Abstract
Strictly anaerobic Prevotella spp. are characterized by their vast metabolic potential. As members of the Prevotellaceae family, they represent the most abundant organisms in the rumen and are typically found in monogastrics such as pigs and humans. Within their largely anoxic habitats, these bacteria are considered to rely primarily on fermentation for energy conservation. A recent study of the rumen microbiome identified multiple subunits of the Na+-translocating NADH:quinone oxidoreductase (NQR) belonging to different Prevotella spp. Commonly, the NQR is associated with biochemical energy generation by respiration. The existence of this Na+ pump in Prevotella spp. may indicate an important role for electrochemical Na+ gradients in their anaerobic metabolism. However, detailed information about the potential activity of the NQR in Prevotella spp. is not available. Here, the presence of a functioning NQR in the strictly anaerobic model organism P. bryantii B14 was verified by conducting mass spectrometric, biochemical, and kinetic experiments. Our findings propose that P. bryantii B14 and other Prevotella spp. retrieved from the rumen operate a respiratory NQR together with a fumarate reductase which suggests that these ruminal bacteria utilize a sodium motive force generated during respiratory NADH:fumarate oxidoreduction.
Highlights
Gram-negative, obligate anaerobic bacteria of the Prevotellaceae family represent the prevailing and most numerous species within the rumen [1,2,3] and commonly occur in the intestinal tract of humans and pigs [4,5,6]
A comprehensive study investigated the rumen microbiome and quantified a total of 8163 bacterial proteins in three distinct rumen fractions of three individual cows that were fed rotationally with varying diets [17] which revealed that a major part of 1881 proteins belonged to the family of Prevotellaceae of which 49 proteins were assigned to P. bryantii B14 (Table S1)
About 72% of the Prevotellaceae-derived proteins were predicted to be cytoplasmic proteins, above 15% belonged to the periplasmic space, and 10% were assigned to inner and outer membrane proteins (Figure 1A and Table S1) which emphasized the capability of mass spectrometry-based analyses to identify subunits of membrane-associated proteins [38]
Summary
Gram-negative, obligate anaerobic bacteria of the Prevotellaceae family represent the prevailing and most numerous species within the rumen [1,2,3] and commonly occur in the intestinal tract of humans and pigs [4,5,6]. Members of the Prevotellaceae family exhibit versatile metabolic capabilities such as the utilization of peptides, proteins, monosaccharides, and non-structural plant polysaccharides [7,8,9]. As a representative of the Prevotellaceae family, the type strain Prevotella bryantii B14, isolated from the rumen [10], is likewise a typical inhabitant of digestive tract ecosystems. When P. copri is grown in defined minimal medium with glucose as sole carbon source, glycolysis represents the major fermentative pathway coupling the respiratory NADH:fumarate oxidoreduction with the redox cycling of ferredoxin [15]
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