Modern Microbialite Morphology

This is Ph.D. student Bekah Shepard's project; she's almost done with her thesis and papers should be submitted soon. Undergraduates Katie Alexander (who is now at ASU) and Natalie Stork are substantially contributers, providing creative ideas and hard labor to keep the Pseudanabaena making more cool structures, separated from those pesky heterotrophs, providing excellent race tracks for them, etc. Many other undergraduates have also helped, including Amy Oberstadt, Dana Armstrong, Katrina Arrendando, and Rubi Medrano.

Bekah has established a laboratory model system composed of the filamentous cyanobacterium Pseudanabaena sp. The Pseudanabaena sp. culture is not pure, but is monospecific with respect to cyanobacteria. The organism consists of 2 micron diameter disc-shaped cells that are stacked against each other like a roll of coins. The groups of cells can be millimeters long. We also have other species of filamentous cyanobacteria in the lab that behave similarly.

The Pseudanabaena sp. experimental system reliably produces cyanobacterial mats with peaks, ridges, and cones several days after inoculation. The specifics of morphological development in the Pseudanabaena sp. mats varies with changing environmental conditions. However a general morphology consisting of intersecting ridges develops under all culture conditions that allow sufficient biomass growth. For example, ridges form in both stagnant and flowing water, under various light conditions, and with different water chemistry. Experiments demonstrate that ridge formation requires a critical cell density and motility in the cells. Growth and migration on a rough surface increases the rate of ridge formation. Experiments have also demonstrated that the basic patterns are not a response to light; ridges form on top of sand layers even when all light is coming from below. This result demonstrates that phototactic migration, which is the standard model for upward growth in cyanobacterial biofilms, is not required.

Bekah produced a very interesting time lapse movie that demonstrates the importance of cyanobacterial motility. It shows two types of inoculations responding to low light levels in fresh media. One self-organized into peaks and ridges almost identical to those at the base of Archean microbialites (figure at right). The other developed small groups of cyanobacteria that clumped together and migrated around and off the edge of intact biofilm. Density waves of bacterial propagate through parts of the intact mat. Watching the time lapse version of morphological development shows that the dynamics of Pseudanabaena motility are complex and very interesting; this motility can form complex structures even under conditions where there is no significant increase in biomass.

Full Resolution Movie (52 MB)

Movie explanation:

The first frame of the movie is shown to the left. The green mat on the left of the image is 1.8 cm across. The camera looked down on the mat and sand-filled tray (right), which were immersed in a few centimeters of artificial seawater. They were illuminated from above. The intensity of green is a first order approximation for the number of cells at each point. Time lapse frames were taken every 10 minutes and 25 hours of motility are shown in the movie.

The experiment on the right started out as a tooth-paste consistency slurry of cyanobacteria buried by a small amount of sand. The bacteria were irregularly distributed, but within the first 2 hours, ridges started to form. This is fast enough that the ridges had to form by the bacteria moving into these specific areas. The length of time was too short relative to the growth rate for ridges to form due to cells reproducing. Thus, the organization of the ridges can be modeled initially as only due to bacterial motility as a response to the environment and local cell density. These ridges had up to 1 mm-high topography.

The green mat on the left is a folded sheet of photosynthetic bacteria from the same culture as the experiment on the right. The morphological changes are not as obvious, but there are some very interesting dynamics within and at the edges of the mat. Pay particular attention to the upper right corner at about 3 seconds into the movie (starting at 350 minutes in the experiment). Small clumps of bacteria start migrating off the main sheet onto the white plastic. They move around and some disappear into a thin light green area on the plastic whereas others rejoin the main sheet. Similar clumps can also be seen migrating around the lower part of the sheet at about 9 seconds into the movie. The cyanobacteria did not form these clumps just to produce higher topography; there has to be a behavior that induces sideways migration of these concentrations of cyanobacteria. This behavior constrains cyanobacterial self-organization in a different way than the growth of ridges as seen in the sand experiment. Interestingly, the migration of clumps on plastic with little biofilm requires that at least some of the cyanbacteria are moving mm with the clumps.

A third interesting dynamic starts in the upper part of the left experiment about 12 seconds into the video. Waves of denser bacteria move irregularly through the mat. The dynamics of these waves are such that it seems unlikely that individual bacteria are moving across the biofilm. Rather, local motility is causing instabilities in local biofilm density, and these instabilities are propagating as waves. This behavior demonstrates that observed dynamics operate over much longer length scales than individual cells or the local cell environment.

Related Publications:

Oberstadt*, Amy, Dana Armstrong*, Natalie Stork*, Rebekah Shepard*, and Dawn Sumner, 2008. Abstract (pdf)
Patterns of motility and morphologensis in filamentous cyanobacterial biofilms. AbSciCon 2008, Astrobiology, v. 8, Abstract 18-12-P.

Shepard*, Rebekah, Natalie Stork*, Amy Oberstadt*, Dana Armstrong*, and Dawn Sumner, 2008. Abstract (pdf)
Random motility creates reticulate morphologies in cyanobacterial biofilms, leaving phototaxis in the dark. AbSciCon 2008, Astrobiology, v. 8, Abstract 18-15-O.

Stork*, Natalie, Rebekah Shepard*, and Dawn Sumner, 2008. Abstract (pdf)
CaCO3 precipitation in freshwater laboratory biofilms dominated by Oscillatoria sp. AbSciCon 2008, Astrobiology, v. 8, Abstract 18-16-P. (Finalist, Student Poster Competition)

Sumner, Dawn Y., James P. Crutchfield, and Rebekah N. Shepard*, 2008. Abstract (pdf)
Microbial motility and morphological biosignatures. AbSciCon 2008, Astrobiology, v. 8, Abstract 24-48-O.

Stork*, Natalie J., Amy E. Oberstadt*, Dana K. Armstrong*, Rebekah N. Shepard*, and Dawn Y. Sumner, 2007. Abstract
Morphologenesis of laboratory biofilms. Geological Society of America Annual Meeting, Abstract.

Shepard*, Rebekah, Natalie Stork*, Megan Murphy*, and Dawn Sumner, 2006.
Influence of dissolved inorganic carbon on cyanobacterial biofilm morphogenesis. Astrobiology Science Conference, Abstract 118. (1st place student poster presentation)

Sumner, Dawn Y., 2006.
Microbial motility and morphological biomarkers. Astrobiology Science Conference, Invited Plenary Abstract 121.

Shepard*, R.N., K. Alexander*, M.A. Murphy*, and D.Y. Sumner, 2005.
Development of complex morphology in a cyanobacterial laboratory model system: implications for the interpretation of fossil microbialites. GSA Earth System Processes II, Abstract 42-6.

Shepard*, Rebekah, Kathryn M. Alexander*, and Dawn Y. Sumner, 2004 Abstract
Promoting processes of peak production in microbial mats. GSA Annual Meeting, Abstracts, v. 36, p. 361.

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Dawn Y. Sumner
Department of Geology
University of California
Davis, CA 95616