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Wednesday, June 04, 2014

The Other Catalase

Microbiology students are taught from Day One that strict anaerobes (organisms that are killed by exposure to oxygen) lack the enzyme catalase, which breaks down hydrogen peroxide to water and O2. You're already familiar with this enzyme if you've ever poured peroxide on a wound and seen it get foamy (blood is rich in catalase) or if you've used a peroxide bleach on your teeth, which causes saliva to become thick and gummy with microscopic bubbles. Catalase is a nearly universal enzyme, but strict anaerobes lack it (seemingly), because they are so seldom exposed to oxygen or its metabolites.

An unexpected result of genome data mining is the finding that non-heme (and thus non-iron-containing) catalase exists in a wide variety of bacteria once thought to contain no catalases. Manganese-containing catalase was first described in Lactobacillus, an organism that produces no cytochromes (and no porphyrins). The same type of enzyme was later experimentally verified in a thermophilic archeon, Pyrobaculum. It now turns out that many strict anaerobes previously believed to be catalase-free (such as most Clostridium species) contain this enzyme.

Phylogenetic distribution of manganese catalase (click to enlarge). At the top are the spore-forming Bacillus, with non-spore-forming Firmicutes (Aerococcus et al.) in a sub-branch below, and the cyanobacteria (Nostoc and Microcoleus) as an out-group to the Bacillus group. One cyanobacterial species, Cyanothece sp. PCC 7424 (a rice-field isolate), occurs as an out-node amongst the Gammaproteobacteria, indicating possible horizontal gene transfer. Archaeal organisms (Halalkalicoccus etc.) with this enzyme tend to be salt-lovers, although Pyrobaculum (not shown), which thrives in 2% salt, also has it. The phylo-tree was constructed from protein sequence alignments using Mega6 freeware. Node assignments were tested with 500 bootstraps.
Why would an anaerobe need catalase? Short answer: because small oxygenated molecules (like hydrogen peroxide and superoxide anion) are damaging to DNA, typically causing guanine to become oxidized to 8-oxo-guanine (which mispairs with adenine). Also, molecular oxygen irreversibly poisons the nitrogenase enzyme that many Clostridium members (and others) rely on to metabolize atmospheric nitrogen.

You would think that if molecular oxygen is a product of catalase action (and damages nitrogenase), Clostridium would not want to have catalase around in its cytoplasm. But Clostridium doesn't localize its catalase to the cytoplasm. It's a spore-surface enzyme. And this is key to understanding its distribution in nature.

Manganese catalase is rather sparsely distributed. It occurs just in certain taxonomic groups and certain species (see illustration, above). The enzyme seems to have been invented by the spore-forming Firmicutes (Bacillus and Clostridium) as a spore-coat enzyme. Many phylogenetically younger Firmicutes that have lost the ability to form spores also have the enzyme, as do some (not all) members of the Rhizobiales (not shown above), probably as an adaptation to low-iron niches. (The canonical heme-containing form of catalase requires iron.) There is evidence, in fact, that Lactobacillus leads a completely iron-free existence.

Where else do we find manganese catalase? Some (but not all) cyanobacteria have it. This is noteworthy in that the cyanobacteria form a specialized, environmentally hardened sessile cell called an akinete. (It's also noteworthy that both cyanobacteria and certain Clostridium members have nitrogenase.) The cyanobacteria that have the manganese catalase are primarily land-dwellers, however, not marine bacteria. This includes Anabaena (a moss symbiont and rice-paddy dweller), Microcoleus (which occurs in arid soils), and certain Nostoc members (which occur on rocks, in lichens), plus Cyanothece (from rice paddies).

Curiously, very few marine organisms have manganese catalase, the chief exceptions being Pirellula and Planctomyces. (And again, interestingly, Pirellula has a specialized sessile form as well as a motile form.) Many halophilic (salt-loving) archeons have the enzyme; surely those qualify as marine organisms? Not really. Halococcus, Natrinema, etc. are not planktonic; open-ocean waters have too little salt. (These organisms require upwards of 30% salinity, much stronger than the 3.5% salinity of sea water.) The salt-loving archeons live in drying-up seas (like the Dead Sea or Great Salt Lake) and at the edges of beaches, where salt concentrations skyrocket. These are, in effect, "terrestrial marine organisms," if that makes sense.

You can also find manganese catalase in some members of the Gammaproteobacteria (namely certain E. coli strains and some Pseudomonads), though curiously not in Shigella, Yersinia, or the Vibrio family (which is largely marine). The spotty nature of the enzyme's distribution among the enterics and Pseudomonads (which have no specialized sessile form) speaks to a possible horizontal gene transfer scenario.

There is little reason to believe manganese catalase is primordial. It certainly didn't come from the sea. In the first place, the enzyme is absent from Pelagibacter, Vibrio, and other important marine organisms. Secondly, sea water contains surprisingly little manganese (less than a part per billion). Marine organisms that do have catalase tend to have the heme-containing version of the enzyme (which makes sense, in that the oldest photosynthetic organisms long go mastered the art of porphyrin synthesis). Manganese catalase is a terrestrial adaptation, primarily of spore-, heterocyst-, and akinete-formers, with others obtaining the enzyme by lateral gene transfer. It's interesting that the Gammaproteobacteria that have manganese catalase (some enterics and some Pseudomonads) are opportunistic pathogens. They probably find the enzyme useful in combating the respiratory burst of phagocytes.

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