Identification of the Gut Microbiome and its Role in Paradoxical Anaerobism in Desert Pupfish

Abstract

The Devils Hole pupfish (Cyprinodon diabolis) frequently enters paradoxical anaerobism (PA) in response to endogenously produced or exogenously supplied ethanol in a dose‐dependent manner. PA is characterized by extended periods (e.g. up to 149 min continuous) of negligible oxygen consumption despite its availability. To decipher the role of the gut microbiota in ethanol‐associated paradoxical anaerobism, gut microbial communities of pupfish were depleted using a cocktail of antibiotics. Compared to the fish in the control group, microbiota‐depleted fish spent more time in paradoxical anaerobism. 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. Although Cetobacterium is known as a primary fermenter, we speculate that it may consume ethanol through secondary fermentation and therefore regulate transition from paradoxical anaerobism to aerobic respiration, thereby playing a critical role in regulating the metabolic status of these fish. This study reports the first characterization of gut microbial communities of critically endangered 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. 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 conservation and aquaculture alike.