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USGS2018

Volcanic ash activates the NLRP3 inflammasome in murine and human macrophages

Volcanic ash is a heterogeneous mineral dust that is typically composed of a mixture of amorphous (glass) and crystalline (mineral) fragments. It commonly contains an abundance of the crystalline silica (SiO 2 ) polymorph cristobalite. Inhalation of crystalline silica can induce inflammation by stimulating the NLRP3 inflammasome, a cytosolic receptor complex that plays a critical role in driving inflammatory immune responses. Ingested material results in the assembly of NLRP3, ASC, and caspase-1 with subsequent secretion of the interleukin-1 family cytokine IL-1β. Previous toxicology work suggests that cristobalite-bearing volcanic ash is minimally reactive, calling into question the reactivity of volcanically derived crystalline silica, in general. In this study, we target the NLRP3 inflammasome as a crystalline silica responsive element to clarify volcanic cristobalite reactivity. We expose immortalized bone marrow-derived macrophages of genetically engineered mice and primary human peripheral blood mononuclear cells (PBMCs) to ash from the Soufrière Hills volcano as well as representative, pure-phase samples of its primary componentry (volcanic glass, feldspar, cristobalite) and measure NLRP3 inflammasome activation. We demonstrate that respirable Soufrière Hills volcanic ash induces the activation of caspase-1 with subsequent release of mature IL-1β in a NLRP3 inflammasome-dependent manner. Macrophages deficient in NLRP3 inflammasome components are incapable of secreting IL-1β in response to volcanic ash ingestion. Cellular uptake induces lysosomal destabilization involving cysteine proteases. Furthermore, the response involves activation of mitochondrial stress pathways leading to the generation of reactive oxygen species. Considering ash componentry, cristobalite is the most reactive pure-phase with other components inducing only low-level IL-1β secretion. Inflammasome activation mediated by inhaled ash and its potential relevance in chronic pulmonary disease was further evidenced in PBMC using the NLRP3 small-molecule inhibitor CP-456,773 (CRID3, MCC950). Our data indicate the functional activation of the NLRP3 inflammasome by volcanic ash in murine and human macrophages in vitro . Cristobalite is identified as the apparent driver, thereby contesting previous assertions that chemical and structural imperfections may be sufficient to abrogate the reactivity of volcanically derived cristobalite. This is a novel mechanism for the stimulation of a pro-inflammatory response by volcanic particulate and provides new insight regarding chronic exposure to environmentally occurring particles.

Frontiers in Immunology↗

USGS2021

Comparative genomics analyses support the reclassification of Bisgaard taxon 40 as Mergibacter gen. nov., with Mergibacter septicus sp. nov. as type species: Novel insights into the phylogeny and virulence factors of a Pasteurellaceae family member associated with mortality events in seabirds

The Pasteurellaceae family has been associated with fatal diseases in numerous avian species. Several new taxa within this family, including Bisgaard taxon 40, have been recently described in wild birds, but their genomic characteristics and pathogenicity are not well understood. We isolated Bisgaard taxon 40 from four species of seabirds, including one sampled during a mass, multi-species mortality event in Florida, United States. Here, we present a comprehensive phenotypic and genetic characterization of Bisgaard taxon 40 and comparative genomic analysis with reference strains from the Pasteurellaceae family, aiming at determining its phylogenetic position, antimicrobial susceptibility profile, and identifying putative virulence factors. In silico multilocus sequence-based and whole-genome-based phylogenetic analysis clustered all Bisgaard taxon 40 strains together on a distinct branch separated from the other members of the Pasteurellaceae family, indicating that Bisgaard taxon 40 could represent a new genus. These findings were further supported by protein similarity analyses using the concatenation of 31 conserved proteins and other taxonomic approaches such as the percentage of conserved protein test. Additionally, several putative virulence factors were identified, including those associated with adhesion (capsule, ompA , ompH ) and colonization ( exbD , fur , galU , galE , lpxA , lpxC , and kdsA ) of the host and a cytolethal distending toxin ( cdt ), which may have played a role in disease development leading to the mortality event. Considerably low minimum inhibitory concentrations (MICs) were found for all the drugs tested, in concordance with the absence of antimicrobial resistance genes in these genomes. The novel findings of this study highlight genomic and phenotypic characteristics of this bacterium, providing insights into genome evolution and pathogenicity. We propose a reclassification of these organisms within the Pasteurellaceae family, designated as Mergibacter gen. nov., with Mergibacter septicus sp. nov. as the type species. The type strain is Mergibacter septicus A25201 T (=DSM 112696).

Frontiers in Microbiology↗

USGS2023

Host vs. pathogen evolutionary arms race: Effects of exposure history on individual response to a genetically diverse pathogen

Introduction: Throughout their range, bighorn sheep ( Ovis canadensis ) populations have seen significant disease-associated declines. Unfortunately, understanding of the underlying epidemiological processes driving the disease dynamics in this species has hindered conservation efforts aimed at improving the health and long-term viability of these populations. Individual response to pathogen exposure emerges from dynamic interactions between competing evolutionary processes within the host and pathogen. The host’s adaptive immune system recognizes pathogens and mounts a defensive response. Pathogens have evolved strategies to overcome adaptive immune defenses including maintaining high genetic diversity through rapid evolution. The outcomes of this evolutionary warfare determine the success of pathogen invasion of the host and ultimately the success of conservation efforts. Methods: During an epizootic dominated by a single strain, we explore these host-pathogen dynamics by examining the variation in effects of pathogen invasion on captive bighorn sheep with differing histories of exposure to genetically diverse strains of Mycoplasma ovipneumoniae (Movi). We monitored clinical signs of disease and sampled animals and their environment to detect spread of Movi among 37 bighorn sheep separated into nine pens based on known exposure Results: We documented Movi transmission within and across pens and we detected Movi DNA in air, water, and invertebrate samples. Higher levels of antibody to Movi prior to the epizootic were associated with a lower likelihood of presenting clinical signs of pneumonia. Nonetheless, higher antibody levels in symptomatic individuals were associated with more severe progressive disease, increased probability and speed of pneumonia-induced mortality, and reduced likelihood of returning to a healthy state. Bighorn sheep with previous exposure to a strain other than the predominant epizootic strain were more likely to recover. Discussion: Our results indicate that Movi-strain variability was sufficient to overwhelm the adaptive host immunological defenses. This outcome indicates, in free-ranging herds, past exposure is likely insufficient to protect bighorn sheep from infection by new Movi strains, although it influences the progression of disease and recovery within the herd. Therefore, given Movi-strain variability and the lack of immunological protection from past exposure, focusing management efforts on minimizing the introduction of Movi into bighorn herds, through separation of domestic and bighorn sheep and avoidance of management activities that create commingling of bighorn sheep carrying differing Movi strains, will likely be the most effective approach for reducing the effects of disease and achieving bighorn sheep conservation goals.

Idaho, Oregon, South Dakota, Washington↗

USGS2020

Life at the frozen limit: Microbial carbon metabolism across a Late Pleistocene permafrost chronosequence

Permafrost is an extreme habitat yet it hosts microbial populations that remain active over millennia. Using permafrost collected from a Pleistocene chronosequence (19 to 33 ka), we hypothesized that the functional genetic potential of microbial communities in permafrost would reflect microbial strategies to metabolize permafrost soluble organic matter (OM) in situ over geologic time. We also hypothesized that changes in the metagenome across the chronosequence would correlate with shifts in carbon chemistry, permafrost age, and paleoclimate at the time of permafrost formation. We combined high-resolution characterization of water-soluble OM by Fourier-transform ion-cyclotron-resonance mass spectrometry (FT-ICR MS), quantification of organic anions in permafrost water extracts, and metagenomic sequencing to better understand the relationships between the molecular-level composition of potentially bioavailable OM, the microbial community, and permafrost age. Both age and paleoclimate had marked effects on both the molecular composition of dissolved OM and the microbial community. The relative abundance of genes associated with hydrogenotrophic methanogenesis, carbohydrate active enzyme families, nominal oxidation state of carbon (NOSC), and number of identifiable molecular formulae significantly decreased with increasing age. In contrast, genes associated with fermentation of short chain fatty acids (SCFAs), the concentration of SCFAs and ammonium all significantly increased with age. We present a conceptual model of microbial metabolism in permafrost based on fermentation of OM and the buildup of organic acids that helps to explain the unique chemistry of ancient permafrost soils. These findings imply long-term in situ microbial turnover of ancient permafrost OM and that this pooled biolabile OM could prime ancient permafrost soils for a larger and more rapid microbial response to thaw compared to younger permafrost soils.

Alaska↗