancy for bacterial and archaeal cells, for example, to position photosynthetic bacteria in a water column to access optimal light levels; also known as gas vacuoles.

Carbonosomes

A recently defined organelle that stores polyhydroxyalkanoates and potentially other carbon storage compounds; thought to be bound by proteins rather than phospholipids.

Chlorosomes

Efficient light-harvesting organelles found in green sulfur bacteria and some other anoxygenic phototrophs. They contain a protein-coated lipid monolayer boundary and are attached to the inner membrane through a proteinaceous baseplate. Chlorosomes have been extensively studied in Chlorobaculum tepidum.

Lipid bodies

Organelles found in eukaryotes and bacteria that function in the storage and hydrolysis of triacylglycerols, wax esters and other neutral lipids. They have a boundary formed by a phospholipid monolayer that also includes protein components. Notable examples are found in Mycobacterium tuberculosis and Rhodococcus opacus; also known as lipid droplets or oil bodies.

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Greening, C., Lithgow, T. Formation and function of bacterial organelles. Nat Rev Microbiol 18, 677–689 (2020). https://doi.org/10.1038/s41579-020-0413-0

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