Giant bacteria are intriguing, underexplored biological enigmas. Many well-studied giants use abundant internal small-molecule stores and/or light to satisfy their oversized energy demands. However, the ways giant heterotrophs (organisms that cannot produce its own food, instead taking nutrition from other sources of organic carbon) fulfill their expanded needs remain elusive. Bacteria of the genus Epulopiscium are intestinal symbionts of tropical marine surgeonfish that are exceptional and unique in the bacterial world. They are the largest known heterotrophic bacteria — a large cigar-shaped individual is a million times the volume of Escherichia coli. To determine how Epulopiscium bacteria fuel their robust metabolism, biologists generated a high-quality draft genome of Epulopiscium viviparus and reconstructed its metabolic potential using a comprehensive approach.
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Confocal micrograph of Epulopiscium viviparus. Image credit: Sannino et al., doi: 10.1073/pnas.2306160120.
“This incredible giant bacterium is unique and interesting in so many ways: its enormous size, its mode of reproduction, the methods by which it meets its metabolic needs and more,” said Cornell University Professor Esther Angert, senior authors of the study.
“Revealing the genomic potential of this organism just kind of blew our minds.”
First discovered in 1985, Epulopiscium bacteria live symbiotically within the intestinal tracts of surgeonfish in the family Acanthuridae in tropical marine coral reef environments, such as the Great Barrier Reef and in the Red Sea.
Because of its gargantuan size, scientists initially believed it was some distinct type of protozoan.
“Studying these giant bacteria requires capturing the fish in which they live and preserving the cells or extracting DNA and RNA as quickly and carefully as possible,” Professor Angert said.
Professor Angert and her colleagues were especially interested to learn how Epulopiscium viviparus fuels its extreme metabolic needs.
Bacteria that feed off nutrients in their environment, rather than creating their own energy from sunlight, generally fall into two camps: those that have access to oxygen and those that don’t.
“Without oxygen, bacteria often use fermentation to extract energy, and fermenting organisms just don’t get as much bang for the buck from nutrients,” Professor Angert said.
Seeing that Epulopiscium viviparus is indeed a fermenter just made the puzzle larger, as its huge size, extreme reproduction and ability to swim would all require more energy, not less.
The researchers discovered that Epulopiscium viviparus has modified its metabolism to make the most of its environment, by using a rare method to make energy and to move (the same swimming method is used by the bacteria that cause cholera), and by devoting a huge portion of its genetic code to making enzymes that can harvest the nutrients available in its host’s gut.
Among the most highly produced enzymes are those used to make ATP, the energy currency of all cells.
A highly folded membrane that runs along the outer edge of Epulopiscium viviparus provides important space for the energy-producing and -transporting proteins, with some surprising similarities to how mitochondria function in the cells of more complex organisms.
“We all know that phrase ‘the mitochondria are the powerhouse of the cell,’ and amazingly, these membranes in Epulopiscium viviparus have kind of converged on the same model as the mitochondria,” Professor Angert said.
“They have a highly folded membrane that increases surface area where these energy-producing pumps can work, and that increased surface area creates a powerhouse of energy.”
“This basic research has a host of potential future applications, particularly as Epulopiscium viviparus has such effective strategies to make use of the nutrients found in algae.”
“Algae is a growing target for livestock feeds, renewable energy and human nutrition, since its growth doesn’t compete with land-based agriculture.”
The study appears in the Proceedings of the National Academy of Sciences.
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David R. Sannino et al. 2023. The exceptional form and function of the giant bacterium Ca. Epulopiscium viviparus revolves around its sodium motive force. PNAS 120 (52): e2306160120; doi: 10.1073/pnas.2306160120
