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Microbial carbon metabolism associated with electrogenic sulphur oxidation in coastal sediments.
ISME J. 2015 Sep; 9(9):1966-78.IJ

Abstract

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 (13)C-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 (13)C-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 further study.

Authors+Show Affiliations

1] Department of Marine Microbiology, Royal Netherlands Institute for Sea Research (NIOZ), Yerseke, The Netherlands [2] Department of Ecosystem Studies, Royal Netherlands Institute for Sea Research (NIOZ), Yerseke, The Netherlands.Department of Ecosystem Studies, Royal Netherlands Institute for Sea Research (NIOZ), Yerseke, The Netherlands.Department of Earth Sciences, Utrecht University, Utrecht, The Netherlands.Department of Environmental, Analytical and Geo-Chemistry, Vrije Universiteit Brussel (VUB), Brussels, Belgium.Centre of Geomicrobiology/Microbiology, Department of Bioscience, Aarhus University, Aarhus, Denmark.Department of Ecosystem Studies, Royal Netherlands Institute for Sea Research (NIOZ), Yerseke, The Netherlands.Department of Marine Microbiology, Royal Netherlands Institute for Sea Research (NIOZ), Yerseke, The Netherlands.Department of Earth Sciences, Utrecht University, Utrecht, The Netherlands.1] Department of Ecosystem Studies, Royal Netherlands Institute for Sea Research (NIOZ), Yerseke, The Netherlands [2] Department of Environmental, Analytical and Geo-Chemistry, Vrije Universiteit Brussel (VUB), Brussels, Belgium.Department of Marine Microbiology, Royal Netherlands Institute for Sea Research (NIOZ), Yerseke, The Netherlands.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

25679534

Citation

Vasquez-Cardenas, Diana, et al. "Microbial Carbon Metabolism Associated With Electrogenic Sulphur Oxidation in Coastal Sediments." The ISME Journal, vol. 9, no. 9, 2015, pp. 1966-78.
Vasquez-Cardenas D, van de Vossenberg J, Polerecky L, et al. Microbial carbon metabolism associated with electrogenic sulphur oxidation in coastal sediments. ISME J. 2015;9(9):1966-78.
Vasquez-Cardenas, D., van de Vossenberg, J., Polerecky, L., Malkin, S. Y., Schauer, R., Hidalgo-Martinez, S., Confurius, V., Middelburg, J. J., Meysman, F. J., & Boschker, H. T. (2015). Microbial carbon metabolism associated with electrogenic sulphur oxidation in coastal sediments. The ISME Journal, 9(9), 1966-78. https://doi.org/10.1038/ismej.2015.10
Vasquez-Cardenas D, et al. Microbial Carbon Metabolism Associated With Electrogenic Sulphur Oxidation in Coastal Sediments. ISME J. 2015;9(9):1966-78. PubMed PMID: 25679534.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Microbial carbon metabolism associated with electrogenic sulphur oxidation in coastal sediments. AU - Vasquez-Cardenas,Diana, AU - van de Vossenberg,Jack, AU - Polerecky,Lubos, AU - Malkin,Sairah Y, AU - Schauer,Regina, AU - Hidalgo-Martinez,Silvia, AU - Confurius,Veronique, AU - Middelburg,Jack J, AU - Meysman,Filip J R, AU - Boschker,Henricus T S, Y1 - 2015/02/13/ PY - 2014/09/24/received PY - 2014/12/08/revised PY - 2014/12/16/accepted PY - 2015/2/14/entrez PY - 2015/2/14/pubmed PY - 2016/4/15/medline SP - 1966 EP - 78 JF - The ISME journal JO - ISME J VL - 9 IS - 9 N2 - 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 (13)C-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 (13)C-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 further study. SN - 1751-7370 UR - https://www.unboundmedicine.com/medline/citation/25679534/Microbial_carbon_metabolism_associated_with_electrogenic_sulphur_oxidation_in_coastal_sediments_ L2 - https://doi.org/10.1038/ismej.2015.10 DB - PRIME DP - Unbound Medicine ER -