The exceptional form and function of the giant bacterium Ca. Epulopiscium viviparus revolves around its sodium motive force

spp. are the largest known heterotrophic bacteria; a large cigar-shaped individual is a million times the volume of . To better understand the metabolic potential and relationship of sp. type B with its host , we generated a high-quality draft genome from a population of cells taken from a single fi...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2023-12, Vol.120 (52), p.e2306160120
Main Authors: Sannino, David R, Arroyo, Francine A, Pepe-Ranney, Charles, Chen, Wenbo, Volland, Jean-Marie, Elisabeth, Nathalie H, Angert, Esther R
Format: Article
Language:English
Subjects:
Acetic acid
Adenosine Triphosphate - metabolism
Algae
Animals
ATP
Bacteria
Bacteria - metabolism
Biological Sciences
Candidatus Epulopiscium viviparus
Carbohydrates
Cell membranes
Cellular Biology
Clostridiales - metabolism
Decarboxylation
E coli
Flagella
Genetics
Genomes
Heterotrophic bacteria
Intestine
Life Sciences
Membrane proteins
Metabolism
Natural populations
Polyploidy
Polysaccharides
Populations
Saccharides
Sodium
Sodium - metabolism
Substrates
Symbiosis
Transcriptomes
Vacuolar Proton-Translocating ATPases - metabolism
Vitamins
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Summary:spp. are the largest known heterotrophic bacteria; a large cigar-shaped individual is a million times the volume of . To better understand the metabolic potential and relationship of sp. type B with its host , we generated a high-quality draft genome from a population of cells taken from a single fish. We propose the name Epulopiscium viviparus to describe populations of this best-characterized species. Metabolic reconstruction reveals more than 5% of the genome codes for carbohydrate active enzymes, which likely degrade recalcitrant host-diet algal polysaccharides into substrates that may be fermented to acetate, the most abundant short-chain fatty acid in the intestinal tract. Moreover, transcriptome analyses and the concentration of sodium ions in the host intestinal tract suggest that the use of a sodium motive force (SMF) to drive ATP synthesis and flagellar rotation is integral to symbiont metabolism and cellular biology. In natural populations, genes encoding both F-type and V-type ATPases and SMF generation via oxaloacetate decarboxylation are among the most highly expressed, suggesting that ATPases synthesize ATP and balance ion concentrations across the cell membrane. High expression of these and other integral membrane proteins may allow for the growth of its extensive intracellular membrane system. Further, complementary metabolism between microbe and host is implied with the potential provision of nitrogen and B vitamins to reinforce this nutritional symbiosis. The few features shared by all bacterial behemoths include extreme polyploidy, polyphosphate synthesis, and thus far, they have all resisted cultivation in the lab.
ISSN:0027-8424
1091-6490
1091-6490
DOI:10.1073/pnas.2306160120