Geothermal gases shape the microbial community of the volcanic soil of Pantelleria, Italy

Abstract

Volcanic and geothermal environments are characterized by low pH, high temperatures, and gas emissions consisting of mainly CO2 and varied CH4, H2S, and H2 contents which allow the formation of chemolithoautotrophic microbial communities. To determine the link between the emitted gases and the microbial community composition, geochemical and metagenomic analysis were performed. Soil samples of the geothermic region Favara Grande (Pantelleria, Italy) were taken at various depths (1 to 50 cm). Analysis of the gas composition revealed that CH4 and H2 have the potential to serve as the driving forces for the microbial community. Our metagenomic analysis revealed a high relative abundance of Bacteria in the top layer (1 to 10 cm), but the relative abundance of Archaea increased with depth from 32% to 70%. In particular, a putative hydrogenotrophic methanogenic archaeon, related to Methanocella conradii, appeared to have a high relative abundance (63%) in deeper layers. A variety of [NiFe]-hydrogenase genes were detected, showing that H2 was an important electron donor for microaerobic microorganisms in the upper layers. Furthermore, the bacterial population included verrucomicrobial and proteobacterial methanotrophs, the former showing an up to 7.8 times higher relative abundance. Analysis of the metabolic potential of this microbial community showed a clear capacity to oxidize CH4 aerobically, as several genes for distinct particulate methane monooxygenases and lanthanide-dependent methanol dehydrogenases (XoxF-type) were retrieved. Analysis of the CO2 fixation pathways showed the presence of the Calvin-Benson-Bassham cycle, the Wood-Ljungdahl pathway, and the (reverse) tricarboxylic acid (TCA) cycle, the latter being the most represented carbon fixation pathway. This study indicates that the methane emissions in the Favara Grande might be a combination of geothermal activity and biological processes and further provides insights into the diversity of the microbial population thriving on CH4 and H2. IMPORTANCE The Favara Grande nature reserve on the volcanic island of Pantelleria (Italy) is known for its geothermal gas emissions and high soil temperatures. These volcanic soil ecosystems represent “hot spots” of greenhouse gas emissions. The unique community might be shaped by the hostile conditions in the ecosystem, and it is involved in the cycling of elements such as carbon, hydrogen, sulfur, and nitrogen. Our metagenome study revealed that most of the microorganisms in this extreme environment are only distantly related to cultivated bacteria. The results obtained profoundly increased the understanding of these natural hot spots of greenhouse gas production/degradation and will help to enrich and isolate the microbial key players. After isolation, it will become possible to unravel the molecular mechanisms by which they adapt to extreme (thermo/acidophilic) conditions, and this may lead to new green enzymatic catalysts and technologies for industry.