Biogeography, Evolution, and Diversity of Epibionts in Phototrophic Consortia

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Abstract
Motile phototrophic consortia are highly regular associations in which numerous cells of green sulfur bacteria surround a flagellated colorless β-proteobacterium in the center. To date, seven different morphological types of such consortia have been described. In addition, two immotile associations involving green sulfur bacteria are known. By employing a culture-independent approach, different types of phototrophic consortia were mechanically isolated by micromanipulation from 14 freshwater environments, and partial 16S rRNA gene sequences of the green sulfur bacterial epibionts were determined. In the majority of the lakes investigated, different types of phototrophic consortia were found to co-occur. In all cases, phototrophic consortia with the same morphology from the same habitat contained only a single epibiont phylotype. However, morphologically indistinguishable phototrophic consortia collected from different lakes contained different epibionts. Overall, 19 different types of epibionts were detected in the present study. Whereas the epibionts within one geographic region were very similar (Dice coefficient, 0.582), only two types of epibionts were found to occur on both the European and North American continents (Dice coefficient, 0.190). None of the epibiont 16S rRNA gene sequences have been detected so far in free-living green sulfur bacteria, suggesting that the interaction between epibionts and chemotrophic bacteria in the phototrophic consortia is an obligate interaction. Based on our phylogenetic analysis, the epibiont sequences are not monophyletic. Thus, the ability to form symbiotic associations either arose independently from different ancestors or was present in a common ancestor prior to the radiation of green sulfur bacteria and the transition to the free-living state in independent lineages. The present study thus demonstrates that there is great diversity and nonrandom geographical distribution of phototrophic consortia in the natural environment.