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Applied and Environmental Microbiology, December 2005, p. 8049-8060, Vol. 71, No. 12
0099-2240/05/$08.00+0     doi:10.1128/AEM.71.12.8049-8060.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Physiology and Phylogeny of Green Sulfur Bacteria Forming a Monospecific Phototrophic Assemblage at a Depth of 100 Meters in the Black Sea

Ann K. Manske,¹ Jens Glaeser,^1, Marcel M. M. Kuypers,² and Jörg Overmann^1*

Department Biologie I, Bereich Mikrobiologie, Ludwig-Maximilians-Universität München, D-80638 Munich, Germany,¹ Max Planck Institute for Marine Microbiology, 28359 Bremen, Germany²

Received 17 June 2005/ Accepted 6 September 2005

The biomass, phylogenetic composition, and photoautotrophic metabolism of green sulfur bacteria in the Black Sea was assessed in situ and in laboratory enrichments. In the center of the western basin, bacteriochlorophyll e (BChl e) was detected between depths of 90 and 120 m and reached maxima of 54 and 68 ng liter^–1. High-pressure liquid chromatography analysis revealed a dominance of farnesyl esters and the presence of four unusual geranyl ester homologs of BChl e. Only traces of BChl e (8 ng liter^–1) were found at the northwestern slope of the Black Sea basin, where the chemocline was positioned at a significantly greater depth of 140 m. Stable carbon isotope fractionation values of farnesol indicated an autotrophic growth mode of the green sulfur bacteria. For the first time, light intensities in the Black Sea chemocline were determined employing an integrating quantum meter, which yielded maximum values between 0.0022 and 0.00075 µmol quanta m^–2 s^–1 at the top of the green sulfur bacterial layer around solar noon in December. These values represent by far the lowest values reported for any habitat of photosynthetic organisms. Only one 16S rRNA gene sequence type was detected in the chemocline using PCR primers specific for green sulfur bacteria. This previously unknown phylotype groups with the marine cluster of the Chlorobiaceae and was successfully enriched in a mineral medium containing sulfide, dithionite, and freshly prepared yeast extract. Under precisely controlled laboratory conditions, the enriched green sulfur bacterium proved to be capable of exploiting light intensities as low as 0.015 µmol quanta m^–2 s^–1 for photosynthetic ¹⁴CO₂ fixation. Calculated in situ doubling times of the green sulfur bacterium range between 3.1 and 26 years depending on the season, and anoxygenic photosynthesis contributes only 0.002 to 0.01% to total sulfide oxidation in the chemocline. The stable population of green sulfur bacteria in the Black Sea chemocline thus represents the most extremely low-light-adapted and slowest-growing type of phototroph known to date.

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* Corresponding author. Mailing address: Department Biologie I, Bereich Mikrobiologie, Ludwig-Maximilians-Universität München, Maria-Ward-Str. 1a, D-80638 München, Germany. Phone: 49 89 2180 6123. Fax: 49 89 2180 6125. E-mail: j.overmann{at}lrz.uni-muenchen.de.

Supplemental material for this article may be found at http://aem.asm.org/.

Present address: Justus-Liebig-Universität Giessen, Institut für Mikro- und Molekularbiologie, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany.

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Applied and Environmental Microbiology, December 2005, p. 8049-8060, Vol. 71, No. 12
0099-2240/05/$08.00+0     doi:10.1128/AEM.71.12.8049-8060.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

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