Fotoferrótrofos 'florescem' em um oceano arqueano análogo

Photoferrotrophs thrive in an Archean Ocean analogue

Sean A. Crowe*, CarriAyne Jones†, Sergei Katsev*,‡, Cédric Magen*, Andrew H. O'Neill§, Arne Sturm¶, Donald E. Canfield†, G. Douglas Haffner§, Alfonso Mucci*, Bjørn Sundby*,‖, and David A. Fowle¶,**
+ Author Affiliations

*Earth and Planetary Sciences, McGill University, Montréal, QC, Canada H3A 2A7;

†Institute of Biology, Nordic Center for Earth Evolution, University of Southern Denmark, 5230 Odense, Denmark;

‡Large Lakes Observatory and Department of Physics, University of Minnesota, Duluth, MN 55812;

§Great Lakes Institute for Environmental Research, University of Windsor, Windsor, ON, Canada N9B 3P4;

¶Department of Geology, University of Kansas, Lawrence, KS 66047; and

‖Institut des Sciences de la Mer de Rimouski, Université du Québec, Rimouski, QC, Canada G5L 3A1

Edited by Andrew H. Knoll, Harvard University, Cambridge, MA, and approved August 27, 2008 (received for review May 31, 2008)

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 μmol·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.

anoxygenic photosynthesis banded iron formation green sulfur bacteria iron oxidation Lake Matano

Footnotes

**To whom correspondence should be addressed. E-mail: fowle@ku.edu

Author contributions: S.A.C., D.E.C., G.D.H., A.M., B.S., and D.A.F. designed research; S.A.C., C.J., C.M., A.H.O., A.S., G.D.H., A.M., and D.A.F. performed research; S.A.C., C.J., S.K., and D.A.F. contributed new reagents/analytic tools; S.A.C., C.J., S.K., A.H.O., D.E.C., A.M., B.S., and D.A.F. analyzed data; and S.A.C., D.E.C., and D.A.F. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. EU275404–EU275407).

This article contains supporting information online at www.pnas.org/cgi/content/full/0805313105/DCSupplemental.

© 2008 by The National Academy of Sciences of the USA

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