Photoferrotrophs thrive in an Archean Ocean analogue

Abstract

Considerable discussion surrounds the potential role of anoxygenic phototrophic Fe(II)-oxidizing bacteria in both the genesis of Banded Iron Formations (BIFs) and early marine productivity. However, anoxygenic phototrophs have yet to be identified in modern environments with comparable chemistry and physical structure to the ancient Fe(II)-rich (ferruginous) oceans from which BIFs deposited. Lake Matano, Indonesia, the eighth deepest lake in the world, is such an environment. Here, sulfate is scarce (<20 micromol x liter(-1)), and it is completely removed by sulfate reduction within the deep, Fe(II)-rich chemocline. The sulfide produced is efficiently scavenged by the formation and precipitation of FeS, thereby maintaining very low sulfide concentrations within the chemocline and the deep ferruginous bottom waters. Low productivity in the surface water allows sunlight to penetrate to the >100-m-deep chemocline. Within this sulfide-poor, Fe(II)-rich, illuminated chemocline, we find a populous assemblage of anoxygenic phototrophic green sulfur bacteria (GSB). These GSB represent a large component of the Lake Matano phototrophic community, and bacteriochlorophyll e, a pigment produced by low-light-adapted GSB, is nearly as abundant as chlorophyll a in the lake's euphotic surface waters. The dearth of sulfide in the chemocline requires that the GSB are sustained by phototrophic oxidation of Fe(II), which is in abundant supply. By analogy, we propose that similar microbial communities, including populations of sulfate reducers and photoferrotrophic GSB, likely populated the chemoclines of ancient ferruginous oceans, driving the genesis of BIFs and fueling early marine productivity.

Fig. 1.

Map showing the location of Lake Matano on Sulawesi Island, Indonesia (Inset), and bathymetric map of Lake Matano. The circle marks a central deep water master station, and the area shaded in red is underlain by anoxic water.

Fig. 2.

Vertical physical and chemical profiles collected at a deep-water master station in 2007. (A) The typical vertical distribution of water density in Lake Matano showing a seasonal pycnocline at 32 m depth and the persistent pycnocline at 110–120 m depth during the month of February 2007. (B) The vertical distribution of dissolved sulfate (blue circles) and sulfate reduction rates (SRR) (black dots connected with orange line). (C) The vertical distribution of dissolved oxygen (red line), iron (blue circles) and total dissolved sulfide (ΣH₂S_d) (green diamonds) over the same time period.

Fig. 3.

Profiles illustrating the transmission of light and the vertical distribution of microorganisms and particles at a deep-water master station in 2007. (A) Photosynthetically active radiation profile collected on a sunny day in February 2007. (B) The distribution of photosynthetic pigments (green circles, Chl a; brown diamonds, BChl e) collected, respectively, in February and March 2007. (C) Light transmission (beam attenuation) profile collected in February 2007.

Fig. 4.

A tree generated by using maximum parsimony and displaying the phylogenic relationships between Lake Matano clones and representative members of the Chlorobiaceae family in addition to Persicobacter diffluens as an outgroup. Bootstrap support is indicated at the branch points of the tree. Lake Matano clones are highlighted in blue, marine isolates in green, and C. ferrooxidans, a known photoferrotroph, in red. Lake Matano clones have up to 95% sequence similarity to C. ferrooxidans.