Stress in a hot place: Ecogenomics and phylogeography in a pantropical sentinel inhabiting multi-stressor volcanic soils

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Understanding of how any metazoan organism tolerates an extreme environment comprised of multiple stressors may help to predict the impacts of current and future multifaceted global change on biodiversity and ecological function. Active volcanic soils represent extreme environments with unique features: elevated metal-ion concentrations, constant degassing over a wide area, and high temperature. Elevated soil temperature, as well as low O2, high CO2, and acidified soil are inhospitable challenges to the resident biota. The present proposal will derive a mechanistic understanding of the adaptation of an ecologically-relevant, ecosytem engineering, soil-dwelling invasive earthworm species (Amynthas gracilis) to cocktails of physico-chemical stressors of natural origin. Furthermore, the observations on this metazoan life-form with extremophile traits will have applications in the bioeconomy (biotechnology, agriculture and vermicomposting), medicine (models for anoxia & hypercapnia), and environmental management (ecotoxicology, risk assessment, land reclamation). Furnas, a rural parish on São Miguel in the Azores, is situated inside a caldera of an active volcano. Persistent volcanic activity at Furnas creates a soil presenting three formidable life-threatening challenges: locally low O2 (10%) and high CO2 levels (54%), high temperatures (37oC), and elevated metal concentrations rendered bioavailable due to soil acidification (pH 5.8). It is astounding that this extreme soil supports a viable population of A. gracilis. [It is noteworthy that CO2 concentrations greater than 17% leads death within 1 minute in exposed humans.] The aim of this project is to investigate specific functional aspects of how this soil-dwelling multi-cellular animal tolerates the inhospitable conditions of active volcanic soils.We will investigate the molecular and physiological responses of populations of A. gracilis under three discrete scenarios:i) earthworms sampled directly from inactive and actively volcanic soils;ii) earthworms transplanted from volcanically active to microcosms located in non-active soils, and vice versa; and iii) a series of laboratory 'exposures' representing every combination of the three chemical/physical challenges encountered in the field (i.e. singular or combinatorial). Our observations will encompass the following: - Comprehensive soil analyses to allow modeling of metal availability for uptake by the earthworms. - Profiling gene expression to reveal how the earthworm regulates its transcriptome enabling it to tolerate the severe challenges presented by active volcanism. - Computational interrogation of genetic data to identify mutations in functionally significant target genes involved in metal stress, thermo-tolerance, CO2 metabolism, and hypoxia.- Measuring the expression level of a conserved gene known as "Hypoxia-Induced Factor" (HIF) which previous studies indicate is paramount in regulating responses to hypoxia, thermal stress, and metal toxicity in vertebrates.- Measuring the expression of genes belonging to the 'heat-shock' superfamily of stress-response chaperones.- Biochemical and physiological measurements to determine the efficiency of O2 transport across the body wall, and the amount and O2-affinity properties of the haemoglobin. - Measuring diurnal changes in the O2 consumption and ATP production rates of Amynthas to establish whether behavior and physiology are modified in active volcanic soils.In parallel, we propose to support a PhD student to determine the genetic structure of A. gracilis populations in the Azores, and (through collaboration) in Asia (Laos, Korea, Thailand, South China), the region of origin of the cosmopolitan species. The studentship will also study the organism's reproduction, reported to be predominately asexual (parthenogenetic), and the implications of this for a species that is a successful invasive colonizer across a wide circum-tropical range.