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Not a just pouch of enzymes: Bacteria also have organelles!

Go to the profile of Clement Aussignargues
Mar 12, 2018
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The article in Nature Reviews Microbiology is here: http://go.nature.com/2tNn519

When I was a first-year college student, a professor explained that in contrast to eukaryotic cells (as of plants and animals), bacterial cells are only bags filled with enzymes in which random collisions dictate… well, mostly everything. One cannot deny that the organization of eukaryotic cells is more complex than of bacteria, but this unfortunately still widespread reductionist point of view couldn’t be more wrong! Intricate sensory and regulation pathways, organization of proteins and enzymes into super- and megacomplexes, specialized structures (e.g. cytoskeleton, magnetosomes), nutrient storage inclusions, energy capture and conversion systems are only a few examples of the sophisticated subcellular organization employed by a multitude of bacterial species.

Another striking example of high-level organization is represented by bacterial microcompartments (BMCs), which are the subject of our review. Historically, these “polyhedral bodies”, as they were initially called, were first observed 60 years ago in electron micrographs of cyanobacteria (the ancestors of chloroplasts). The first isolated BMC was found to be composed of a protein shell enclosing ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), the key enzyme in carbon dioxide fixation (and the most abundant enzyme on Earth), hence the name carboxysome was proposed for this BMC. Carboxysomes were thought to be the only existing BMCs for more than 20 years. Only in the mid-90s, when genome sequencing became available, genes encoding homologues of carboxysomal shell proteins were found in Salmonella. These different types of BMCs are now termed metabolosomes and were demonstrated to be involved in the degradation of small carbon compounds, like propanediol and ethanolamine, to provide energy. A common feature of carboxysomes and metabolosomes is the function of the shell to insulate the enzymes they encapsulate from the cytosol, while allowing selective diffusion of substrates and products. This has several consequences: 1) preventing the escape of toxic or volatile compounds from the lumen of the BMC, 2) protecting the encapsulated enzymes from detrimental cytoplasmic molecules (oxygen, for example, can damage some enzymes or decrease the efficiency of carbon dioxide fixation), 3) concentrating enzymes and substrates to improve metabolic efficiencies and fluxes, 4) reducing competition with other metabolic pathways. Thus, BMCs can be considered as functionally analogous to lipid-bound eukaryotic organelles, and therefore are indeed one type of bacterial organelle.

Foreground, crystal structure of a 40 nm in diameter synthetic BMC shell. Background, electron micrograph of the same shells after crystallization and deposition on a transmission electron microscopy grid.


One of the most important findings of the last decade of research on BMCs is how widespread and functionally diverse they are: there are at least 23 types, differing in the substrates they use and the chemistry they encapsulate. They have been found in 2/3 of all sequenced bacterial phyla; certainly, more types remain to be discovered! Underscoring their importance is the involvement of BMCs in the pathogenicity of certain bacteria (e.g. Listeria monocytogenes, enterohemorrhagic Escherichia coli) that can utilize nutrients like propanediol and ethanolamine present in the human gut. Moreover, BMCs provide a promising target for biotechnological applications. The ever-growing understanding of their structure and strategies of self-assembly (some building the shell around a pre-formed core and others assembling the shell and the cargo at the same time) enables us to envision and build tailor-made nano-bioreactors and enzyme scaffolds. Components of the shells and the enzymatic cores of BMCs as well as other/new enzymes can be regarded as a set of building blocks that can be used in mix-and-match approaches to confer new functions, produce desired chemicals and generate energy. Imagine the wide range of possibilities of using BMCs and their encapsulated enzymes as bioengineered metabolic modules that can easily be introduced into new host organisms, while at the same time ensuring that the encapsulated pathway is insulated from the host metabolism and vice versa!

So as a take-home message, a BMC is a bacterial proteinaceous organelle, that confers a way to compartmentalize, protect and enhance the flux through metabolic pathways. They are becoming a powerful tool for biotechnological applications. Small but mighty!

 

Written with Jan Zarzycki, Fei Cai and Markus Sutter.

Go to the profile of Clement Aussignargues

Clement Aussignargues

Postdoctoral Research Associate, Michigan State University

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