Cells of most bacterial species are around 2 micrometers in length, with some of the largest specimens reaching 750 micrometers. The newly-discovered species, named Candidatus (Ca.) Thiomargarita magnifica, has an average cell length greater than 9,000 micrometers and is visible to the naked eye.
Single filament of Ca. Thiomargarita magnifica. Image credit: Jean-Marie Volland.
“Bacteria and archaea are the most diverse and abundant organisms on Earth,” said Université des Antilles Professor Olivier Gros and colleagues.
“With only a small fraction of them isolated in culture, we remain grossly ignorant of their biology.”
“While most model bacteria and archaea are small, some remarkably large cells, referred to as giant bacteria, are evident in at least four phyla, and have cellular sizes in the range of tens or even hundreds of microns.”
“Some exceptional members of sulfur-oxidizing gammaproteobacteria Thiomargarita namibiensis, for instance, are known to reach up to 750 micrometers (average size – 180 micrometers),” they said.
“Such bacterial giants raise the question of whether more macro-bacteria might still be out there but have not yet been identified.”
The newly-described species, Ca. Thiomargarita magnifica, dwarfs all other known giant bacteria by about 50-fold.
It was first discovered in 2009 in shallow tropical marine mangroves in Guadeloupe, Lesser Antilles.
“When I saw them, I thought, ‘strange’,” Professor Gros said.
“In the beginning I thought it was just something curious, some white filaments that needed to be attached to something in the sediment like a leaf.”
“I thought they were eukaryotes; I didn’t think they were bacteria because they were so big with seemingly a lot of filaments,” said Dr. Silvina Gonzalez-Rizzo, a researcher at the Université des Antilles.
“We realized they were unique because it looked like a single cell. The fact that they were a ‘macro’ microbe was fascinating!”
Morphology and ultrastructure of Ca. Thiomargarita magnifica: (A) size comparison of selected bacterial (green) and eukaryotic (blue) model systems on a log scale; (B) light microscopy montage of the upper half of a Ca. Thiomargarita magnifica cell, with a broken basal part revealing a tube-like morphology due to the large central vacuole and numerous spherical intracellular sulfur granules (a tardigrade is shown for scale); (C) 3D rendering of segmented cells from HXT and CLSM, putatively at various stages of the developmental cycle; from left to right 3D rendered cells are cell D, B, F, G, and D; note smallest stage correspond to cell D terminal segment and was added to the left for visualization purposes; (D) CLSM observation of cell K after fluorescent labeling of membranes with FM 1-43x showing the continuity of the cell from the basal pole to the first complete constriction at the apical end; (E) TEM montage of the apical constriction of a cell, with the cytoplasm constrained to the periphery; (F) higher magnification of the area marked in E, with sulfur granules and pepins at various stages of development; (G) higher magnification of the area marked in E showing two pepins (arrowheads). Abbreviations: S – sulfur granule, V – vacuole. Image credit: Volland et al., doi: 10.1126/science.abb3634.
Using various microscopy techniques, such as hard X-ray tomography, confocal laser scanning microscopy and transmission electron microscopy, the researchers visualized entire filaments up to 9.66 mm long and confirmed that they were indeed giant single cells rather than multicellular filaments, as is common in other large sulfur bacteria.
The techniques also allowed the scientists to observe novel, membrane-bound compartments that contain DNA clusters.
They dubbed these organelles pepins, after the small seeds in fruits. DNA clusters were plentiful in the single cells.
“Ca. Thiomargarita magnifica contains three times more genes than most bacteria and hundreds of thousands of genome copies (polyploidy) that are spread throughout the entire cell,” said Dr. Jean-Marie Volland, a researcher at DOE’s Joint Genome Institute, Lawrence Berkeley National Laboratory and the Laboratory for Research in Complex Systems.
For the team, characterizing Ca. Thiomargarita magnifica has paved the way for multiple new research questions. Among them, is the bacterium’s role in the mangrove ecosystem.
“In terms of metabolism, it does chemosynthesis, which is a process analogous to photosynthesis for plants,” Dr. Volland said.
Another outstanding question is whether the pepins played a role in the evolution of Ca. Thiomargarita magnifica’s extreme size, and whether or not pepins are present in other bacterial species.
The precise formation of pepins and how molecular processes within and outside of these structures occur and are regulated also remain to be studied.
“Through its gigantic cell size, its large genome, its di-morphic life cycle, but most importantly through its compartmentalization of genetic material in membrane-bound pepins, Ca. Thiomargarita magnifica adds to the list of bacteria that have evolved a higher level of complexity,” the authors said.
“It is the first and only bacteria known to date to unambiguously segregate their genetic material in membrane-bound organelles in the manner of eukaryotes and therefore challenges our concept of a bacterial cell.”
The team’s paper was published in the journal Science.
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Jean-Marie Volland et al. 2022. A centimeter-long bacterium with DNA contained in metabolically active, membrane-bound organelles. Science 376 (6600): 1453-1458; doi: 10.1126/science.abb3634
