The gliding movements displayed by several species of blue—green algae and bacteria have not as yet been satisfactorily explained. Earlier observations of gross behaviour and morphology have suggested several mechanisms, but we believe that none of the previous explanations encompass all of the motility characteristics observed in the blue—green alga, Oscillatoria princeps Vaucher Fig. Burkholder, P. Article Google Scholar. Schmid, G. Google Scholar. Schulz, G. Jarosch, R. Salton, M. Holwill, M.
Fritsch, F. Press, Prell, H. Jost, M. Pankratz, H. Ris, H. Download references. You can also search for this author in PubMed Google Scholar. Reprints and Permissions. This bacterium is usually deep purple red in color but can be reddish brown as well. It has been found in a few small springs in the Mammoth area of Yellowstone, and is quite abundant in some of the hydrogen sulfide-containing springs at Thermopolis, Wyoming.
This artist's animation features Calothrix, a brownish rod-shaped cyanobacterium that forms dark brown mats along the moist edges and in the outflow of many Yellowstone thermal features. It contains a pigment that acts as a sunscreen and protects Calothrix from high levels of UV radiation. This artist's animation features Desulfurococcus, a spherical shaped organism with a surface protein that forms a lattice of mesh cross-shaped units.
It does not need oxygen but obtains energy by ingesting organic carbon compounds like sugars and lipids. This artist's animation features Synechococcus, rod-shaped cyanobacteria that create green mats and can form some of the most prominent green colors in thermal features. They are photosynthetic and intolerant of sulfur. This artist's animation features Metallosphaera, a spherical-shaped member of the domain Archaea that appears orange when in large groups. This organism is a hyperthermophile, meaning it can grow at very high temperatures to 80 degrees C to degrees F.
This artist's animation features Thermus, a rod-shaped bacterium that sometimes forms bright red or orange streamers. It contains pigments called cartenoids that act as a sunscreen and protect it from high levels of sunlight.
This artist's animation features Caldisphaera, a micro-organism that grows in high-temperature and acidic environments. It converts yellow precipitated sulfur into hydrogen sulfide -- the gas that smells like rotten eggs and is very poisonous and corrosive. The before and after images, were taken 30 min apart. Comparison of linear distance traveled per unit time speed and number of body lengths traveled per unit time relative speed for various prokaryotic microbial species and select eukaryotes.
Similarly to the positive phototaxis resulting in a symbol created by motile filaments above, the filaments showed the same response with a foil cutout of four different small holes. There was a positive correlation between positive phototaxis and photosynthetic yield.
Changes in photosynthetic efficiency over time in Light and Dark treatments measured at 10 min intervals. The mat was interwoven with enough strength to peel it away as a solid layer and the shells were found beneath the mat in the same locations in a horizontal plane.
Observations of particulate matter burial. Pieces of shells placed on an intact mat became completely buried in the sediment underneath due to the mat over-growth in about 3 days.
The mat was grown in groundwater at room temperature overlaying sediment cores taken from the site of mat sampling. Circles point our attention to sites where shells were visible on top of the mat before , and the same sites where they have disappeared under the mat after. Fortunately, modern cyanobacteria exhibit a range of carbon and sulfur physiologies such as respiration, oxygenic photosynthesis, anoxygenic photosyntheis, and chemosyntheis Falkowski et al.
The majority of microbial mats on Earth are still dominated by cyanobacteria, and in these extreme habitats where eukaryotic photosynthetic algae cannot thrive, cyanobacteria serve as the base of the food web Stahl, Because microbial mats are characterized by steep redox changes and fluctuating physico-chemical microscale gradients of light, dissolved oxygen and nutrients Buhring et al.
It is quite conceivable that motility confers significant advantages for optimizing variable life styles of oxygenic photosynthesis, anoxygenic photosynthesis, and chemosynthesis across sharp gradients of resources and physico-chemical conditions that prevail in such low-oxygen and high-sulfur ecosystems Shepard and Sumner, ; Buhring et al. However, their motility rates are on the high end of non-flagellated and non-ciliated microbes, and at the lower end of motility rates for flagellated and ciliated microbes Milo and Phillips, Their relatively slow and steady life style may be quite adequate for operating at spatial scales relevant to them enabling to form and maintain mat structure, find sunlight and optimize photosynthesis, and in the process, efficiently bury carbon in the underlying sediments — all features that may have been important for oxygenation of early Earth.
Microbes such as those found in and on biofilms not only seek nutrients and light, but also seek out each other by clustering together in coordinated motion.
The Oscillatoria from ECB and MIS are not only phototactic, having the ability to position themselves precisely within optimal light conditions — but also are capable of active aggregation and dispersal. The aggregation effect of the Oscillatoria filaments to create an interwoven mat in the lab is almost identical to the aggregation effect seen in similar thermophilic Oscillatoria Castenholz, The hallmark of the response is to quickly create mat-like structures of individual filaments dependent upon initial filament density.
High-density filaments spread throughout a groundwater medium and form into a singular, large mat. The individual filaments traveled away from the main colony in a uniform dispersion, staying in contact with the central colony through long tendrils of interwoven filaments. The eventual result was uniform dispersion throughout the medium. This behavior was observed both in the light and in the dark although at a much reduced speed relative to their speed in the light , suggesting this behavior is not limited to phototaxis, and chemotaxis may be a potential factor.
Additional research is needed to identify the ecological role of this motile response in the dark. This is crucial as random movements at their speed alone may not cause a cell to move into an area that would increase their light optimization either from an area of low light to high light, or vice versa.
Simulated random movement of filaments of increasing length may have a far better chance of finding a more favorable area Tamulonis et al. Light is a critical factor for these cyanobacteria, so optimization of light harvesting is vital. Light conditions that are too low will lead to insufficient carbon fixation, and light conditions that are too high are inhibitory and can cause severe cell damage.
Ecologically and physiologically meaningful rates of movement are important for responding to rapid changes in light and redox conditions that are likely to be presenting in situ. Clustering together as a mat creates other significant biological advantages, such as protection from predation, and even sensing redox gradients Stocker, The strategy of clumping and dispersing over the lake sediment surface all the while staying connected to each other, could be an advantageous tactic for staying put in an ideal environment.
This strategy may be left over from the past and today prevents them from being transported by the strong storms and wind-induced turbulence of the Great Lakes. By keeping a tight network among the mat, larger sections are more likely to be ripped off the sediment, thus transporting a larger colony that would have a higher chance of surviving in a new environment.
The quick motility also would allow those to grow into any new gaps and prevent the remainder of the mat community from being sloughed off in a similar fashion. The formation of characteristic finger-like projections of mats is caused by the buoyancy of trapped microbially generated gasses such as H 2 S and CH 4 Nold et al.
Andersen et al. They concluded that the difference in illumination would not likely be different enough between prostrate and raised mats to confer any sort of advantage. Other Antarctic researchers have found that motility is critical for optimizing available resources in these sub-glacial lake environments, and have argued that this feature likely plays a key role in acclimating to environmental changes Hawes et al.
The observed increase in speed due to high temperature groundwater could be a reaction to non-ideal ambient physical or chemical conditions. Such behavior has been observed in other mat-forming cyanobacteria as a reaction to multiple stimuli, including depleting nutrient concentrations and damaging UV light intensity Tamulonis et al. Additionally, the greater movement at higher temperatures may reflect higher metabolic activity or the advantage for more rapid movement to enable cells to escape an unfavorable micro-environment Nadeau and Castenholz, Even the shallow 1—1.
Time-series monitoring using sondes deployed in the bottom of MIS during major storm events has revealed that such events during summer months can occasionally mix warm surface lake water down to 23 m to the mats Ruberg et al. Our temperature-motile stimuli response studies show that the Oscillatoria can survive in a wide range of temperatures, suggesting this feature could be important in the dispersal and colonization of these cyanobacteria throughout the Karst coastline of Lake Huron, as they are found in multiple sites that have no direct groundwater connection.
It is also possible that the increase in ambient water temperature simply increases the rate of reactions related to motility Neidhardt et al. In contrast, perhaps they are not moving as fast as they can, but are conserving energy and diverting it to other, more important cellular processes.
As conditions become less ideal, such as with increasing temperatures, they may allocate more energy toward motility that would allow them to move faster and find a more suitable habitat. It could be that over their long geobiologic history, cyanobacteria have evolved ecologically advantageous features such as motility that allow them to succeed in sharply contrasting redox environments in which they frequently occur.
Many aspects of cyanobacterial motility remain unexplored. Motility that has been observed in the present study has been primarily phototactic and chemotactic. Although the precise mechanisms of cyanobacterial motility are still unknown, earlier studies have revealed certain structural and physiological key features such as: slime secretion processes, organelles, and distinct surface proteins Hoiczyk, With such precise photomovement capabilities, specific mechanisms for motility presumably exist, and further in vitro microscopic research will be needed to reveal them.
Gliding of cyanobacteria is controlled by a number of external stimuli, but when residing in a calm environment, light seems to be the most important Hoiczyk, Others have found that in addition to phototactic movement, the long filament shape also serves to maximize light exposure of the cells Tamulonis et al. Phototactic positioning in an ideal microenvironment works best for long filamentous bacteria that are in a microbial mat as they can indirectly sense light many lengths greater than their individual cell lengths.
Further, the increase in photosynthetic yield remained elevated throughout the duration of the experiment, indicating that the cells remained in the favorable photosynthetic conditions. This particular experiment looked at horizontal movement in response to light, a phenomenon that is more relevant to ECB than MIS. The deep benthic environment of MIS is relatively flat and light is distributed equally to all parts, whereas the shallow benthic environment of ECB has significant macrophyte vegetation and floating algal mats that may cause small areas of shade resulting in inhomogeneous light distribution.
Vertical phototaxis discussed below may allow for the Oscillatoria to remain on top of the mat during the day, as many similar cyanobacteria exhibit negative phototaxis when in direct light. Mat-forming cyanobacteria, Microcoleus chthonoplastes found in hypersaline mats at Salins-de-Giraud, France, exhibit phototactic migrations to the upper layer of the mat during the day and are spread homogenously through the mat at night Tamulonis et al.
During the night, the white chemosynthetic bacteria are present at the top of the mat, and the Oscillatorians rest underneath.
It is unknown whether the chemosynthesizers move toward the surface, whether the Oscillatorians descend in this diurnal cycle, or if a combination of both occurs.
However, if the filaments are descending, it would be a motile response that is not phototactic — but is likely to be a chemotactic response toward fluctuating redox at night when oxygen production ceases. At the ECB, the Oscillatoria are found upon, under, and around plant growth, detritus and other stationary objects within the water saturation of the groundwater spring. These features allow for the cyanobacteria to migrate to the shade if needed. Oscillatoria , having longer filaments that allow them to measure light between more distant points, which enhances their capacity to navigate with noisy light signals, detect subtle gradients and avoid falling into small sub-optimal light traps Tamulonis et al.
These physical parameters found in the environment of the microbial mat, along with our results, affirm the necessity of precise phototactic movement as a primary response stimulus of motility. Similar cyanobacteria found in hot water springs in arctic regions responded primarily to various other stimuli other than light Castenholz, These cyanobacteria were motile as a mat community in response to fluctuating stimuli in their environment, such as water temperature due to cold-water runoff mixing with the hot water springs.
The fluctuation of the physical parameters of this system proved to dictate the motile behavior of these organisms. However, the environment of ECB and especially the MIS maintain consistency in physical-chemical conditions due to the constant influx of groundwater into the system. This inflow maintains a stable level of dissolved oxygen, water temperature, flow, and conductivity Ruberg et al.
The amount of light present at the level of the mat is therefore the most variable motility stimulus, reliant upon diurnal light cycling, cloud cover, weather patterns, and water depth clarity. Due to the similarities between these organisms in the Arctic and Lake Huron, a similar ancestry is possible with subsequent divergent evolution due to environmental stresses. When small bits of shell were placed upon an intact mat overlaying sediment, the mat eventually grew over them. Over time, such filament overgrowth on falling particles may effectively bury organic detritus from sinking plankton and other organisms of the MIS into the benthic carbon reservoir.
Previous research has shown that the majority of organic matter in the carbon sink originated from phytoplankton that has settled from the water column onto the mat Nold et al.
This organic matter falls through the mat by the movement of Oscillatoria into the underlying anaerobic sediments where they become preserved.
The scenario works like this: when decaying plankton and other suspended debris fall onto the mat, the cyanobacterial filaments climb over it to seek sunlight and push the detritus down into the anaerobic sediment where it tends to be preserved Biddanda et al. The ability of mats to quickly bury objects substantially larger than plankton demonstrates the enhanced capacity of sinkhole ecosystems overlain by cyanobacterial mats to efficiently bury carbon.
The source of this sedimentary carbon, as determined by its stable isotope signature, appears to be exclusively settling plankton and debris from the overlying lake water column Sanders et al. Once the organic carbon is below the mat in the anaerobic layer, it is slow to degrade and becomes preserved as observed in sulfur-fed springs of Lake Cadagno in Switzerland Hays, ; Hebting et al.
Indeed, the gradual microbial metabolism of this carbon reservoir under low redox conditions creates hydrogen sulfide and methane bubbles which may become trapped in the tightly woven microbial mat, creating finger-like projections of the mat Biddanda et al. Ubiquitous, but tiny microbes continually obtain and use information from their microenvironment to meet the fundamental challenges of everyday life Dusenbery, ; McBride, Microbes responding collectively to microenvironmental gradients in their habitats are the engines that drive the cycling of major bioactive elements on Earth National Academy of Sciences, ; Falkowski et al.
Long cyanobacterial filaments that are fast-moving are able to optimize light capture Tamulonis et al. Benthic cyanobacterial mats covering submerged sinkhole ecosystems of Lake Huron exhibit rapid motility of their filaments in response to light and other environmental cues.
Such integrated filament motility may play critical roles in mat structure, formation, and maintenance of redox gradients, optimizing individual and collective photosynthesis in a light-poor environment and favoring enhanced sedimentary carbon accrual. Lake Huron sinkholes represent the only known refugia for such cyanobacteria in the Northern hemisphere; ice-covered Antarctic lakes are the only other known habitat.
Such taxonomically simple but metabolically versatile microbial communities represent a major gap in our understanding of how life shaped the chemistry and habitability of our planet, and makes them ideal systems for exploring important unresolved issues in evolution, biodiversity and physiology. For example, within the submerged sinkhole mat communities of Lake Huron, perhaps the oldest form of biological warfare — the one between cyanobacteria and cyanophage viruses — still rages Voorhies et al.
Thus, the cyanobacteria-dominated submerged sinkholes are model communities for examining microbial physiology in an extreme environment with potential applications to our search for life beyond the home planet. Such knowledge will be critical to the conservation of these small and distantly distributed ecosystems in a rapidly changing world.
Cyanobacteria continue to play important ecological roles in modern Earth Falkowski et al. It is of considerable biogeochemical interest that ecologically similar modern-day microbial mat communities that reduce carbon and oxidize sulfur are found in geographically distant locations such as Antarctic lakes, thermal springs, and other extreme sulfur-rich environments that resemble conditions on early Earth. In modern-day low-oxygen refugia such as submerged sinkholes, motility may confer cyanobacteria the ability to thrive under low-light conditions by maximizing their metabolism across sharply varying gradients of redox and chemical resources in their benthic habitats.
If such motile traits prevailed in cyanobacteria during the Proterozoic, they might have been critical to the filaments staying on top of the benthos in the turbid shallow ocean — optimizing photosynthesis and burying away planktonic organic carbon production — leading to the eventual oxygenation of the environment Allwood et al.
BB planned and designed the study, obtained funding, participated in the sampling and the running of experiments, wrote and reviewed the manuscript. AM conducted the sampling, designed and carried out the experiments, drew up the first outline of the paper, wrote and reviewed the manuscript.
SL conducted sampling, preliminary motility studies, wrote and reviewed the manuscript. MS assisted with sampling, conducted the photosynthetic efficiency experiments, wrote and reviewed the manuscript. AW assisted with sampling, conducted preliminary motility experiments, prepared figures, wrote and reviewed the manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. National Center for Biotechnology Information , U. Journal List Front Microbiol v. Front Microbiol. Published online Sep 7.
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