Habitability of Highly Mineralizing Environments

There is a potential paradox here: on one hand, for all the reasons above, volcanic hydrothermal systems were probably the first habitable zones on the early Earth; on the other hand, they are dangerous for life, because of the lethal effects of mineral precipitation on cells. Fossilization of microbial cells possibly occurs by precipitation of many different minerals: e.g. silica (e.g. Westall et al. 1995; Toporski et al. 2002; Benning et al. 2004), manganese oxide (Tebo et al. 2004), calcium phosphate (Benzerara et al. 2004a, 2004b). Cells can be totally entombed in the precipitates (Benning et al. 2004; Benzerara et al. 2004a, 2004b).

The ecological and evolutionary implications of fossilization are profound (see Cald-well and Caldwell 2004 for a conceptual view of these issues). Mineralization processes have a major influence on habitability. The traditional view considers microbes to be purely "passive" in the precipitation of the minerals: microbes modify indirectly the chemical conditions of the surrounding environment by their metabolic activity and hence foster mineral precipitation. This is substantiated by chemical/thermodynamical modeling (e.g. Frankel and Bazylinski 2003).

It is possible that the ability to biomineralize may only be a side-effect of metabolism. It does not provide a selective advantage to a microbe. It may actually be disadvantageous: the precipitation of few hundred nanometer thick layers of minerals around cells may limit diffusion of nutrients necessary for life; the formation of nanometer-sized crystals may disrupt cellular structures and hence be lethal. The fitnesses (i.e. an individual's ability to propagate its genes) of a microbe promoting biomineralization vs. that of a microbe inhibiting biomineralization have, however, never been measured.

Some strategies developed by microbes to inhibit precipitation of minerals on their membrane might be operating in highly mineralized environments. One example is the formation of sheaths, which are extracellular tubes surrounding microbes and that offer preferential nucleation sites for crystals. Microbial cells can get rid of these tubes and form new sheaths (Phoenix et al. 2000; Konhauser et al. 2001). Emerson and Ghiorse (1992) showed that sheathless variants arise spontaneously in laboratory cultures if predation and mineral precipitation are no longer present. Schultze-Lam et al. (1992) proposed that some cyanobac-teria synthesize protein surface layers (S-layers), which provide nucleation sites for calcite precipitation and that they can shed when encrusted in mineral precipitates.

There is however no conclusive evidence that those strategies are more developed in microbes inhabiting highly mineralizing environments than anywhere else. Moreover, the comparison of the various studies on mineral precipitation on bacterial cells is confusing regarding whether this process is lethal or not (see Kappler et al. 2005). Some authors suggest that biomineralization on cell walls occurs during or after death of cells (e.g. Wierzchos et al. 2005), while others report the existence of viable cells encrusted by minerals (e.g. Phoenix et al. 2001; Tebo et al. 2004).

Seemingly passive biomineralization may actually provide an advantage to microorganisms. First of all, some studies contest that mineral precipitation on cells is always a passive mechanism (Castanier et al. 1999). They suggest that some species have a better ability than others to precipitate calcium phosphates or calcium carbonates (Castanier et al. 1999). Could this ability to precipitate minerals be advantageous in some cases?

Several potential advantages have been proposed for extracellular biomineralization: detoxification of toxic heavy metals, reactive oxygen species, UV light, predation or viruses; protection against immune system for pathogenic microbes; protection against grazing; storage of an electron acceptor for later use in anaerobic respiration; scavenging of mi-cronutrient trace metals (e.g. Sommer et al. 2003; Mire et al. 2004; Tebo et al. 2004; Ghiorse 1984). Chan et al. (2004) suggested that extracellular iron oxide precipitation may provide energy to microbial cells. Whereas this has almost never been proposed for minerals like silica, calcium carbonates or calcium phosphates, it is usually considered that lead phosphate precipitation by bacteria is a detoxification process. Microbially driven calcium phosphate precipitation, though, shares many similarities with biomineralization of lead phosphate. It is thus reasonable to consider that microbial calcium phosphate precipitation may have a similar ecological 'status' as lead phosphate precipitation and such bio-mineralization processes may have played a role in the habitability of highly mineralizing seemingly "toxic" environments.

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