Epulopiscium

Epulopiscium spp. are a group of Gram-positive bacteria that have a symbiotic relationship with surgeonfish. These bacteria are known for their unusually large size, many ranging from 200–700 μm in length. Until the discovery of Thiomargarita namibiensis in 1999, Epulopiscium spp. were thought to be the largest bacteria.[1][2] They are still the largest known heterotrophic bacteria.

Epulopiscium
Scientific classification
Kingdom:
Bacteria
Phylum:
Firmicutes
Class:
Clostridia
Order:
Clostridiales
Genus:
Epulopiscium

In addition to their large size, Epulopiscium, commonly referred to as "epulos," are morphologically diverse and extremely polyploid.[3] Epulos also have unique reproductive strategies in which certain cells can form intracellular offspring, similar to microbial sporulation; furthermore, several epulo morphologies exhibit sporulation.

While the bacteria have not been successfully grown in the lab, scientists have gained a better understanding of Epulopiscium spp. through microscopic, phylogenetic, and genomic analyses.

Naming and discovery

Epulopiscium means "a guest at a banquet of fish" in Latin, from epulum ("feast" or "banquet") and piscium ("of a fish"),[4] as the organism was found inside the gut of marine surgeonfish. Epulopiscium cells were initially classified as protists on the basis of their large size and unusual ultrastructure.

Originally, Epulopiscium populations were thought to be a single species and given the name Epulopiscium fishelsoni in 1988, by Montgomery (one of the co-discovers) and Pollak. The epithet fishelsoni honors Lev Fishelson, a Polish-born Israeli ichthyologist[5][6] who was part of the group that made the discovery while studying the intestines of a brown surgeonfish from the Red Sea in 1985.[7]

Later, however, Epulopiscium fishelsoni was shown to comprise two phylogenetically distinct groups of bacteria by Angert and collaborators using rRNA gene sequence comparisons.[1] Subsequent studies illustrated the relationship between these symbionts and the host surgeonfish.

Physiology

The largest Epulopiscium cells can be seen with the naked eye. However, because of their size, Epulopiscium spp. must compensate for their small surface-to-volume ratio, compared to other bacteria. One distinct feature is the cell membrane, which contains many folds to increase the effective surface area.

Additionally, Epulopiscium spp. are extremely polyploid, with individuals containing hundreds of thousands of copies of the genome. Since bacteria rely on diffusion rather than cytoskeletal transport as in eukaryotes, this extreme polyploidy allows for the production of gene products at numerous sites in the cell to produce biomolecules where they are needed.

Reproduction
Epulopiscium spp. type B life cycle.[8]

The largest Epulopiscium morphologies exhibit a unique viviparous reproduction. This unusual and derived form of sporulation produces anywhere from one to twelve daughter cells that grow inside of the parent cell, until the parent eventually lyses, and dies.[9][10] These cells appear to not use binary fission for reproduction. Some morphologies use endospore formation for reproduction.[11] However, there are some smaller morphologies that reproduce through binary fission and spore formation.

Although sporulation is widespread among other bacteria (such as Bacillus subtilis and Clostridium spp.) in the phylum Firmicutes, spore formation is usually brought about by overcrowding, the accumulation of toxins in the environment, or starvation, rather than a standard form of reproduction. The production of multiple endospores has been observed in other large gut symbionts such as Metabacterium polyspora, which are phylogenetically related to Epulopiscium spp. Since sporulation affords bacteria much more protection from the outside environment than binary fission, it is thought that the evolution of this unusual life cycle may assist transfer of the bacteria from one host to another.

Symbiosis

Epulopiscium spp. and their surgeonfish hosts are suggested to have a nutritional symbiotic relationship: Epulopiscium spp. have only been found in surgeonfish that eat algae and detritus. It is suggested that Epulopiscium spp. assist in the fish's digestion[12]. However, scientists have been unable to culture Epulopiscium outside of its natural habitat.

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References
  1. Angert ER, Clements KD, Pace NR (1993). "The largest bacterium". Nature. 362 (6417): 239–241. Bibcode:1993Natur.362..239A. doi:10.1038/362239a0. PMID 8459849.
  2. Angert ER, Brooks AE, Pace NR (1996). "Phylogenetic analysis of Metabacterium polyspora: Clues to the evolutionary origin of Epulopiscium spp., the largest bacteria". Journal of Bacteriology. 178 (5): 1451–6. doi:10.1128/jb.178.5.1451-1456.1996. PMC 177821. PMID 8631724.
  3. Hutchison, Elizabeth; Yager, Nicholas A.; Taw, May N.; Taylor, Matthew; Arroyo, Francine; Sannino, David R.; Angert, Esther R. (2018). "Developmental stage influences chromosome segregation patterns and arrangement in the extremely polyploid, giant bacterium Epulopiscium sp. type B". Molecular Microbiology. 107 (1): 68–80. doi:10.1111/mmi.13860. ISSN 1365-2958. PMID 29024073.
  4. Prescott, Lansing M.; Sherwood, Linda M.; Woolverton, Christopher J. (2006). "Procaryotic Cell Structureand Function" (PDF). Microbiology. p. 43.
  5. Goren, Menachem (2013). "Professor Lev Fishelson, renowned and respected biologist 1923-2013". Israel Journal of Ecology & Evolution. 59 (3): 164. doi:10.1080/15659801.2013.899808.
  6. "Professor Emeritus, Lev Fishelson". Dept. of Zoology, Faculty of Life Sciences. Tel Aviv University.
  7. Fishelson, Lev; Montgomery, W. Linn; Myrberg, A.A. (1985). "A unique symbiosis in the gut of tropical herbivorous surgeonfishes (Acanthuridae: Teleostei) from the Red Sea". Science. 229 (4708): 49–51. Bibcode:1985Sci...229...49F. doi:10.1126/science.229.4708.49. PMID 17795131.
  8. Angert, Esther R.; Choat, J. Howard; Clements, Kendall D.; Mendell, Jennifer E. (2008-05-06). "Extreme polyploidy in a large bacterium". Proceedings of the National Academy of Sciences. 105 (18): 6730–6734. doi:10.1073/pnas.0707522105. ISSN 0027-8424. PMC 2373351. PMID 18445653.
  9. Angert ER, Clements KD (2004). "Initiation of intracellular offspring in Epulopiscium". Molecular Microbiology. 51 (3): 827–835. doi:10.1046/j.1365-2958.2003.03869.x. PMID 14731282. S2CID 19426788.
  10. "Intracellular offspring production by some Firmicutes". The Epulopiscium Website. Cornell Dept. of Microbiology.
  11. Angert, Esther R. (March 2005). "Alternatives to binary fission in bacteria". Nature Reviews. Microbiology. 3 (3): 214–224. doi:10.1038/nrmicro1096. ISSN 1740-1526. PMID 15738949.
  12. Pollak, Peggy E.; Montgomery, W. Linn (1994-08-01). "Giant bacterium (Epulopiscium fishelsoni ) influences digestive enzyme activity of an herbivorous surgeonfish (Acanthurus nigrofuscus)". Comparative Biochemistry and Physiology Part A: Physiology. 108 (4): 657–662. doi:10.1016/0300-9629(94)90352-2. ISSN 0300-9629.

Further reading
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