Bacteria in human mouth reproduce through rare form of cell division, study finds

One of the most diverse ecosystems on the planet is closer than you think: it’s right inside your mouth. Your mouth is a thriving ecosystem of more than 500 different species of bacteria living in distinct, structured communities called biofilms. Nearly all of these bacteria grow by dividing in two, with one parent cell giving rise to two daughter cells.

New research from the Marine Biological Laboratory (MBL) and ADA Forsyth has uncovered an extraordinary mechanism of cell division in Corynebacterium matruchotii, one of the most common bacteria found in dental plaque. This filamentous bacterium doesn’t simply divide; it divides into multiple cells at once, a rare process called multiple fission. The research is published in Proceedings of the National Academy of Sciences.

The team observed that C. matruchotii cells divided into 14 different cells at a time, depending on the length of the original mother cell. These cells also only grew on one pole of the mother filament, a process called “tip extension.”

C. matruchotii filaments act as a scaffold within dental plaque, which is a biofilm. Dental plaque is just one microbial community within a huge population of microorganisms that live and coexist with a healthy human body, an environment known as the “human microbiome.”

This discovery sheds light on how these bacteria proliferate, compete with other bacteria for resources, and maintain their structural integrity in the complex environment of dental plaque.

“Coral reefs contain corals, forests contain trees, and the dental plaque in our mouths contains Corynebacterium. The Corynebacterium cells in dental plaque are like a big, bushy tree in the forest; they create a spatial structure that provides habitat for many other species of bacteria around them,” said Jessica Mark Welch, co-author of the paper, senior scientist at ADA Forsyth and adjunct scientist at MBL.

“These biofilms are like microscopic rainforests. The bacteria in these biofilms interact with each other as they grow and divide. We think the unusual cell cycle of C. matruchotii allows this species to form these very dense networks at the heart of the biofilm,” said Scott Chimileski, MBL researcher and lead author of the paper.

The microbial forest

This research builds on a 2016 paper that used an imaging technique developed at MBL called CLASI-FISH (combinatorial labeling and spectral imaging by fluorescence in situ hybridization) to visualize the spatial organization of dental plaque collected from healthy donors.

This earlier study imaged bacterial consortia within dental plaque, called “hedgehogs” because of their appearance. One of the key findings of this original study was that filamentous cells of C. matruchotii acted as the basis of the hedgehog structure.

The current study delved deeper into the biology of C. matruchotii, using time-lapse microscopy to study the growth of filamentous cells. Rather than simply capturing a snapshot of this microbial rainforest, the scientists were able to image the bacterial growth dynamics of the miniature ecosystem in real time. They saw how these bacteria interact with each other, use space, and, in the case of C. matruchotii, the incredible ways in which they thrive.

“To understand how different types of bacteria work together in plaque biofilm, we need to understand the basic biology of these bacteria, which live nowhere other than in the human mouth,” said Mark Welch.

Dentists recommend brushing your teeth (and thus removing plaque) twice a day. Yet this biofilm keeps coming back no matter how diligently you brush. Extrapolating from cell elongation experiments measured in micrometers per hour, scientists found that C. matruchotii colonies could grow up to half a millimeter per day.

Other Corynebacterium species are found elsewhere in the human microbiome, including on the skin and inside the nasal cavity. However, Corynebacterium species from the skin and nose are shorter, rod-shaped cells that do not elongate by tip extension or divide by multiple fission.

“Something about this very dense, competitive dental plaque habitat may have driven the evolution of this growth pattern,” Chimileski said.

Exploratory growth

C. matruchotii lack flagella, the organelles that allow bacteria to move. Since these bacteria cannot swim, the researchers speculate that their unique elongation and cell division may allow them to explore their environment, similar to the mycelial networks seen in fungi and the soil-dwelling Streptomyces bacteria.

“If these cells have the ability to preferentially move toward nutrients or other species to form beneficial interactions, this could help us understand how the spatial organization of plaque biofilms occurs,” Chimileski said.

“Who would have thought that our familiar mouth would harbor a microbe whose reproductive strategy is virtually unique in the bacterial world,” said study co-author Gary Borisy, a senior scientist at ADA Forsyth and former director of the Marine Biology Laboratory. “The next challenge is to understand what this strategy means for the health of our mouths and bodies.”