Mapping metabolic activity at single cell resolution in intact volcanic fumarole soil

Interactions among microorganisms and their mineralogical substrates govern the structure, function, and emergent properties of microbial communities. These interactions are predicated on spatial relationships, which dictate metabolite exchange and access to key substrates. To quantitatively assess links between spatial relationships and metabolic activity, this study presents a novel approach to map all organisms, the metabolically active subset, and associated mineral grains, all while maintaining spatial integrity of an environmental microbiome. We applied this method at an outgassing fumarole of Vanuatu’s Marum Crater, one of the largest point sources of several environmentally relevant gaseous compounds, including H2O, CO2, and SO2. With increasing distance from the soil-air surface and from mineral grain outer boundaries, organism abundance decreased but the proportion of metabolically active organisms often increased. These protected niches may provide more stable conditions that promote consistent metabolic activity of a streamlined community. Conversely, mineral exteriors accumulate more organisms that may cover a wider range of preferred conditions, implying that only a subset of the community will be active under any particular environmental regime. More broadly, the approach presented here allows investigators to see microbial communities “as they really are” and explore determinants of metabolic activity across a range of microbiomes.