8 Biologically Controlled Mineralization in Prokaryotes Biologically Controlled Mineralization in Prokaryotes

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    Biologically Controlled Mineralization in Prokaryotes

    Dennis A. Bazylinski Department of Biochemistry, Biophysics, and Molecular Biology

    Iowa State University Ames, Iowa 50011 U.S.A.

    Richard B. Frankel Department of Physics

    California Polytechnic State University San Luis Obispo, California 93407 U.S.A.

    INTRODUCTION As stated in an Chapter 4, prokaryotes of both Domains or Superkingdoms, the

    Bacteria and the Archaea, mediate the formation of a large number of diverse minerals. They are known to do this either through biologically induced mineralization (BIM) (Lowenstam 1981) (the subject of Chapter 4 in this volume; Frankel and Bazylinski 2003) or biologically controlled mineralization (BCM). The latter has also been referred to as organic matrix-mediated mineralization (Lowenstam 1981) and boundary-organized biomineralization (Mann 1986). There are several important differences between BIM and BCM that will be discussed in detail in this chapter, most notably those dealing with aspects of the mineral crystals and the biomineralization process (see also Weiner and Dove 2003). However, there is another significant difference between the two modes of biomineralization and this is the aspect of functionality. Generally, in BIM there is no function to the biomineralized particles except, perhaps, as a solid substrate for attachment in the case of bacteria or as a form of protection against certain environmental conditions or attack from predators. However, it is easier to recognize the primary function of bone or shells produced by molluscs; two well-characterized examples of BCM by higher organisms. Functionality should always be examined when dealing with examples of biomineralization particularly in situations where the mineral product displays some qualities of both BIM and BCM.

    In BCM, the organism exerts a great degree of crystallochemical control over the nucleation and growth of the mineral particles. For the most part, the minerals are directly synthesized at a specific location within or on the cell and only under certain conditions. The mineral particles produced by bacteria in BCM are characterized as well-ordered crystals with narrow size distributions, and specific, consistent particle morphologies. Because of these features, BCM processes are likely to be under specific chemical/biochemical and genetic control. In the microbial world, the most characterized example of BCM is magnetosome formation by the magnetotactic bacteria, a group of microorganisms in which BCM-produced magnetic crystals appear to have a relatively specific function. There are some examples of biomineralization that appear to be intermediate between BIM and BCM; these are covered in Chapter 4 (Frankel and Bazylinski 2003) since the mineralization product usually has more features in common with BIM. This chapter is, in effect, a review of the magnetotactic bacteria. However, it should be remembered that the production of magnetic minerals by the magnetotactic bacteria is used in this volume as an example of BCM. The microbiological, geological, chemical, biochemical, and physical approaches used to study BCM in the magnetotactic

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    bacteria are universal and will certainly be utilized again in other examples of BCM in bacteria discovered in the future.

    THE MAGNETOTACTIC BACTERIA Classification and general features

    The magnetotactic bacteria are a heterogeneous group of prokaryotes that passively align and actively swim along the Earth’s geomagnetic field lines (Blakemore 1975, 1982). This group is morphologically, metabolically, and phylogenetically diverse and cellular morphotypes that have been observed include coccoid (roughly spherical or ovoid), rod-shaped, vibrioid (curved), spirilloid (helical) and even multicellular forms (Blakemore et al. 1982; Farina et al. 1983; Rogers et al. 1990; Bazylinski 1995). The term “magnetotactic bacteria” therefore has no taxonomic significance and should be interpreted as a collection of diverse bacteria that possess the apparently widely distributed trait of magnetotaxis (Bazylinski 1995).

    Despite the diversity of these magnetotactic bacteria, they have several important features in common: 1) all that have been described are gram-negative members of the Domain Bacteria (it is possible that some members of the Domain Archaea produce magnetosomes but none have been reported); 2) they are all motile, generally by flagella (although this does not preclude the possibility of the existence of non-motile bacteria that synthesize magnetosomes which, by definition, would be magnetic but not magnetotactic); 3) all exhibit a negative tactile and/or growth response to atmospheric concentrations of oxygen; 4) all strains in pure culture have a respiratory form of metabolism (i.e., none are known to ferment substrates); and 5) they all possess a number of magnetosomes, the signature feature of the group (Bazylinski 1995; Bazylinski and Moskowitz 1997). The bacterial magnetosome is defined as an intracellular single- magnetic-domain crystal of a magnetic iron mineral enveloped by a membrane (Balkwill et al. 1980). The membrane is intracellular and may be connected to the cytoplasmic membrane. There is some evidence that the magnetosome membrane comprises a vesicle in which the magnetosome subsequently nucleates and grows (Gorby et al. 1988).

    There are two general types of magnetotactic bacteria based upon the minerals they biomineralize: there are the iron-oxide types that mineralize crystals of magnetite (Fe3O4) and the iron-sulfide types that mineralize crystals of greigite (Fe3S4) (Bazylinski and Frankel 2000b). The iron-oxide type are obligate microaerophiles, facultative anaerobes (that are microaerophilic when growing with O2), or obligate anaerobes while the iron- sulfide type appear to be obligate anaerobes. Ecology of magnetotactic bacteria

    Magnetotactic bacteria are ubiquitous in aquatic environments containing water with pH values close to neutrality and are not thermal, strongly polluted, or well-oxygenated (Moench and Konetzka 1978; Blakemore 1982). They are cosmopolitan in distribution (Blakemore 1982) and because magnetotactic bacterial cells are easy to observe and separate from mud and water by exploiting their magnetic behavior using simple laboratory magnets (Moench and Konetzka 1978), there are frequent reports of their occurrence in various freshwater and marine locations (e.g., Matitashvili et al. 1992; Iida and Akai 1996).

    On a local basis, magnetotactic bacteria are generally present in the highest numbers at the microaerobic oxic-anoxic transition zone (OATZ) and just below it in the anaerobic zone (Bazylinski 1995). In many freshwater habitats, the OATZ is located at the sediment-water interface or just below it. However, in some brackish-to-marine systems,

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    the OATZ is found, or is seasonally located, in the water column. The Pettaquamscutt Estuary (Narragansett Bay, RI, USA) (Bazylinski et al. 1995) and Salt Pond (Woods Hole, MA, USA) (Wakeham et al. 1984, 1987) are typical examples of this situation. Hydrogen sulfide, produced by sulfate-reducing bacteria in the anaerobic zone and sediment, diffuses upward while oxygen diffuses downward from the surface resulting in a double, vertical, chemical concentration gradient with a co-existing redox gradient. Strong pycnoclines and other physical factors, probably including the microorganisms themselves, stabilize the vertical chemical gradients and the resulting OATZ.

    Several morphotypes of iron-oxide and iron-sulfide magnetotactic bacteria are found at sites like the Pettaquamscutt Estuary and Salt Pond. The magnetite-producing magnetotactic bacteria are generally present at the OATZ proper and appear to behave as microaerophiles. Experiments with pure cultures support this observation. Two strains of magnetotactic bacteria have been isolated from the Pettaquamscutt and are now in pure culture. One is a vibrio designated strain MV-2 (Meldrum et al. 1993b; Dean and Bazylinski 1999) and the other is a coccus designated strain MC-1 (DeLong et al. 1993; Meldrum et al. 1993a; Frankel et al. 1997; Dean and Bazylinski 1999). Both strains grow as microaerophiles although strain MV-2 can also grow anaerobically with nitrous oxide (N2O) as a terminal electron acceptor. Other cultured magnetotactic bacterial strains, including spirilla (e.g., Blakemore et al. 1979; Schleifer et al. 1991; Schüler et al. 1999) and rods (Sakaguchi et al. 1993a), are microaerophiles or anaerobes or both. The greigite- producers appear to be strict anaerobes positioned in the more sulfidic waters just below the OATZ where oxygen is barely or not detectable (Bazylinski et al. 1990, 1992; Bazylinski 1995). To date, no greigite-producing magnetotactic bacterium has been grown in pure culture. Phylogeny of the magnetotactic bacteria

    Because magnetite particles resembling those of magnetotactic bacteria in ancient and recent sediments have been interpreted as magnetofossils (discussed later in the chapter), it is important to understand the phylogeny of the magnetotactic bacteria. Phylogenetic analysis, based on the sequences of 16S ribosomal RNA genes of many cultured and uncultured magnetotactic bacteria, initially showed that the magnetite- producing strains are associated with the α-subdivision of the Proteobacteria (Burgess et al. 1993; DeLong et al. 1993; Eden et al. 1991; Schleifer et al. 1991; Spring and Schleifer 1995; Spring et al. 1992, 1994, 1998), a vast assemblage of Gram-negative prokaryotes in the Do