Hidden deep in a cave – Discovery of a unique new species of bacteria

An image of an HS-3 plated colony, showing the characteristic transparent and iridescent appearance. 1 credit

Japanese scientists have discovered a type of bacteria in a cave that exhibits multicellular behavior and a unique two-phase life cycle.

The bacterium, HS-3, was isolated from a limestone cave wall that is periodically submerged by an underground river. HS-3 has two different life phases; on a solid surface, it self-organizes into a layered structured colony with liquid crystal-like qualities. The HS-3 colony matures into a semi-enclosed sphere that contains clusters of “daughter” coccobacillus cells, or short rod-shaped cells, which are released upon contact with water.

“The emergence of multicellularity is one of the greatest mysteries of life on Earth,” says corresponding author Kouhei Mizuno, professor at the National Institute of Technology (KOSEN), Tokyo, Japan. “The fact is that we already know the higher function and adaptability of multicellularity, but we know next to nothing of its origins. Established function and adaptability are not necessarily their own formative driving force. multicellularity is the conflict between the “benefits of individuals” and the “benefit of the group” that must have existed at the beginning of the evolutionary transition.We do not have a good existing model to study multicellularity, except for theoretical models .

One such model, called “ecological scaffolding”, argues that the environment exerts selection pressure on a developing population, arguing that Darwinian natural selection is still applicable to single-celled organisms.

Mizuno and his lab student Ohta identified HS-3 from water drops on a limestone cave wall on the island of Kyushu in northern Japan in 2008. They were initially looking for lipid-accumulating bacteria, but Ohta discovered a small colony with extraordinarily beautiful color and texture upon inspection. old bacterial agar plates before disposal. Due to their disorganized structure, most bacteria on agar have an opaque texture, however, this colony was transparent and had an iridescent tint. Phenotypic comparisons with closely related species confirmed that this colony was a new species, HS-3, which the scientists named Jeongeupia bag (meaning “cradle”).

The team used microscopy to analyze colony growth. The cells began to reproduce simply as coccobacilli, but the onset of cell elongation caused the colony to form a single-layer structure, oriented like a liquid crystal. Bulges form especially at the edge of the colony, relieving internal pressure and granting HS-3 the unique ability to maintain this two-dimensional liquid arrangement for an extended period of time, which may be a prerequisite for HS-3 to establish a multicellular behavior.

Then the colony then grew to form additional layers. The inner filamentous cells deformed, generating vortex-structured domains. These domains and the liquid crystal-like arrangement explain the transparency observed in HS-3 colonies on agar. After two days, rapid cell reproduction occurred inside and the colony began to swell three-dimensionally, forming a semi-closed sphere housing the coccobacillus cells. After the fifth day, the inner cells were crowded out of the colony, triggering a chain reaction of this event in adjacent colonies and thus indicating some multicellular control.

Since the cave wall sampling site of HS-3 was regularly subject to the flow of water into the cave, the team submerged the mature semi-spherical colonies in water. The inner coccobacilli were released into the water, leaving behind the filamentous cell architecture. By placing these daughter cells on fresh agar, they found that the cells were able to replicate the original filamentous structure, showing that the two distinct phases of the HS-3 life cycle are reversible and may have arisen due changing conditions inside the cave. .

“It took us 10 years to be sure that it was not a contamination of two different species and that it was not simply a mutation”, explains Mizuno. “At first, we used a series of microscopic observations to film the whole process from a single cell to a colony, for which we developed our own methods. Next, we found that morphological changes in cells and colonies were both controlled and reversible. These data led us to believe that it is a “multicellularity” of HS-3. »

“The first stage of the HS-3 life cycle suggests that liquid crystal-like organization is involved in the emergence of multicellularity, which has not been previously reported. The existence of the second stage of the life involves the involvement of the dynamic water environment in the emergence of HS-3 multicellularity,” says co-corresponding author Kazuya Morikawa, professor in the Division of Biomedical Sciences at the University of Tsukuba, Japan. .

“We were surprised by the various curious properties that HS-3 encompasses, one of which is that the multicellular behavior of this new species fits well with the recently proposed ‘ecological scaffolding’ hypothesis. We now believe that the leap to multicellularity would be a more elaborate and beautiful process than what we have imagined so far. 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.
DOI: 10.7554/eLife.71920