Bacterial S-layer preservation and rare arsenic-antimony-sulphide bioimmobilization in siliceous sediments from Champagne Pool hot spring, Waiotapu, New Zealand

Journal of the Geological Society, Mar 2005 by Phoenix, Vernon R, Renaut, Robin W, Jones, Brian, Ferris, F Grant

Abstract:

Siliceous sinter, loose sediments, and suspended floes in Champagne Pool, an anoxic hot (75 °C) spring at Waiotapu, New Zealand, are composed of opaline silica and metal-rich sulphides that contain many well-preserved, mineralized microbes. Detailed analysis by transmission electron microscopy and energy dispersive spectrometry has shown that bacterial cell wall and capsular material is preserved by the immobilization of high levels of As, Sb and S in the organic matrix. Calculation of the probable metal species in the spring water suggests that arsenic and antimony are present in solution as negative and neutrally charged sulphide or hydroxide complexes (such as HAs^sub 2^S^sub 4^^sup -^, H^sub 3^AsO^sub 3^ and HSb^sub 2^S^sub 4^^sup -^). The early adsorption of these complexes onto reactive groups on the bacterial surface may be paramount in the excellent preservation of cell morphology. As biomineralization progresses, biomineral composition commonly becomes dominated by the precipitation of a supersaturated Al-rich amorphous silica phase. Biomineralization commonly preserves S-layers, an ordered mosaic of proteins on the outer surface of the cell wall. These are the finest ultrastructure details thus far found in microbes preserved by hydrothermal mineralization, and can be used as an aid to identify microfossils. The S-layers preserved here probably belong to Clostridium thermohydrosulfuricum or Desulfotomaculum nigrifacans.

Keywords: siliceous sinter, biomineralization, hot spring, sulphides, bacteria.

The biomineralization of microorganisms has been studied in detail at many hot-spring systems around the world, where the discharged fluids are commonly supersaturated with respect to several mineral phases (Ferris et al. 1986; Pentecost 1995; Schultze-Lam et al. 1995; Cady & Farmer 1996; Hinman & Lindstrom 1996; Jones et al. 1998; Konhauser et al. 2001; Mountain et al. 2003). A major reason for such investigations is to provide insights into the fossilization processes. By increasing knowledge of how organic structures are preserved in mineral matrices, the interpretation of the ancient microfossil record may be greatly enhanced (Schultze-Lam et al. 1995). Biomineralization and ultimately fossilization in high-temperature hot springs are passive processes, such that bacteria simply act as nucleation sites for mineral formation. Therefore, the composition of the biomineral is controlled by the chemistry of the spring water. Upon expulsion from the hot-spring vent, many geothermal fluids become supersaturated with respect to amorphous silica as a result of cooling and (or) evaporation, or supersaturated with respect to CaCOj because of rapid CO: degassing. It follows that most hot-spring biomineralization is either amorphous silica (opal-?), which may incorporate high levels of Fe (e.g. Ferris et al. 1986; Schultze-Lam et al. 1995; Cady & Farmer 1996; Hinman & Lindstrom 1996; Renaut & Jones 2000; Asada & Tazaki 2001; Konhauser et al. 2001; Mountain et al. 2001), or calcite and (or) aragonite (e.g. Chafetz & Folk 1984; Pentecost 1995).

Biomineralization begins as fine precipitates (microcrysts) on the outer surface of the microorganism, commonly while the microbe is still alive (Phoenix et al. 2000, 2001). Then, as biomineralization progresses, the microcrysts may merge and coalesce to form thicker precipitates that gradually destroy any fine structure of the cell. The cell wall and extracellular material are often only crudely preserved in this process, and the internal cytoplasm may degrade and be destroyed (Schultze-Lam et al. 1995; Konhauser& Ferris 1996).

This paper describes the exceptional preservation of ultrastructural details in biomineralized microorganisms from Champagne Pool in the Waiotapu geothermal area in New Zealand, and considers their implications for fossilization. Detailed analyses of these deposits have revealed the preservation of S-layers, a crystalline and ultra-fine mosaic of interconnected proteinaceous subunits that are present on the outer surface of cell walls. These matrices are the finest ultrastructural details yet found that have been preserved by hot-spring biomineralization. S-layers commonly vary between species and can thus be used as a 'fingerprint" for their identification. This new evidence increases our ability to identify species preserved by mineralization in the geological record. Identification is normally difficult because of the loss of morphological detail during preservation (see Jones et al. 200 Ib). Furthermore, many of the microorganisms at Champagne Pool are preserved by As-Sb-S sorption onto cell wall and extracellular polymers. Such As-Sb-S-enriched compositions have not been previously documented in fossilized bacteria at hot springs, and a new mechanism is invoked for their involvement in the preservation of ultrastructural details. The results of this study suggest that rapid adsorption of heavy metals onto cell wall and extracellular polymers is fundamental in enhancing microfossil preservation.