Open Access Research

Genomic analysis reveals key aspects of prokaryotic symbiosis in the phototrophic consortium “Chlorochromatium aggregatum

Zhenfeng Liu17, Johannes Müller2, Tao Li18, Richard M Alvey19, Kajetan Vogl1, Niels-Ulrik Frigaard3, Nathan C Rockwell4, Eric S Boyd5, Lynn P Tomsho1, Stephan C Schuster1, Petra Henke2, Manfred Rohde6, Jörg Overmann2 and Donald A Bryant15*

Author Affiliations

1 Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, PA 16802, USA

2 Leibniz-Institut DSMZ-Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Inhoffenstraße 7B, 38124, Braunschweig, Germany

3 Section for Marine Biology, Department of Biology, University of Copenhagen, Strandpromenaden 5 3000, Helsingør, Denmark

4 Department of Molecular and Cellular Biology, University of California, Davis, CA 95616, USA

5 Department of Microbiology, Montana State University, Bozeman, MT 59717, USA

6 Helmholtz-Zentrum für Infektionsforschung, 38124 Braunschweig, Germany

7 Current address: Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089, USA

8 Current address: Algal Genomics Research Group, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei 430072, China

9 Current address: Department of Biology, Chaminade University, Honolulu, HI 96816, USA

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Genome Biology 2013, 14:R127  doi:10.1186/gb-2013-14-11-r127

Published: 22 November 2013

Abstract

Background

Chlorochromatium aggregatum’ is a phototrophic consortium, a symbiosis that may represent the highest degree of mutual interdependence between two unrelated bacteria not associated with a eukaryotic host. ‘Chlorochromatium aggregatum’ is a motile, barrel-shaped aggregate formed from a single cell of ‘Candidatus Symbiobacter mobilis”, a polarly flagellated, non-pigmented, heterotrophic bacterium, which is surrounded by approximately 15 epibiont cells of Chlorobium chlorochromatii, a non-motile photolithoautotrophic green sulfur bacterium.

Results

We analyzed the complete genome sequences of both organisms to understand the basis for this symbiosis. Chl. chlorochromatii has acquired relatively few symbiosis-specific genes; most acquired genes are predicted to modify the cell wall or function in cell-cell adhesion. In striking contrast, ‘Ca. S. mobilis’ appears to have undergone massive gene loss, is probably no longer capable of independent growth, and thus may only reproduce when consortia divide. A detailed model for the energetic and metabolic bases of the dependency of ‘Ca. S. mobilis’ on Chl. chlorochromatii is described.

Conclusions

Genomic analyses suggest that three types of interactions lead to a highly sophisticated relationship between these two organisms. Firstly, extensive metabolic exchange, involving carbon, nitrogen, and sulfur sources as well as vitamins, occurs from the epibiont to the central bacterium. Secondly, ‘Ca. S. mobilis’ can sense and move towards light and sulfide, resources that only directly benefit the epibiont. Thirdly, electron cycling mechanisms, particularly those mediated by quinones and potentially involving shared protonmotive force, could provide an important basis for energy exchange in this and other symbiotic relationships.