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ISME J. 2016 Aug;10(8):1902-14. doi: 10.1038/ismej.2015.260. Epub 2016 Jan 19.

Tuning fresh: radiation through rewiring of central metabolism in streamlined bacteria.

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Department of Ecology and Genetics, Limnology and Science for Life Laboratory, Uppsala University, Uppsala, Sweden.
Department of Ecology and Genetics, Evolutionary Biology and Uppsala Multidisciplinary Center for Advanced Computational Science, Uppsala University, Uppsala, Sweden.
Department of Energy, Joint Genome Institute, Walnut Creek, CA, USA.
Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, USA.
IRB-BSC Program in Computational Biology, Barcelona Supercomputing Centre, Barcelona, Spain.
Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain.
Department of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, USA.
Department of Bacteriology, University of Wisconsin-Madison, Madison, WI, USA.
Department of Cellular and Molecular Biology, Molecular Evolution and Science for Life Laboratory, Uppsala University, Uppsala, Sweden.


Most free-living planktonic cells are streamlined and in spite of their limitations in functional flexibility, their vast populations have radiated into a wide range of aquatic habitats. Here we compared the metabolic potential of subgroups in the Alphaproteobacteria lineage SAR11 adapted to marine and freshwater habitats. Our results suggest that the successful leap from marine to freshwaters in SAR11 was accompanied by a loss of several carbon degradation pathways and a rewiring of the central metabolism. Examples for these are C1 and methylated compounds degradation pathways, the Entner-Doudouroff pathway, the glyoxylate shunt and anapleuretic carbon fixation being absent from the freshwater genomes. Evolutionary reconstructions further suggest that the metabolic modules making up these important freshwater metabolic traits were already present in the gene pool of ancestral marine SAR11 populations. The loss of the glyoxylate shunt had already occurred in the common ancestor of the freshwater subgroup and its closest marine relatives, suggesting that the adaptation to freshwater was a gradual process. Furthermore, our results indicate rapid evolution of TRAP transporters in the freshwater clade involved in the uptake of low molecular weight carboxylic acids. We propose that such gradual tuning of metabolic pathways and transporters toward locally available organic substrates is linked to the formation of subgroups within the SAR11 clade and that this process was critical for the freshwater clade to find and fix an adaptive phenotype.

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