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The ISME Journal (2015) 9, 19661978 & 2015 International Society for Microbial Ecology All rights reserved 1751-7362/15 http://www.nature.com/ismej
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ORIGINAL ARTICLE
Microbial carbon metabolism associated with electrogenic sulphur oxidation in coastal sediments
Diana Vasquez-Cardenas1,2, Jack van de Vossenberg2,6, Lubos Polerecky3,Sairah Y Malkin4,7, Regina Schauer5, Silvia Hidalgo-Martinez2, Veronique Confurius1, Jack J Middelburg3, Filip JR Meysman2,4 and Henricus TS Boschker1
1Department of Marine Microbiology, Royal Netherlands Institute for Sea Research (NIOZ), Yerseke,The Netherlands; 2Department of Ecosystem Studies, Royal Netherlands Institute for Sea Research (NIOZ), Yerseke, The Netherlands; 3Department of Earth Sciences, Utrecht University, Utrecht, The Netherlands;
4Department of Environmental, Analytical and Geo-Chemistry, Vrije Universiteit Brussel (VUB), Brussels, Belgium and 5Centre of Geomicrobiology/Microbiology, Department of Bioscience, Aarhus University, Aarhus, Denmark
Recently, a novel electrogenic type of sulphur oxidation was documented in marine sediments, whereby filamentous cable bacteria (Desulfobulbaceae) are mediating electron transport over cm-scale distances. These cable bacteria are capable of developing an extensive network within days, implying a highly efficient carbon acquisition strategy. Presently, the carbon metabolism of cable bacteria is unknown, and hence we adopted a multidisciplinary approach to study the carbon substrate utilization of both cable bacteria and associated microbial community in sediment incubations. Fluorescence in situ hybridization showed rapid downward growth of cable bacteria, concomitant with high rates of electrogenic sulphur oxidation, as quantified by microelectrode profiling. We studied heterotrophy and autotrophy by following 13C-propionate and -bicarbonate incorporation into bacterial fatty acids. This biomarker analysis showed that propionate uptake was limited to fatty acid signatures typical for the genus Desulfobulbus. The nanoscale secondary ion mass spectrometry analysis confirmed heterotrophic rather than autotrophic growth of cable bacteria. Still, high bicarbonate uptake was observed in concert with the development of cable bacteria. Clone libraries of 16S complementary DNA showed numerous sequences associated to chemoautotrophic sulphur-oxidizing Epsilon- and Gammaproteobacteria, whereas 13C-bicarbonate biomarker labelling suggested that these sulphur-oxidizing bacteria were active far below the oxygen penetration. A targeted manipulation experiment demonstrated that chemoautotrophic carbon fixation was tightly linked to the heterotrophic activity of the cable bacteria down to cm depth. Overall, the results suggest that electrogenic sulphur oxidation is performed by a microbial consortium, consisting of chemoorganotrophic cable bacteria and chemolithoautotrophic Epsilon-and Gammaproteobacteria. The metabolic linkage between these two groups is presently unknown and needs...