Insights into communities, metabolic and ecological potential of the bacteria of two extreme acidic environments
Creators: name: Sheremet, Andriy
Publisher: name: Science
Year: 2022
Subjects: subject: Metagenomics
subject: Molecular Microbiology
subject: Microbial Ecology
subject: Extremophiles
subject: Acidophiles
subject: Candidate Phyla
subject: Genome Streamlining
subject: Stable Isotope Probing
subject: Short-Chain Alkanes Biodegradation
subject: Biology--Bioinformatics
subject: Biology--Ecology
subject: Biology--Microbiology
subject: Biology--Molecular

description: This work examines the microbial communities in two extremely acidic habitats:the terrestrial environment of the Paint Pots Mound (Kootenay National Park, BritishColumbia, Canada) and the sediments of an ultra-acidic lake in the Smoking Hills (CapeBathurst, Northwest Territories, Canada) area. While the acidification of both locationsoriginates from the natural pyrite ore oxidation processes, the sites show a dramaticcontrast in microbial compositions, function, complexity, and diversity. The chemicalcomposition of the sites is suggestive of that of acid mine drainage (AMD) systems;however, the habitats of the Paint Pots and Smoking Hills are pristine, unlike the majorityof AMD, and therefore offer a unique opportunity in microbial ecology research.The microbial communities of the sites are explored using metagenomics andstable isotope probing. Microbial load and diversity in both locations were low. However,despite their high acidity, metal, and sulfate content similarities, the habitats hostedcontrasting microbial communities.The Paint Pots Mound environment is notable for the elevated abundance of suchlineages as WPS-2, AD3, Ca. Binatia, Elsterales, and atmospheric methane oxidizers ofthe genus Methylocapsa, compared to other habitats reported in the literature. Membersof the phylum WPS-2, also known as Eremiobacterota, dominated bare, nonvegetatedzones. Metabolically, it was proposed that these organisms were organoheterotrophs,using amino acids, peptides, and nucleotides for growth, and were, perhaps, adapted toscavenging or parasitizing and antimicrobial compound resistance. At the same time, themetagenomic data indicated the presence of multiple lineages of soluble and particulatemethane monooxygenase homologs. Such results aligned with the soil activity towardsoxidating methane, ethane, and propane. As a result of a DNA stable isotope probingexperiment, using 13 C labeled propane, it was established that 2-propanemonooxygenases were associated with propane oxidation, carried out by taxonomicallydiverse groups of organisms. The short-chain hydrocarbon oxidation activity in the PaintPots soil was comparable to the soils from natural gas seepage sites.In contrast, the prokaryotic community of the Smoking Hills lake sediments wasdominated by a single species of Acidithiobacillus ferrivorans SH11, constituting morethan 73% of the 16S rRNA gene amplicons. The site was characterized by low microbialcell count and lithoautotrophic metabolism, centered on iron and sulfur oxidation andCO 2 fixation via the Calvin–Benson–Bassham cycle. At the same time, the genomicfeatures of A. ferrivorans SH11 suggested these organisms were undergoing genomestreamlining. The genome of these organisms was characterized by increased genedensity and fractions of genes annotated with COG or Pfam, compared to culturedisolates. The degree of genome streamlining in these organisms living inside the Arcticcircle surpassed that of the uncultured Acidithiobacillus genomes recovered from hotsprings. A strong inverse relationship between genome size and a fraction of genesannotated with COG, observed for Acidithiobacillus genomes, was a common trendamong other genera in Proteobacteria.Therefore, as the Smoking Hills environment was dominated by an autotrophicorganism with a streamlined genome, the notable members of the Paint Pots Moundcommunity were mainly metabolically diverse heterotrophs.