Prokaryotic Organelles. Yes, There Are Such Things.
by Elio
One of the venerable distinctions between eukaryotes and prokaryotes used to be that prokaryotes do not have organelles. This distinction has now gone by the wayside because bacteria and archaea have been shown to possess protein bound structures that can appropriately be called organelles. They go by other names as well, such as microcompartments, nanocompartments, encapsulins, etc. Call them what you wish, they are all a way to compartmentalize enzymes that may not work well free in the cytoplasm or a strategy to keep toxic compounds in isolation. True, they may seem to be rather unpretentious protein bags that do not suggest a symbiotic origin as seen in mitochondria or chloroplasts. So far none have been shown to carry DNA.
Figure 1. Carboxysomes and their subcellular context (arrowheads in panels A and B indicate the positions of carboxysomes). A β‑Carboxysomes present in Synechococcus elongatus. B α‑Carboxysomes present in Cyanobium. (Courtesy of Lynne Whitehead.) C Close-up of a β‑carboxysome from S. elongatus. D Close-up of a β‑carboxysome from Anabaena variabilis M3. Source
Prokaryotic microcompartments and their ilk are involved in a great variety of microbial activities, from photosynthesis to certain diseases. So important are these structures to our understanding of microbial metabolism that we need to review our long-held beliefs of how the microbial cytoplasm works.
Among the first discovered and best studied prokaryotic organelles are the carboxysomes, structures that store RuBisCO, the enzyme that carries out carbon dioxide fixation during photosynthesis. They further help it out by increasing the local CO2 concentration using what is called a CO2-concentrating mechanism (CCM). Carboxysomes encapsulate the enzyme carbonic anhydrase that supplies CO2 from a cytoplasmic pool of bicarbonate. Not only that, carboxysomes sequester toxic aldehyde intermediates and thus remove them from the cytoplasm. Carboxysomes and their CCMs are found in the cyanobacteria, the dominant photosynthetic microbes, and in some proteobacteria. The proteins of the shells are not all identical – they come in several evolutionarily distinct forms.
Figure 2. A Negative stain micrograph of an apo-SrpI shell in contrast with © the holo-SrpI shell that includes the CyD cargo. B and D 3D reconstruction of apo-Srpl and holo-SrpI, respectively. E Difference map showing additional density for the holo-SrpI with a homologous cysteine desulfurase dimer docked in (pdb: 6c9e). Source
Carboxysomes present an opportunity for possibly spectacular improvements in crop production. Imagine cloning the CCM from cyanobacteria into plant chloroplasts. This might well increase the level of photosynthesis of such crops and augment their production to a significant extent. This kind of bioengineering is not easy, but it's being attempted in several laboratories, e.g. here, here, and here.
Prokaryotic organelles are not limited to the carboxysomes, far from it. There is an abundance of them, found in at least 19 bacterial phyla. An older example of a bacterial organelle is one involved in propane-diol metabolism. It sequesters a toxic aldehyde intermediate and make it susceptible to degradation. More recent is the discovery of a class of even smaller compartments called encapsulins, which are simpler than the previously known microcompartments. Typically, they consist of just two proteins, one that self-assembles into an icosahedral shell not unlike a viral capsid, and a cargo protein that is often multifunctional. Interestingly, cargo proteins have a peptide sequence that dictates their encapsulation. The cargo proteins that are so encapsulated are quite diverse. They include some involved in iron mineralization, peroxidation, and tolerance to starvation and to certain stresses. As pointed out here, a recurring theme is the encapsulation of components of redox reactions.
Figure 3. (CyD), unencapsulated cysteine desulfurase (CyD alone), unencapsulated cysteine desulfurase lacking its NTD (ΔNTD-CyD alone), and empty nanocompartment using a coupled-enzyme assay with alanine dehydrogenase and production of NADH as a readout of cysteine desulfurase activity. Source
A recent paper from nine American and Canadian laboratories (with D. F. Savage as the last author) describes a new family of such nanocompartments. It was found in the cyanobacterium Synechococcus elongatus and is involved in sulfur metabolism. This structure is upregulated during sulfate starvation. Its sole cargo the enzyme cysteine desulfurase, which removes the sulfur from cysteine to convert it into alanine. The authors further identify a terminal sequence in this cargo protein that is necessary and sufficient for the compartmentalization.
A detailed study of this encapsulin revealed structural features that are seen by cryo-electronmicroscopy. Interestingly, The shell protein shares features with the capsid protein of phages of the very populous order tailed phages, the Caudovirales, which suggests a possible common ancestry. Lastly, homologs of the shell protein are found in various mycobacteria, including human and avian pathogens.
The authors conclude: "Our identification of SrpI (the shell protein) and its homologs as members of an evolutionarily distinct encapsulin family may provide further insights into the divergence and origin of prokaryotic nanocompartments. Already, the breadth and diversity of known encapsulin systems is vast, yet it is likely that more await discovery."
