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The Energetic Potential for Undiscovered Manganese Metabolisms in Nature.

ABSTRACT: Microorganisms are found in nearly every surface and near-surface environment, where they gain energy by catalyzing reactions among a wide variety of chemical compounds. The discovery of new catabolic strategies and microbial habitats can therefore be guided by determining which redox reactions can supply energy under environmentally-relevant conditions. In this study, we have explored the thermodynamic potential of redox reactions involving manganese, one of the most abundant transition metals in the Earth's crust. In particular, we have assessed the Gibbs energies of comproportionation and disproportionation reactions involving Mn²⁺ and several Mn-bearing oxide and oxyhydroxide minerals containing Mn in the +II, +III, and +IV oxidation states as a function of temperature (0-100°C) and pH (1-13). In addition, we also calculated the energetic potential of Mn²⁺ oxidation coupled to O₂, NO₂ ^-, NO₃ ^-, and FeOOH. Results show that these reactions-none of which, except O₂ + Mn²⁺, are known catabolisms-can provide energy to microorganisms, particularly at higher pH values and temperatures. Comproportionation between Mn²⁺ and pyrolusite, for example, can yield 10 s of kJ (mol Mn)^-1. Disproportionation of Mn³⁺ can yield more than 100 kJ (mol Mn)^-1 at conditions relevant to natural settings such as sediments, ferromanganese nodules and crusts, bioreactors and suboxic portions of the water column. Of the Mn²⁺ oxidation reactions, the one with nitrite as the electron acceptor is most energy yielding under most combinations of pH and temperature. We posit that several Mn redox reactions represent heretofore unknown microbial metabolisms.

SUBMITTER: LaRowe DE

PROVIDER: S-EPMC8220133 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The Greenland Ice Sheet is a biome which is mainly microbially driven. Several different niches can be found within the glacial biome for those microbes able to withstand the harsh conditions, e.g., low temperatures, low nutrient conditions, high UV radiation in summer, and contrasting long and dark winters. Eukaryotic algae can form blooms during the summer on the ice surface, interacting with communities of bacteria, fungi, and viruses. Cryoconite holes and snow are also habitats with their own microbial community. Nevertheless, the microbiome of supraglacial habitats remains poorly studied, leading to a lack of representative genomes from these environments. Under-investigated extremophiles, like those living on the Greenland Ice Sheet, may provide an untapped reservoir of chemical diversity that is yet to be discovered. In this study, an inventory of the biosynthetic potential of these organisms is made, through cataloging the presence of biosynthetic gene clusters in their genomes. There were 133 high-quality metagenome-assembled genomes (MAGs) and 28 whole genomes of bacteria obtained from samples of the ice sheet surface, cryoconite, biofilm, and snow using culturing-dependent and -independent approaches. AntiSMASH and BiG-SCAPE were used to mine these genomes and subsequently analyze the resulting predicted gene clusters. Extensive sets of predicted Biosynthetic Gene Clusters (BGCs) were collected from the genome collection, with limited overlap between isolates and MAGs. Additionally, little overlap was found in the biosynthetic potential among different environments, suggesting specialization of organisms in specific habitats. The median number of BGCs per genome was significantly higher for the isolates compared to the MAGs. The most talented producers were found among Proteobacteria. We found evidence for the capacity of these microbes to produce antimicrobials, carotenoid pigments, siderophores, and osmoprotectants, indicating potential survival mechanisms to cope with extreme conditions. The majority of identified BGCs, including those in the most prevalent gene cluster families, have unknown functions, presenting a substantial potential for bioprospecting. This study underscores the diverse biosynthetic potential in Greenland Ice Sheet genomes, revealing insights into survival strategies and highlighting the need for further exploration and characterization of these untapped resources.

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The Energetic Potential for Undiscovered Manganese Metabolisms in Nature.

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