Scientists in Japan have found a species of bacteria in a cave that exhibits multicellular behavior and a unique two-phase life cycle.
The HS-3 bacterium was isolated from a limestone cave wall that is regularly flooded by an underground river. HS-3 has two distinct life stages; on a solid surface, it self-organizes into a layered colony with liquid-crystal-like properties. The HS-3 colony matures into a semi-closed sphere containing clusters of ‘daughter’ coccobacillus cells, or short rod-shaped cells, which are released upon contact with water.
“The origin of multicellularity is one of the greatest mysteries of life on Earth,” says corresponding author Kouhei Mizuno, a professor at the National Institute of Technology (KOSEN) in Tokyo, Japan. “The point is that we already know the superior function and adaptability of multicellularity, but we know almost nothing about its origins. Established function and adaptability are not necessarily their own formative driving forces. A curiosity of multicellularity is the conflict between “individual advantage” and “group advantage” that must have existed in the early phase of the evolutionary transition. We don’t have a good existing model to study multicellularity, other than theoretical models.”
One such model, called the “ecological framework,” asserts that the environment exerts selection pressures on an evolving population, and argues that Darwinian natural selection is still applicable to unicellular organisms.
Mizuno and his lab student Ohta identified HS-3 in 2008 from dripping water on a limestone cave wall on Japan’s northern island of Kyushu. They initially looked for lipid accumulating bacteria, but Ohta discovered a small colony of exceptionally beautiful color and texture when examining old bacterial agar plates prior to disposal. Due to their disorganized structure, most bacteria on agar have an opaque texture, however, this colony was transparent and had an iridescent hue. Phenotypic comparisons with closely related species confirmed this colony as a new species, HS-3, which the scientists named Jeongeupia sacculi (means “cradle”).
The team used microscopy to analyze colony growth. The cells simply began to reproduce as coccobacilli, but the occurrence of cell elongation caused the colony to form a monolayer structure oriented like a liquid crystal. Bulges form especially at the edge of the colony, relieving internal pressure and giving HS-3 the unique ability to maintain this two-dimensional fluid arrangement over an extended period of time, which may be a prerequisite for HS-3 to establish multicellular behavior.
Then the colony expanded to form additional layers. The inner filamentous cells collapsed, creating whorl-structured domains. These domains and the liquid crystal-like arrangement explain the transparency observed in HS-3 colonies on agar. After two days, cells proliferated rapidly inside, and the colony began to swell three-dimensionally, forming a semi-closed sphere housing the Coccobacillus cells. By day five, the internal cells had been displaced from the colony, triggering a chain reaction of this event in neighboring colonies, thereby indicating some multicellular control.
Because the sampling site on HS-3’s cave wall was regularly exposed to flowing water in the cave, the team submerged the mature hemispherical colonies in water. The inner coccobacilli were released into the water leaving behind the filamentous cell architecture. By plating these daughter cells on fresh agar, they discovered that the cells were able to reproduce the original filamentous structure, showing that the two distinct phases of the HS-3 life cycle are reversible and possibly due to the changing conditions originated in the cave.
“It took us 10 years to be sure that it wasn’t a contamination of two different species and not just a mutation,” says Mizuno. “First, we filmed the entire process from a single cell to a colony using a series of microscopic observations, for which we developed our own methods. Then we found that the morphological changes in cells and colonies were both controlled and reversible. These data led us to believe that HS-3 is ‘multicellular’.”
“The first phase of the life cycle of HS-3 suggests that the liquid crystal-like organism is involved in the formation of multicellularity, which has not been previously reported. The existence of the second life stage implies the involvement of the dynamic aquatic environment in the emergence of HS-3 multicellularity,” says co-corresponding author Kazuya Morikawa, professor in the Department of Biomedical Sciences, Tsukuba University, Japan.
“We were surprised by the several curious properties exhibited by HS-3, one of which is that the multicellular behavior of this new species fits well with the recently proposed ‘ecological scaffolding’ hypothesis. We now think that the leap to multicellularity would be a more involved and beautiful process than we previously imagined,” commented Mizuno and Morikawa.
Reference: “Novel Multicellular Prokaryote Discovered Beside an Underground Stream” by Kouhei Mizuno, Mais Maree, Toshihiko Nagamura, Akihiro Koga, Satoru Hirayama, Soichi Furukawa, Kenji Tanaka and Kazuya Morikawa, October 11, 2022, eLife.
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