Abstract
BackgroundPupfishes frequently enter paradoxical anaerobism in response to endogenously produced or exogenously supplied ethanol in a dose-dependent manner. To decipher the role of the gut microbiota in ethanol-associated paradoxical anaerobism, gut microbial communities were depleted using a cocktail of antibiotics and profiled using 16S rRNA gene sequencing.ResultsCompared to the control group (n = 12), microbiota-depleted fish (n = 12) spent more time in paradoxical anaerobism. Our analysis indicated that the bacterial phyla Proteobacteria, Fusobacteria, Bacteroidetes, Firmicutes, Actinobacteria, Patescibacteria, and Dependentiae dominated the pupfish gut, which is consistent with other fish gut microbiota. Although the gut microbial communities with and without antibiotic treatment were similarly diverse, they were distinct and the greatest contribution to the dissimilarity (27.38%) was the common fish commensal Cetobacterium.ConclusionsThis study reports the first characterization of gut microbial communities of pupfish and suggests the microbiome may play a critical role in regulating metabolic strategies that are critical for survival in extremes of temperature and oxygen concentration. We speculate that Cetobacterium, a primary fermenter, also consumes ethanol through secondary fermentation via an alcohol dehydrogenase and therefore regulates the transition from paradoxical anaerobism to aerobic respiration in fish. Given the wide distribution and abundance of Cetobacterium in warm-water fishes, this process may be of broad importance, and suggests that the microbiome be carefully considered for both conservation and aquaculture.
Highlights
Pupfishes frequently enter paradoxical anaerobism in response to endogenously produced or exogenously supplied ethanol in a dose-dependent manner
Exposure to antibiotics led to increased time in paradoxical anaerobism Exposure to a cocktail of antibiotics made fish more prone to entering paradoxical anaerobism (Fig.1)
Pupfish exposed to antibiotics and ethanol spent 40.5 ± 11.3% of the post-ethanol time in paradoxical anaerobism - approximately 3.6X longer than did control fish (Fig.1b)
Summary
Pupfishes frequently enter paradoxical anaerobism in response to endogenously produced or exogenously supplied ethanol in a dose-dependent manner. To decipher the role of the gut microbiota in ethanolassociated paradoxical anaerobism, gut microbial communities were depleted using a cocktail of antibiotics and profiled using 16S rRNA gene sequencing. We demonstrated that two lineages of pupfishes reared at 33 °C frequently entered a state of paradoxical anaerobism [2, 3]. Pupfish (2020) 2:20 dependent anion channels (VDACs) in living pupfish and the phenotype of paradoxical anaerobism [2] (see discussion for details). If our model is correct, changes in ethanol metabolism should affect use of paradoxical anaerobism. Our earlier work measuring ethanol accumulation by 28 °C- and 33 °C-acclimated fish suggested a microbial interaction. Measuring ethanol accumulation in a sealed container with fish required us to pre-boil aquarium water, rinse the fish, and ensure the fish did not defecate or swim vigorously during the assay; rapid reduction of exogenous ethanol in the water otherwise occurred [2]
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