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Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function

Key Points

  • Planctomycetes form a distinctive phylum of the Bacteria, having a unique combination of features such as peptidoglycan-lacking proteinaceous cell walls, and intracellular membranes that form separate compartments within the cell cytoplasm. Such compartments are proving to be functionally as well as structurally distinct entities and are important for our understanding of the origin of the eukaryotic cell.

  • Planctomycetes are present in many different habitats, including the oceans, marine sediments, freshwater lakes, wastewater and terrestrial soils.

  • Anammox planctomycetes form a distinct family within the phylum and are anaerobic autotrophs that can oxidize ammonia to dinitrogen without oxygen. They play a major part in the global nitrogen cycle and form the basis for new industrial processes aimed at remediating nitrogen-rich wastewater. The unique physiology of these organisms is based on the presence of a specialized organelle, the anammoxosome, which might represent a bacterial analogue of the eukaryotic mitochondrion.

  • Comparative genomics and proteomics have revealed that the distinction between anammox and non-anammox planctomycetes goes beyond ammonium metabolism. Genomics has also reinforced the view that planctomycetes are members of a wider Planctomycetes–Verrucomicrobia–Chlamydiae (PVC) superphylum.

  • An endocytosis-like mechanism for the uptake of macromolecules such as proteins has been described in the planctomycete genus Gemmata. This mechanism is analogous, and possibly even homologous, to the eukaryotic process of endocytosis.

  • Research on planctomycetes is shedding new light on the origin and evolution of the eukaryotic endomembrane systems. In particular, it challenges current models for the origin of the nucleus that depend on the fusion of cells from different domains of life.

Abstract

Planctomycetes form a distinct phylum of the domain Bacteria and possess unusual features such as intracellular compartmentalization and a lack of peptidoglycan in their cell walls. Remarkably, cells of the genus Gemmata even contain a membrane-bound nucleoid analogous to the eukaryotic nucleus. Moreover, the so-called 'anammox' planctomycetes have a unique anaerobic, autotrophic metabolism that includes the ability to oxidize ammonium; this process is dependent on a characteristic membrane-bound cell compartment called the anammoxosome, which might be a functional analogue of the eukaryotic mitochondrion. The compartmentalization of planctomycetes challenges our hypotheses regarding the origins of eukaryotic organelles. Furthermore, the recent discovery of both an endocytosis-like ability and proteins homologous to eukaryotic clathrin in a planctomycete marks this phylum as one to watch for future research on the origin and evolution of the eukaryotic cell.

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Figure 1: An idealized planctomycete in the process of cell division.
Figure 2: Phylogenetic relationships between planctomycetes and other organisms.
Figure 3: Cell structure of planctomycetes.
Figure 4: Anammox planctomycetes.
Figure 5: An endocytosis-like process in planctomycetes.

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Acknowledgements

Research on planctomycetes in the J.A.F. laboratory is supported by the Australian Research Council (ARC Discovery Project DP0881485).

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Correspondence to John A. Fuerst.

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DATABASES

Entrez Genome Project for planctomycetes

Blastopirellula marina

Gemmata obscuriglobus

Isosphaera pallida

Pirellula staleyi

Planctomyces brasiliensis

Planctomyces limnophilus

Planctomyces maris

Rhodopirellula baltica

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Glossary

Nucleoid

The region of the bacterial cell that contains the genomic DNA, usually seen in thin sections as a fibrillar region; in electron micrographs of cryosubstituted Escherichia coli cell sections, the nucleoid seems to occupy much of the cell, whereas it forms a highly condensed fibrillar structure in planctomycetes.

Anammox

Anaerobic ammonium oxidation, a process performed by some species of planctomycetes, whereby ammonium is oxidized to dinitrogen using nitrite as an electron acceptor via intermediates, including toxic hydrazine.

C1 transfer

The process by which a compound containing only one carbon atom (a C1 compound; such as methane, methylamine, formate and formaldehyde) is enzymatically transformed into another C1 compound.

Sulphatases

Enzymes that hydrolytically cleave sulphate esters to yield inorganic sulphate and an alcohol.

Clathrin

A eukaryotic protein that coats the vesicles formed during endocytosis.

Anammoxosome

An organelle within the pirellulosome of anammox planctomycetes that is surrounded by a single bilayer membrane and contains enzymes that are essential for the oxidation of ammonia to dinitrogen.

Heterolactic fermentation

A pathway for anaerobic fermentation of carbohydrates; typically found in lactic acid bacteria, in which the dominant end products are lactic acid, ethanol and carbon dioxide.

Divisome

A complex of proteins that is associated with cell division in peptidoglycan-synthesizing bacteria and that locates to the septum of cells dividing by binary fission. The complex includes cell division protein FtsZ and, usually, other proteins such as FtsI, FtsA and FtsK, as well as penicillin-binding proteins involved in peptidoglycan synthesis.

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Fuerst, J., Sagulenko, E. Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nat Rev Microbiol 9, 403–413 (2011). https://doi.org/10.1038/nrmicro2578

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  • DOI: https://doi.org/10.1038/nrmicro2578

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