Abstract
Methanosarcina acetivorans, considered a strict anaerobic archaeon, was cultured in the presence of 0.4–1% O2 (atmospheric) for at least 6 months to generate air-adapted cells; further, the biochemical mechanisms developed to deal with O2 were characterized. Methane production and protein content, as indicators of cell growth, did not change in air-adapted cells respect to cells cultured under anoxia (control cells). In contrast, growth and methane production significantly decreased in control cells exposed for the first time to O2. Production of reactive oxygen species was 50 times lower in air-adapted cells versus control cells, suggesting enhanced anti-oxidant mechanisms that attenuated the O2 toxicity. In this regard, (i) the transcripts and activities of superoxide dismutase, catalase and peroxidase significantly increased; and (ii) the thiol-molecules (cysteine + coenzyme M-SH + sulfide) and polyphosphate contents were respectively 2 and 5 times higher in air-adapted cells versus anaerobic-control cells. Long-term cultures (18 days) of air-adapted cells exposed to 2% O2 exhibited the ability to form biofilms. These data indicate that M. acetivorans develops multiple mechanisms to contend with O2 and the associated oxidative stress, as also suggested by genome analyses for some methanogens.
Highlights
The reactive oxygen species (ROS) are toxic for most cells because they induce (i) oxidation of polysaccharides and polyunsaturated fatty acids, as well as amino acid residues, of sulfhydryl groups in proteins; (ii) loss of metals in metalloproteins; and (iii) DNA mutations, among many others [1]
A survey of genes coding for enzymes putatively involved in oxidative stress in genomes from 27 different genera belonging to the 5 orders of methanogens, available in the Kyoto Encyclopedia of Genes and Genomes (KEGG) data base, showed that M. acetivorans is among the methanogens with the largest number of genes coding for anti-oxidant proteins (Table 1)
It has been proposed that the presence or absence of one or both of the superoxide dismutase (SOD) and CAT activities determines whether an anaerobe is aerotolerant [20]
Summary
The reactive oxygen species (ROS) are toxic for most cells because they induce (i) oxidation of polysaccharides and polyunsaturated fatty acids, as well as amino acid residues, of sulfhydryl groups in proteins; (ii) loss of metals in metalloproteins; and (iii) DNA mutations, among many others [1]. Aerobic microorganisms have developed multiple strategies to handle ROS stress including: (i) enzymes that scavenge ROS such as superoxide dismutase (SOD), catalase (CAT) and peroxidases (PXs); (ii) protein repair mechanisms such as the thioredoxin system; (iii) DNA damage repair enzymes such as RecA; and (iv) anti-oxidant metabolites such as glutathione, α-tocopherol, carotenes, ascorbate, and trypanothione, which are able to directly inactive ROS [1,2,3,4]. Mechanisms of Tolerance to Oxygen in Methanogens
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