Dataset Information

Widespread use of emersion and cutaneous ammonia excretion in Aplocheiloid killifishes.

ABSTRACT: The invasion of land required amphibious fishes to evolve new strategies to avoid toxic ammonia accumulation in the absence of water flow over the gills. We investigated amphibious behaviour and nitrogen excretion strategies in six phylogenetically diverse Aplocheiloid killifishes (Anablepsoides hartii, Cynodonichthys hildebrandi, Rivulus cylindraceus, Kryptolebias marmoratus, Fundulopanchax gardneri, and Aplocheilus lineatus) in order to determine if a common strategy evolved. All species voluntarily emersed (left water) over several days, and also in response to environmental stressors (low O2, high temperature). All species were ammoniotelic in water and released gaseous ammonia (NH3 volatilization) during air exposure as the primary route for nitrogen excretion. Metabolic depression, urea synthesis, and/or ammonia accumulation during air exposure were not common strategies used by these species. Immunostaining revealed the presence of ammonia-transporting Rhesus proteins (Rhcg1 and Rhcg2) in the skin of all six species, indicating a shared mechanism for ammonia volatilization. We also found Rhcg in the skin of several other fully aquatic fishes, implying that cutaneous ammonia excretion is not exclusive to amphibious fishes. Overall, our results demonstrate that similar nitrogen excretion strategies while out of water were used by all killifish species tested; possibly the result of shared ancestral amphibious traits, phenotypic convergence, or a combination of both.

SUBMITTER: Livingston MD

PROVIDER: S-EPMC6111154 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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Publications

Widespread use of emersion and cutaneous ammonia excretion in Aplocheiloid killifishes.

Livingston Michael D MD Bhargav Vikram V VV Turko Andy J AJ Wilson Jonathan M JM Wright Patricia A PA

Proceedings. Biological sciences 20180815 1884

The invasion of land required amphibious fishes to evolve new strategies to avoid toxic ammonia accumulation in the absence of water flow over the gills. We investigated amphibious behaviour and nitrogen excretion strategies in six phylogenetically diverse Aplocheiloid killifishes (Anablepsoides hartii, Cynodonichthys hildebrandi, Rivulus cylindraceus, Kryptolebias marmoratus, Fundulopanchax gardneri, and Aplocheilus lineatus) in order to determine if a common strategy evolv ...[more]

PMID: 30111602

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Project description:Ammonia tolerance is a universal characteristic among the ammonia-oxidizing bacteria (AOB); in contrast, the known species of ammonia-oxidizing archaea (AOA) have been regarded as ammonia sensitive, until the identification of the genus "Candidatus Nitrosocosmicus." However, the mechanism of its ammonia tolerance has not been reported. In this study, the AOA species "Candidatus Nitrosocosmicus agrestis," obtained from agricultural soil, was determined to be able to tolerate high concentrations of NH3 (>1,500 μM). In the genome of this strain, which was recovered from metagenomic data, a full set of genes for the pathways of polysaccharide metabolism, urea hydrolysis, arginine synthesis, and polyamine synthesis was identified. Among them, the genes encoding cytoplasmic carbonic anhydrase (CA) and a potential polyamine transporter (drug/metabolite exporter [DME]) were found to be unique to the genus "Ca. Nitrosocosmicus." When "Ca. Nitrosocosmicus agrestis" was grown with high levels of ammonia, the genes that participate in CO2/HCO3- conversion, glutamate/glutamine syntheses, arginine synthesis, polyamine synthesis, and polyamine excretion were significantly upregulated, and the polyamines, including putrescine and spermidine, had significant levels of production. Based on genome analysis, gene expression quantification, and polyamine determination, we propose that the production and excretion of polyamines is probably one of the reasons for the ammonia tolerance of "Ca. Nitrosocosmicus agrestis," and even of the genus "Ca. Nitrosocosmicus."IMPORTANCE Ammonia tolerance of AOA is usually much lower than that of the AOB, which makes the AOB rather than AOA a predominant ammonia oxidizer in agricultural soils, contributing to global N2O emission. Recently, some AOA species from the genus "Ca. Nitrosocosmicus" were also found to have high ammonia tolerance. However, the reported mechanism for the ammonia tolerance is very rare and indeterminate for AOB and for AOA species. In this study, an ammonia-tolerant AOA strain of the species "Ca. Nitrosocosmicus agrestis" was identified and its potential mechanisms for ammonia tolerance were explored. This study will be of benefit for determining more of the ecological role of AOA in agricultural soils or other environments.

Dataset Information

Widespread use of emersion and cutaneous ammonia excretion in Aplocheiloid killifishes.

Publications

Widespread use of emersion and cutaneous ammonia excretion in Aplocheiloid killifishes.

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