U.S. Department of EnergyOffice of Scientific and Technical Information
Tuning fresh: radiation through rewiring of central metabolism in streamlined bacteria
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 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 »
- Authors:
-
[1];
[4];
- Uppsala Univ. (Sweden). Dept. of Ecology and Genetics
- Uppsala Univ. (Sweden). Dept. of Ecology and Genetics, Uppsala Multidisciplinary Center for Advanced Computational Science
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- Bigelow Lab. for Ocean Sciences, East Boothbay, ME (United States)
- Barcelona Supercomputing Centre (Spain). IRB-BSC Program in Computational Biology; Catalan Inst. of Research and Advanced Studies (ICREA), Barcelona (Spain)
- Univ. of Wisconsin, Madison, WI (United States). Dept. of Civil and Environmental Engineering, Dept. of Bacteriology
- Uppsala Univ. (Sweden). Dept. of Cellular and Molecular Biology
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1379540
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Journal Article: 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
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
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., 2016.
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. https://doi.org/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. https://doi.org/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},
url = {https://www.osti.gov/biblio/1379540},
journal = {The ISME Journal},
issn = {1751-7362},
number = 8,
volume = 10,
place = {United States},
year = {Tue Jan 19 00:00:00 EST 2016},
month = {Tue Jan 19 00:00:00 EST 2016}
}
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Hidden in plain sight—highly abundant and diverse planktonic freshwater Chloroflexi
text, January 2018
- Mehrshad, Maliheh; Salcher, Michaela M.; Okazaki, Yusuke
- BioMed Central
Freshwater carbon and nutrient cycles revealed through reconstructed population genomes
journal, January 2018
- Linz, Alexandra M.; He, Shaomei; Stevens, Sarah L. R.
- PeerJ, Vol. 6
Niche-specific metabolic adaptation in biotrophic and necrotrophic oomycetes is manifested in differential use of nutrients, variation in gene content, and enzyme evolution
journal, April 2019
- Ah-Fong, Audrey M. V.; Kagda, Meenakshi S.; Abrahamian, Melania
- PLOS Pathogens, Vol. 15, Issue 4
Repeated evolutionary transitions of flavobacteria from marine to non-marine habitats: Repeated evolutionary transitions
journal, January 2019
- Zhang, Hao; Yoshizawa, Susumu; Sun, Ying
- Environmental Microbiology, Vol. 21, Issue 2
Correction for Props et al., “Gene Expansion and Positive Selection as Bacterial Adaptations to Oligotrophic Conditions”
journal, December 2020
- Props, Ruben; Monsieurs, Pieter; Vandamme, Peter
- mSphere, Vol. 5, Issue 6
Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake
journal, September 2019
- Okazaki, Yusuke; Nishimura, Yosuke; Yoshida, Takashi
- Environmental Microbiology, Vol. 21, Issue 12
Prokaryotic Population Dynamics and Viral Predation in a Marine Succession Experiment Using Metagenomics
journal, December 2019
- Haro-Moreno, Jose M.; Rodriguez-Valera, Francisco; López-Pérez, Mario
- Frontiers in Microbiology, Vol. 10
Gene Expansion and Positive Selection as Bacterial Adaptations to Oligotrophic Conditions
journal, February 2019
- Props, Ruben; Monsieurs, Pieter; Vandamme, Peter
- mSphere, Vol. 4, Issue 1
Prokaryotic Population Dynamics and Viral Predation in a Marine Succession Experiment Using Metagenomics
journal, December 2019
- Haro-Moreno, Jose M.; Rodriguez-Valera, Francisco; López-Pérez, Mario
- Frontiers in Microbiology, Vol. 10
Niche-specific metabolic adaptation in biotrophic and necrotrophic oomycetes is manifested in differential use of nutrients, variation in gene content, and enzyme evolution
journal, April 2019
- Ah-Fong, Audrey M. V.; Kagda, Meenakshi S.; Abrahamian, Melania
- PLOS Pathogens, Vol. 15, Issue 4
Metabolic evolution and the self-organization of ecosystems
journal, March 2017
- Braakman, Rogier; Follows, Michael J.; Chisholm, Sallie W.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 15
Competition and niche separation of pelagic bacteria in freshwater habitats
text, January 2017
- Pernthaler, Jakob
- Wiley-Blackwell Publishing, Inc.
Genomes from uncultivated prokaryotes: a comparison of metagenome-assembled and single-amplified genomes
journal, September 2018
- Alneberg, Johannes; Karlsson, Christofer M. G.; Divne, Anna-Maria
- Microbiome, Vol. 6, Issue 1
Competition and niche separation of pelagic bacteria in freshwater habitats: Niches of freshwater bacterioplankton
journal, May 2017
- Pernthaler, Jakob
- Environmental Microbiology, Vol. 19, Issue 6
Model Communities Hint at Promiscuous Metabolic Linkages between Ubiquitous Free-Living Freshwater Bacteria
journal, May 2018
- Garcia, Sarahi L.; Buck, Moritz; Hamilton, Joshua J.
- mSphere, Vol. 3, Issue 3
Cultivation and genomics of the first freshwater SAR11 (LD12) isolate
journal, March 2018
- Henson, Michael W.; Lanclos, V. Celeste; Faircloth, Brant C.
- The ISME Journal, Vol. 12, Issue 7