Conspicuous Veils Formed by Vibrioid Bacteria on Sulfidic Marine Sediment

Abstract

We describe the morphology and behavior of a hitherto unknown bacterial species that forms conspicuous veils (typical dimensions, 30 by 30 mm) on sulfidic marine sediment. The new bacteria were enriched on complex sulfidic medium within a benthic gradient chamber in oxygen-sulfide countergradients, but the bacteria have so far not been isolated in pure culture, and a detailed characterization of their metabolism is still lacking. The bacteria are colorless, gram-negative, and vibrioid-shaped (1.3-to 2.5-by 4-to 10-m) cells that multiply by binary division and contain several spherical inclusions of poly-␤-hydroxybutyric acid. The cells have bipolar polytrichous flagella and exhibit a unique swimming pattern, rotating and translating along their short axis. Free-swimming cells showed aerotaxis and aggregated at ca. 2 M oxygen within opposing oxygen-sulfide gradients, where they were able to attach via a mucous stalk, forming a cohesive whitish veil at the oxic-anoxic interface. Bacteria attached to the veil kept rotating and adapted their stalk lengths dynamically to changing oxygen concentrations. The joint action of rotating bacteria on the veil induced a homogeneous water flow from the oxic water region toward the veil, whereby the oxygen uptake rate could be enhanced up to six times, as shown by model calculations. The veils showed a pronounced succession pattern. New veils were generated de novo within 24 h and had a homogeneous whitish translucent appearance. Bacterial competitors or eukaryotic predators were apparently kept away by the low oxygen concentration prevailing at the veil surface. Frequently, within 2 days the veil developed a honeycomb pattern of regularly spaced holes. After 4 days, most veils were colonized by grazing ciliates, leading to the fast disappearance of the new bacteria. Several-week-old veils finally developed into microbial mats consisting of green, purple, and colorless sulfur bacteria.Marine sediments and biofilms are characterized by opposing gradients of chemical compounds, which can react with each other via exergonic redox reactions (6, 14). The bestinvestigated gradient systems are sulfide-oxygen or sulfide-nitrate countergradients, and a variety of microorganisms which are specialized in efficiently utilizing the energy released by the redox reaction of the two gradient compounds have been described. Detailed physiological studies of species which can be cultured in homogeneous media, e.g., Thiobacillus spp., have been performed (18). However, many conspicuous gradient microorganisms in natural habitats (e.g., the colorless sulfide oxidizer Thiovulum majus) can be kept in the laboratory only as enrichment cultures, and only a few species have been successfully isolated in pure culture based on gradient media (24). While detailed physiological studies are still lacking, the behavior and motility of gradient microorganisms, especially of the relatively large and easily identifiable colorless and photosynthetic sulfur-oxidizing bacteria, have been described in the literature...

A 3D Motile Rod-Shaped Monotrichous Bacterial Model

“…In the (IB) method with a fixed grid such as used here, the additional computational cost of including more model cells is small compared to the computational cost of solving the full Navier- [62,66], pattern formation in biofilm [35,34] or bacterial veil formation [100,101,26] would require significantly more model cells as well as a much larger computational grid. As a step toward a simplified bacterial model and the eventual study of the complex behavior of many swimming bacteria, we employ here a simplified model bacterial cell Figure 11: YZ-view of a bacterium swimming with one layer of fluid markers.…”

Ecology and Physics of Bacterial Chemotaxis in the Ocean

“…Flow over the surface has the effect of thinning the DBL, sharpening the gradients, and thus increasing solute transport to or from the surface. This happens, for example, at the sediment-water interface (165,192) and over corals (98), where the DBL becomes thinner as the speed of the flow increases. DBLs are important because they control the exchange of solutes at those interfaces (192) and because they harbor largely steady gradients that can serve as robust chemical cues for chemotactic microorganisms.…”

“…Assuming a constant and uniform release rate (for example, of hydrogen sulfide) from the sediment surface, molecular diffusion establishes a linear concentration gradient reaching a fraction of a millimeter (0.1 to 1 mm) into the water above the sediments. This region is the "diffusion boundary layer" (DBL) (165,192). The DBL harbors steep gradients not only of substances released from the sediments but also of those (e.g., oxygen) diffusing in from the water above and consumed at the sediments (165,192).…”

“…This region is the "diffusion boundary layer" (DBL) (165,192). The DBL harbors steep gradients not only of substances released from the sediments but also of those (e.g., oxygen) diffusing in from the water above and consumed at the sediments (165,192). The DBL is contained within a region of water adjacent to the sedimentwater interface (the "momentum boundary layer") where turbulence is quenched, due to the proximity of the solid surface, and flow is thus laminar, preventing the rapid erosion of gradients.…”

The EPS Matrix: The “House of Biofilm Cells”

“…More information about the specific components of the biofilm EPS, as well as their localization and stability, will likely support Costerton and Irvin's visionary concept of "biofilm as a tissue" in 1981, when EPS still was called the "glycocalyx" (4). In this regard, there exciting evidence is emerging that in several microbial communities, EPS often has a defined macromolecular "honeycomb" structure (19,22).…”