Niche Filtering of Bacteria in Soil and Rock Habitats of the Colorado Plateau Desert, Utah, USA.

A common feature of microbial colonization in deserts is biological soil crusts (BSCs), and these comprise a complex community dominated by Cyanobacteria. Rock substrates, particularly sandstone, are also colonized by microbial communities. These are separated by bare sandy soil that also supports microbial colonization. Here we report a high-throughput sequencing study of BSC and cryptoendolith plus adjacent bare soil communities in the Colorado Plateau Desert, Utah, USA. Bare soils supported a community with low levels of recoverable DNA and high evenness, whilst BSC yielded relatively high recoverable DNA, and reduced evenness compared to bare soil due to specialized crust taxa. The cryptoendolithic community displayed the greatest evenness but the lowest diversity, reflecting the highly specialized nature of these communities. A strong substrate-dependent pattern of community assembly was observed, and in particular cyanobacterial taxa were distinct. Soils were virtually devoid of photoautotrophic signatures, BSC was dominated by a closely related group of Microcoleus/Phormidium taxa, whilst cryptoendolithic colonization in sandstone supported almost exclusively a single genus, Chroococcidiopsis. We interpret this as strong evidence for niche filtering of taxa in communities. Local inter-niche recruitment of photoautotrophs may therefore be limited and so communities likely depend significantly on cyanobacterial recruitment from distant sources of similar substrate. We discuss the implication of this finding in terms of conservation and management of desert microbiota.

Epidermal cells help coordinate leukocyte migration during inflammation through fatty acid-fuelled matrix metalloproteinase production.

In addition to satisfying the metabolic demands of cells, mitochondrial metabolism helps regulate immune cell function. To date, such cell-intrinsic metabolic-immunologic cross-talk has only been described operating in cells of the immune system. Here we show that epidermal cells utilize fatty acid ß-oxidation to fuel their contribution to the immune response during cutaneous inflammation. By live imaging metabolic and immunological processes within intact zebrafish embryos during cutaneous inflammation, we uncover a mechanism where elevated ß-oxidation-fuelled mitochondria-derived reactive oxygen species within epidermal cells helps guide matrix metalloproteinase-driven leukocyte recruitment. This mechanism requires the activity of a zebrafish homologue of the mammalian mitochondrial enzyme, Immunoresponsive gene 1. This study describes the first example of metabolic reprogramming operating within a non-immune cell type to help control its contribution to the immune response. Targeting of this metabolic-immunologic interface within keratinocytes may prove useful in treating inflammatory dermatoses.

Immunoresponsive gene 1 augments bactericidal activity of macrophage-lineage cells by regulating ß-oxidation-dependent mitochondrial ROS production.

Evidence suggests the bactericidal activity of mitochondria-derived reactive oxygen species (mROS) directly contributes to killing phagocytozed bacteria. Infection-responsive components that regulate this process remain incompletely understood. We describe a role for the mitochondria-localizing enzyme encoded by Immunoresponsive gene 1 (IRG1) during the utilization of fatty acids as a fuel for oxidative phosphorylation (OXPHOS) and associated mROS production. In a zebrafish infection model, infection-responsive expression of zebrafish irg1 is specific to macrophage-lineage cells and is regulated cooperatively by glucocorticoid and JAK/STAT signaling pathways. Irg1-depleted macrophage-lineage cells are impaired in their ability to utilize fatty acids as an energy substrate for OXPHOS-derived mROS production resulting in defective bactericidal activity. Additionally, the requirement for fatty acid ß-oxidation during infection-responsive mROS production and bactericidal activity toward intracellular bacteria is conserved in murine macrophages. These results reveal IRG1 as a key component of the immunometabolism axis, connecting infection, cellular metabolism, and macrophage effector function.