L. GERASIMENKO, V. ORLEANSKY and L. ZAITSEVA
Institute of Microbiology of RAS, Prospect 60-letya Octyabrya 7/2, Moscow, 117812, Russia
Abstract. Mineralization (silification, carbonatization and phosphatization) of cyanobacteria was studied in nature and laboratory. The increase in concentration of silica, phosphates, carbonates, and calcium leads to a sequence of morphological changes of cyanobacteria: (1) Formation of slime sheath, (2) formation of isolated globules of minerals on the slime sheath, (3) mineralization of slime sheaths of viable cells, and (4) mineralization of trichomes of dead cells.
Cyanobacteria are ancient organisms that were surprisingly stable over the entire evolution of life on Earth. The similarity of organic remains from ancient stromatolites, oncolites, and phosphorites to extant cyanobacteria [1-3] suggests the predominant role of these photo-synthetic organisms in biogenic carbonates deposition. Accordingly, the observation of the mineralization processes in nature and laboratory experiments allows us to understand cyanobacterial activity in the geological past.
Cyanobacteria, together with other bacteria, form microbial communities that dominated Earth for over 3 billion years and were responsible for important geological processes, including the accumulation of many sedimentary rocks and mineral resources. However, eukaryotic organisms pushed cyanobacteria from epicontinental marine basins to ecological niches, often with extreme conditions: hyperhaline lagoons of the sea, soda lakes, and hot springs, where thermophilic, halophilic, and alkaliphilic microbial communities survive even today.
Thermophilic communities were observed in the caldera of the volcano, Uzon, in Kamchatka and Kuril Islands; halophilic communities, in the lagoons of Sivash in Crimea; and alkaliphilic communities in soda lakes in Siberia. In hot springs with a large content of silica, the community is partly mineralized (Fig. 1(a) and (b)). These siliceous crusts contain mineralized microbial remains, i.e.: modern microfossils . Different stages of silification were found in these crusts (Fig. 1(c)). The process of mineralization begins with the penetration of silica within the cell and precipitation of minute globules on the cell walls. During the next stage, globules fuse into a single crust surrounding the cell. The external surface of the cells is smooth, while the internal surface is globular. Later, opal globules fill the spaces between and within the filaments until completely silicified rock is formed.
In the laboratory, it was shown that penetration of silica occurs only after the cell's death. Living cells have mechanisms of precluding high silica concentrations, namely the formation of the thick slime sheaths.
The thermophilic and halophilic mats often contain carbonate inclusions represented by aragonite and calcite. Cyanobacteria observed in these mats are also carbonatized. The rigid correlation between the content of cyanobacteria in the mat  indicates that one of the reasons is the alkalization of the media resulting from the active photosynthesis of cyanobacte-
ria. Laboratory experiments show that the precipitation of carbonates reaches its maximum when photosynthetic conditions are optimal . The increase in the content of calcium++ (Ca++) and carbonates in the medium results in morphological changes, primarily in the formation of slime sheaths. Later Ca-carbonate globules precipitate on sheaths of living cells and gradually mineralized the entire trichomes of dead cells. Experimental data show that some content of carbonates or carbon dioxide (CO2) in the media plays a decisive inhibiting effect on the growth of cyanobacteria. High concentrations of carbonates increase the pH of the medium to >11; and high concentrations of CO2 decrease the pH to <5. The cells die and mineralization of trichomes occurs.
The action of phosphorus on the growth and mineralization of cells was studied carefully. Our experiments showed that halophilic cyanobacteria—Microcoleus chthono-plastes, the dominant organism of cyanobacterial mats—can survive in a wide range of inorganic phosphorus concentrations. However, irrespective of concentrations, the active re-
Figure 2. Formation of mineral microtubes of fluorine-apatite. Bar=1|m.
moval of phosphorus from the medium was observed in the first 3 hr and was completed in 24 hr [7,8]. Experiments showed that not all phosphorus penetrated the cell, the larger part of it was absorbed on the surface. The higher its concentration in the medium, the more intensive is the absorption. The active influx of phosphorus into the cell occurs by its active transport through the membrane. It accumulates in larger quantities than outside the cell, and its concentration there is higher than the cell requires for its metabolism. In Microco-leus chthonoplastes, the active transport occurs with a maximum rate in the first 3 min of contact. In 3 days, a two-fold decrease in rate was observed.
Phosphorus can be stored in microbial cells in the form of inorganic polyphosphates that serve as a phosphorus reserve to provide for cell survival under phosphorus starvation. Various fractions of polyphosphates may respond differently to changes in the environment. Fractional distribution of the phosphates in cyanobacteria grown in the presence of different concentrations of polyphosphates corresponded to morphological alterations in the cells related to their mineralization. The superficial accumulation of acid-insoluble polyphosphates, localized close to the cell surface, stimulated the mineralization of slime sheaths. Under a high concentration of phosphorus (lethal for cells) the accumulation of orthophosphates and nucleoside phosphates was observed. This is when mineralization of trichomes begins .
The x-ray investigation of mineral sheaths and trichomes showed that the emerging, poorly crystallized phosphate minerals of the apatite group have a major diffTactionary maximum that is close to francolite . To obtain a crystallized apatite in the laboratory, NaF was added to the medium since F is an isomorphic element of the apatite structure . The solid precipitate was studied with scanning electron microscopy, and electron micrographs showed dispersive-lay spherulite-like particles on which there were well-ordered microtubes (Fig. 2).
They may be situated on or in the precipitate, near trichoms or on them. The microtubes ranged in diameter from 0.8 to 1.1 |im, and their length varied from 1.0 to 12.0 |m. Microtubes consist of small, individual, especially smooth spherulites of 0.2-0.5 |im, and the spherulites may be densely packed.
The observed mineral microtubes resemble modern and ancient microfossils by their gross morphology. Thus, the data presented show that in some cases, filamentous or tubular structures may not represent the fossilized microorganism itself. That is why it is necessary to be careful in their interpretation.
Thus, the action of different ions on cells is similar in spite of the fact that phosphorus, calcium, and carbonate are necessary components for the growth of all cyanobacteria, but silica is a necessary element only for specific groups of alga. The increase in concentration of these components leads to morphological changes of the cells (Fig. 3), which are:
1. The surface of the cells becomes covered with a slime sheaths. This sheath may be twice as thick as the trichomes. The appearance of this sheath in cyanobacteria and many other microorganisms indicates an unfavorable environment and is a cellular
response for its protection. The sheath consists of an amorphous substance containing polysaccharide microfibrils as a matrix. The latter may become a center of a mineralization process in that they form mineral microtubes around the cyanobacte-rial filaments.
2. As ion concentration increases, isolated mineral globules precipitate on the sheaths, then emerge in them. Later they fuse on larger bodies and finally form a complete mineral sheath. Mineral accumulation occurs only in the slime sheath and does not involve trichomes. Cells remain viable, and occasionally, it was observed that trichomes move out of the mineral covering leaving an empty tube behind.
3. As concentration increases, the culture dies, and the trichome itself becomes mineralized. Large rates of absorption in first few minutes explain the good preservation of morphological structures of cyanobacteria in ancient rocks.
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