TotM: Lactobacillus manganese transporter MntA, an unusual universal defence against oxygen

rusty.jpgLiving beings have a complex relationship with oxygen. We living in a planet whose atmosphere has more than one fifth of this element in its free molecular form, but at the same this element is fatally toxic. Oxygen is a powerful reagent that breaks many of the carbon to carbon links that form the backbone of our organic chemistry. Just look at its effects on iron! Even worse, photosynthetic organisms keep pumping this poison to the air, ensuring a stable supply, while a big portion of our biosphere has learn to use the same reactive properties that make it such a dangerous gas for the production of metabolic energy. This implies that before the origin of oxygenic photosynthesis our planet atmosphere must have been very different. Life must have originated under anaerobic conditions, and even today many organisms prefer to live in oxygen poor environments.

 

The use of oxygen in metabolism requires the existence of an array of antioxidant protections, enzymes that are able to synthesize protective compounds or to transform highly reactive oxygen species into a less aggressive form. The cost usually is worth it, and the energy we obtain from these tiny furnaces propels, among many other, the incredible biological computers that is our brains. Given the high cost of oxygen protection and the high benefit of oxygen utilization, one would expect an unbreakable ecological wall between anaerobic and aerobic organisms. But quite often life does not make any sense.

 

800px-Bulgarian_yogurt.JPGLactic acid bacteria, such as Lactobacillus, are extremely important organisms for food industry and even our own health. They are avid fermenters and are either the main protagonist or very important secondary characters in the production of basically any fermented food, from dairy products to alcoholic beverages, meats or vegetables. As fermenters, they don’t use oxygen for anything important in their metabolism. Even more, they lack typical catalases and many other important anti-oxygen mechanisms, as you would expect of an anaerobic bacteria. And yet you can find them growing happily while exposed to the supposedly deadly atmosphere of our world. How?

 

In order to survive oxygen exposition, this group of bacteria employs the sheer power of manganese. They contain an special type of catalase-like enzymes that use manganese instead of an heme group, and they accumulate manganese within their cytoplasm. Manganese then forms complexes with several functional groups, specially free phosphate, that act as powerful antioxidant molecules. This type of defenses is not exclusive of Lactobacillus, and defensive manganese complexes can be found in all domains of life. Their effectivity as protection is highlighted when we examine their role in other bacterial species, Deinococcus radiodurans. This organism, that was nicknamed by microbiologist as “Conan the Bacterion” is able to withstand terrifying levels of oxidizing agents and ionizing radiations, an impressive ability in which manganese complexes play an important role. And while the survivability of Lactobacillus is far less impressive, the fact that is able to live “normally” with just that line of defence is no less impressive.

 

lactobacillus.jpgAnother implication of this manganese bioaccumulation is the fact that Lactobacillus cells contain very little iron. Iron and manganese can compete for the same chemical groups, and thus iron must be kept to a minimal level to sustain the trick. Manganese is relatively much more scarce, though. In order to accumulate this element, Lactobacillus needs highly active transporters that keep absorbing it. The first described of this transporters was MntA, divalent cationic pump that consumes ATP to transport manganese and other divalent cations, such as cadmium. The protein has orthologs in many other bacterial species, as we can observe in our tree of the month from the Lactobacillus plantarum phylome, but very few can do the same. So please, before eating your next piece of cheese or yogurt, take a deep breathing and remember those tiny heroes that managed to live like no one else to make your food more delicious. Bon appetit!

 

References:

https://www.ncbi.nlm.nih.gov/pubmed/25146195

https://www.ncbi.nlm.nih.gov/pubmed/23249283

https://www.ncbi.nlm.nih.gov/pubmed/22247543

https://www.ncbi.nlm.nih.gov/pubmed/15817790

https://www.ncbi.nlm.nih.gov/pubmed/12419613

https://www.ncbi.nlm.nih.gov/pubmed/10543781

https://www.ncbi.nlm.nih.gov/pubmed/3522109

 

Pictures:

Photography of gear covered by rust. Public domain license.

Photography of bulgarian yogurt, one of many products obtained using Lactobacillus. Photography by Ned Jelyazkov. Creative Commons license.

Microphotography of Lactobacillus sp. stained with gram dye. Photographed by Riccardo Ariotti. Creative Commons license.