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

Eiler, Alexander ; Mondav, Rhiannon LU orcid ; Sinclair, Lucas ; Fernandez-Vidal, Leyden ; Scofield, Douglas G ; Schwientek, Patrick ; Martinez-Garcia, Manuel ; Torrents, David ; McMahon, Katherine D and Andersson, Siv Ge , et al. (2016) In The Isme Journal 10(8). p.1902-1914
Abstract

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... (More)

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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type
Contribution to journal
publication status
published
subject
keywords
Adaptation, Physiological, Alphaproteobacteria/genetics, Biological Evolution, Carbon/metabolism, Ecosystem, Fresh Water/microbiology, Phenotype, Phylogeny, Plankton/genetics
in
The Isme Journal
volume
10
issue
8
pages
1902 - 1914
publisher
Nature Publishing Group
external identifiers
  • scopus:84954485294
  • pmid:26784354
ISSN
1751-7362
DOI
10.1038/ismej.2015.260
language
English
LU publication?
no
id
677fb4d9-6afa-4e53-a340-bb2f8049cc19
date added to LUP
2023-06-05 16:01:42
date last changed
2024-04-05 18:48:16
@article{677fb4d9-6afa-4e53-a340-bb2f8049cc19,
  abstract     = {{<p>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.</p>}},
  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 Ge and Stepanauskas, Ramunas and Woyke, Tanja and Bertilsson, Stefan}},
  issn         = {{1751-7362}},
  keywords     = {{Adaptation, Physiological; Alphaproteobacteria/genetics; Biological Evolution; Carbon/metabolism; Ecosystem; Fresh Water/microbiology; Phenotype; Phylogeny; Plankton/genetics}},
  language     = {{eng}},
  number       = {{8}},
  pages        = {{1902--1914}},
  publisher    = {{Nature Publishing Group}},
  series       = {{The Isme Journal}},
  title        = {{Tuning fresh : radiation through rewiring of central metabolism in streamlined bacteria}},
  url          = {{http://dx.doi.org/10.1038/ismej.2015.260}},
  doi          = {{10.1038/ismej.2015.260}},
  volume       = {{10}},
  year         = {{2016}},
}