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

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 reconstruc tions 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 organicmore » 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.« less
Authors:
 [1] ; ORCiD logo [1] ;  [1] ;  [1] ;  [2] ;  [3] ;  [4] ;  [5] ;  [6] ;  [7] ; ORCiD logo [4] ;  [3] ;  [1]
  1. Uppsala Univ. (Sweden). Dept. of Ecology and Genetics
  2. Uppsala Univ. (Sweden). Dept. of Ecology and Genetics, Uppsala Multidisciplinary Center for Advanced Computational Science
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Bigelow Lab. for Ocean Sciences, East Boothbay, ME (United States)
  5. Barcelona Supercomputing Centre (Spain). IRB-BSC Program in Computational Biology; Catalan Inst. of Research and Advanced Studies (ICREA), Barcelona (Spain)
  6. Univ. of Wisconsin, Madison, WI (United States). Dept. of Civil and Environmental Engineering, Dept. of Bacteriology
  7. Uppsala Univ. (Sweden). Dept. of Cellular and Molecular Biology
Publication Date:
Grant/Contract Number:
AC02-05CH11231
Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 10; Journal Issue: 8; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Research Org:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES
OSTI Identifier:
1379540

Eiler, Alexander, Mondav, Rhiannon, Sinclair, Lucas, Fernandez-Vidal, Leyden, Scofield, Douglas G., Schwientek, Patrick, Martinez-Garcia, Manuel, Torrents, David, McMahon, Katherine D., Andersson, Siv G. E., Stepanauskas, Ramunas, Woyke, Tanja, and Bertilsson, Stefan. Tuning fresh: radiation through rewiring of central metabolism in streamlined bacteria. United States: N. p., Web. doi:10.1038/ismej.2015.260.
Eiler, Alexander, Mondav, Rhiannon, Sinclair, Lucas, Fernandez-Vidal, Leyden, Scofield, Douglas G., Schwientek, Patrick, Martinez-Garcia, Manuel, Torrents, David, McMahon, Katherine D., Andersson, Siv G. E., Stepanauskas, Ramunas, Woyke, Tanja, & Bertilsson, Stefan. Tuning fresh: radiation through rewiring of central metabolism in streamlined bacteria. United States. doi:10.1038/ismej.2015.260.
Eiler, Alexander, Mondav, Rhiannon, Sinclair, Lucas, Fernandez-Vidal, Leyden, Scofield, Douglas G., Schwientek, Patrick, Martinez-Garcia, Manuel, Torrents, David, McMahon, Katherine D., Andersson, Siv G. E., Stepanauskas, Ramunas, Woyke, Tanja, and Bertilsson, Stefan. 2016. "Tuning fresh: radiation through rewiring of central metabolism in streamlined bacteria". United States. doi:10.1038/ismej.2015.260. https://www.osti.gov/servlets/purl/1379540.
@article{osti_1379540,
title = {Tuning fresh: radiation through rewiring of central metabolism in streamlined bacteria},
author = {Eiler, Alexander and Mondav, Rhiannon and Sinclair, Lucas and Fernandez-Vidal, Leyden and Scofield, Douglas G. and Schwientek, Patrick and Martinez-Garcia, Manuel and Torrents, David and McMahon, Katherine D. and Andersson, Siv G. E. and Stepanauskas, Ramunas and Woyke, Tanja and Bertilsson, Stefan},
abstractNote = {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 reconstruc tions 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.},
doi = {10.1038/ismej.2015.260},
journal = {The ISME Journal},
number = 8,
volume = 10,
place = {United States},
year = {2016},
month = {1}
}

Works referenced in this record:

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journal, March 2004
  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
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