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Depos t on of banded ron format ons by anoxygen c phototroph c Fe(II)-ox d z ng bacter a

A n d r e a s K a p p l e r C l a u d i a P a s q u e r o *

California Institute of Technology, GPS Division, Pasadena, California 91125, USA

Kurt O. Konhauser

Dianne K. Newman

Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta T6G 2E3, Canada California Institute of Technology, GPS Division, Pasadena, California 91125, USA

ABSTRACT

The mechanism of banded iron formation (BIF) deposition is controversial, but classically has been interpreted to reflect ferrous iron [Fe(II)] oxidation by molecular oxygen after cyanobacteria evolved on Earth. Anoxygenic photoautotrophic bacteria can also catalyze Fe(II) oxidation under anoxic conditions. Calculations based on experimentally determined Fe(II) oxidation rates by these organisms under light regimes representative of ocean water at depths of a few hundred meters suggest that, even in the presence of cyanobacteria, anoxygenic phototrophs living beneath a wind- mixed surface layer provide the most likely explanation for BIF deposition in a stratified ancient ocean and the absence of Fe in Precambrian surface waters.

(Beukes, 2004; Tice and Lowe, 2004). These observations led to the conclusion that the low abundance of Fe in the shallow-water environ- ment was due to the creation of a CO2-rich zone by the activity of microbial mats. According to this argument, downward diffusion of CO2 would have intercepted Fe(II) upwelling from deep waters, re- sulting in the precipitation of ferrous carbonates and thus preventing Fe(II) from reaching shallow waters. Here we consider whether a dif- ferent explanation for the restriction of Fe(II) to deep waters might be possible. Specifically, we test the hypothesis that anoxygenic Fe(II)- oxidizing phototrophs living below a mixed layer inhabited by cya- nobacteria could have been responsible for the absence of Fe in shallow waters and for Precambrian BIF deposition in a stratified ancient ocean.

Keywords: banded iron formation, oxidation, anoxygenic photosyn- thesis, cyanobacteria.

INTRODUCTION

Banded iron formations (BIFs) are Precambrian sedimentary de- posits that generally consist of alternating layers of iron minerals and silica (Beukes and Klein, 1992). How these deposits formed at different periods in Earth history has not been resolved, despite intensive in- vestigation over the last century. Central to this enigma is the contro- versy over when O2 evolved on the planet (Buick, 1992; Kasting, 1993; Holland, 1994; Canfield and Teske, 1996), and whether it was present in sufficient concentrations to be responsible for the deposition of the earliest BIFs (ca. 3.8–2.2 Ga).

MATERIALS AND METHODS Source of Organisms, Media, and Growth Conditions

Light is a critical parameter that limits any phototrophic metab- olism. Because both light intensity and light quality vary substantially with depth in the water column (Fig. 1), light can be expected to con- strain the maximum depth at which anoxygenic phototrophic bacteria can catalyze Fe(II) oxidation. To determine the effect of light intensity on the rate of phototrophic Fe(II) oxidation, we grew two representative

In the absence of O2, only two potential mechanisms for the ox- idation of ferrous iron [Fe(II)] to ferric iron [Fe(III)] are known: pho- tochemical oxidation by ultraviolet light (Cairns-Smith, 1978; Fran- cois, 1986) and light-dependent enzymatic Fe(II) oxidation by anoxygenic phototrophic bacteria (Widdel et al., 1993), the most an- cient type of photosynthetic organisms (Xiong et al., 2000). Although Fe(II) can be oxidized photochemically in simple aqueous systems (Braterman et al., 1983), such oxidation has not been reported in more complex environments such as seawater. In contrast, both freshwater and marine anoxygenic phototrophs can catalyze the oxidation of Fe(II) (Widdel et al., 1993; Ehrenreich and Widdel, 1994; Straub et al., 1999; Heising et al., 1999; Kappler and Newman, 2004; Croal et al., 2004). Fe(II) serves as the electron donor for these organisms, which convert

CO2 into biomass by using light energy: 4Fe2

CO2

11H2O

h

  • [CH2O]

4Fe(OH)3

8H .

Recently, stratigraphic analyses of a Precambrian Fe deposit (i.e., the Buck Reef Chert, Western Australia) established that a banded iron- rich chert formed offshore, below the base of storm waves at depths of more than 200 m; in addition, a carbon-rich, black and white banded chert unit was inferred to have been deposited in a shallow nearshore environment that was occasionally stirred by storms and large waves

Figure depths tensity equals

1. Wavelength-dependent light intensity at different water (indicated by numbers assigned to contour lines). Light in-

is given in ~30,000 lux

percent of surface

(~600

mol

quanta

light intensity, where m 2 s 1), estimated to

100% be 24

h average expected for light intensity on summer day (Thimijan and Heins, 1983).

horizontal surface on clear Contour lines were derived

using attenuation and Baker (1981).

coefficients given for clear ocean water Dashed lines represent light intensities

by Smith at 25 and

100 m

depth,

water

column

respectively, including and 17.6-m-thick layer

absorption by 25 and 100 m of anoxygenic phototrophic

*Present address: Center for Applied Geoscience, University of Tu¨bingen, 72074 T¨ubingen, Germany.

Fe(II) oxidizers containing 106 cells/mL. Shaded wavelength region where carotenoids absorb light.

area

indicates

2005 Geological Society of America. For permission to copy, contact Copyright Permissions, GSA, or editing@geosociety.org. Geology; November 2005; v. 33; no. 11; p. 865–868; doi: 10.1130/G21658.1; 3 figures; Data Repository item 2005170.

865

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