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 Lab. (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:
- 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. 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. Tue .
"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}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 13 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Bacterial Species and Speciation
journal, August 2001
- Cohan, Frederick M.
- Systematic Biology, Vol. 50, Issue 4
Contribution of SAR11 Bacteria to Dissolved Dimethylsulfoniopropionate and Amino Acid Uptake in the North Atlantic Ocean
journal, July 2004
- Malmstrom, R. R.; Kiene, R. P.; Cottrell, M. T.
- Applied and Environmental Microbiology, Vol. 70, Issue 7
Resourceful heterotrophs make the most of light in the coastal ocean
journal, October 2007
- Moran, Mary Ann; Miller, William L.
- Nature Reviews Microbiology, Vol. 5, Issue 10
Energy Starved Candidatus Pelagibacter Ubique Substitutes Light-Mediated ATP Production for Endogenous Carbon Respiration
journal, May 2011
- Steindler, Laura; Schwalbach, Michael S.; Smith, Daniel P.
- PLoS ONE, Vol. 6, Issue 5
Bacteria are different: Observations, interpretations, speculations, and opinions about the mechanisms of adaptive evolution in prokaryotes
journal, June 2000
- Levin, B. R.; Bergstrom, C. T.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 13
Unique glycine-activated riboswitch linked to glycine-serine auxotrophy in SAR11
journal, January 2009
- Tripp, H. James; Schwalbach, Michael S.; Meyer, Michelle M.
- Environmental Microbiology, Vol. 11, Issue 1
Single-cell genomics reveal low recombination frequencies in freshwater bacteria of the SAR11 clade
journal, January 2013
- Zaremba-Niedzwiedzka, Katarzyna; Viklund, Johan; Zhao, Weizhou
- Genome Biology, Vol. 14, Issue 11
The sRNA SorY confers resistance during photooxidative stress by affecting a metabolite transporter in Rhodobacter sphaeroides
journal, March 2015
- Adnan, Fazal; Weber, Lennart; Klug, Gabriele
- RNA Biology, Vol. 12, Issue 5
Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis
journal, April 2000
- Castresana, J.
- Molecular Biology and Evolution, Vol. 17, Issue 4
Natural variation in SAR11 marine bacterioplankton genomes inferred from metagenomic data
journal, January 2007
- Wilhelm, Larry J.; Tripp, H. James; Givan, Scott A.
- Biology Direct, Vol. 2, Issue 1
The effect of nitrogen limitation on cellular DMSP and DMS release in marine phytoplankton: climate feedback implications
journal, August 2007
- Sunda, William G.; Hardison, Rance; Kiene, Ronald P.
- Aquatic Sciences, Vol. 69, Issue 3
The Evolution of Two-Component Systems in Bacteria Reveals Different Strategies for Niche Adaptation
journal, January 2006
- Alm, Eric; Huang, Katherine; Arkin, Adam
- PLoS Computational Biology, Vol. 2, Issue 11
Evolution by leaps: gene duplication in bacteria
journal, January 2009
- Serres, Margrethe H.; Kerr, Alastair RW; McCormack, Thomas J.
- Biology Direct, Vol. 4, Issue 1
Single-Cell Genomics Reveals Hundreds of Coexisting Subpopulations in Wild Prochlorococcus
journal, April 2014
- Kashtan, N.; Roggensack, S. E.; Rodrigue, S.
- Science, Vol. 344, Issue 6182
High-resolution SAR11 ecotype dynamics at the Bermuda Atlantic Time-series Study site by phylogenetic placement of pyrosequences
journal, March 2013
- Vergin, Kevin L.; Beszteri, Bánk; Monier, Adam
- The ISME Journal, Vol. 7, Issue 7
Photochemical transformation of dissolved organic matter in lakes
journal, June 2000
- Bertilsson, Stefan; Tranvik, Lars J.
- Limnology and Oceanography, Vol. 45, Issue 4
Dynamics of the response of cyanobacteria to salt stress: Deciphering the molecular events
journal, April 1996
- Joset, Francoise; Jeanjean, Robert; Hagemann, Martin
- Physiologia Plantarum, Vol. 96, Issue 4
Explaining microbial genomic diversity in light of evolutionary ecology
journal, March 2014
- Cordero, Otto X.; Polz, Martin F.
- Nature Reviews Microbiology, Vol. 12, Issue 4
Pyrosequencing reveals contrasting seasonal dynamics of taxa within Baltic Sea bacterioplankton communities
journal, October 2009
- Andersson, Anders F.; Riemann, Lasse; Bertilsson, Stefan
- The ISME Journal, Vol. 4, Issue 2
Dynamics of the SAR11 bacterioplankton lineage in relation to environmental conditions in the oligotrophic North Pacific subtropical gyre
journal, September 2009
- Eiler, Alexander; Hayakawa, Darin H.; Church, Matthew J.
- Environmental Microbiology, Vol. 11, Issue 9
A Guide to the Natural History of Freshwater Lake Bacteria
journal, March 2011
- Newton, R. J.; Jones, S. E.; Eiler, A.
- Microbiology and Molecular Biology Reviews, Vol. 75, Issue 1
IMG: the integrated microbial genomes database and comparative analysis system
journal, December 2011
- Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K.
- Nucleic Acids Research, Vol. 40, Issue D1
Nutrient requirements for growth of the extreme oligotroph ‘Candidatus Pelagibacter ubique’ HTCC1062 on a defined medium
journal, October 2012
- Carini, Paul; Steindler, Laura; Beszteri, Sara
- The ISME Journal, Vol. 7, Issue 3
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006
- Stamatakis, Alexandros
- Bioinformatics, Vol. 22, Issue 21
Seasonal bloom dynamics and ecophysiology of the freshwater sister clade of SAR11 bacteria ‘that rule the waves’ (LD12)
journal, March 2011
- Salcher, Michaela M.; Pernthaler, Jakob; Posch, Thomas
- The ISME Journal, Vol. 5, Issue 8
Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea
journal, December 2008
- Carlson, Craig A.; Morris, Robert; Parsons, Rachel
- The ISME Journal, Vol. 3, Issue 3
Proteorhodopsin in the ubiquitous marine bacterium SAR11
journal, November 2005
- Giovannoni, Stephen J.; Bibbs, Lisa; Cho, Jang-Cheon
- Nature, Vol. 438, Issue 7064
Metagenomic Insights into the Evolution, Function, and Complexity of the Planktonic Microbial Community of Lake Lanier, a Temperate Freshwater Ecosystem
journal, July 2011
- Oh, Seungdae; Caro-Quintero, Alejandro; Tsementzi, Despina
- Applied and Environmental Microbiology, Vol. 77, Issue 17
Seasonality and environmental control of freshwater SAR11 (LD12) in a temperate lake (Lake Erken, Sweden)
journal, August 2013
- Heinrich, F.; Eiler, A.; Bertilsson, S.
- Aquatic Microbial Ecology, Vol. 70, Issue 1
One Carbon Metabolism in SAR11 Pelagic Marine Bacteria
journal, August 2011
- Sun, Jing; Steindler, Laura; Thrash, J. Cameron
- PLoS ONE, Vol. 6, Issue 8
SAR11 clade dominates ocean surface bacterioplankton communities
journal, December 2002
- Morris, Robert M.; Rappé, Michael S.; Connon, Stephanie A.
- Nature, Vol. 420, Issue 6917
SAR11 marine bacteria require exogenous reduced sulphur for growth
journal, March 2008
- Tripp, H. James; Kitner, Joshua B.; Schwalbach, Michael S.
- Nature, Vol. 452, Issue 7188
The Entner-Doudoroff pathway: history, physiology and molecular biology
journal, September 1992
- Conway, Tyrrell
- FEMS Microbiology Letters, Vol. 103, Issue 1
The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific
journal, March 2007
- Rusch, Douglas B.; Halpern, Aaron L.; Sutton, Granger
- PLoS Biology, Vol. 5, Issue 3
Accelerated Profile HMM Searches
journal, October 2011
- Eddy, Sean R.
- PLoS Computational Biology, Vol. 7, Issue 10
Estimating the Population Size for Capture-Recapture Data with Unequal Catchability
journal, December 1987
- Chao, Anne
- Biometrics, Vol. 43, Issue 4
Selfish operons: the evolutionary impact of gene clustering in prokaryotes and eukaryotes
journal, December 1999
- Lawrence, Jeffrey
- Current Opinion in Genetics & Development, Vol. 9, Issue 6
Streamlining and Core Genome Conservation among Highly Divergent Members of the SAR11 Clade
journal, September 2012
- Grote, Jana; Thrash, J. Cameron; Huggett, Megan J.
- mBio, Vol. 3, Issue 5
Infrequent marine–freshwater transitions in the microbial world
journal, September 2009
- Logares, Ramiro; Bråte, Jon; Bertilsson, Stefan
- Trends in Microbiology, Vol. 17, Issue 9
Implications of streamlining theory for microbial ecology
journal, April 2014
- Giovannoni, Stephen J.; Cameron Thrash, J.; Temperton, Ben
- The ISME Journal, Vol. 8, Issue 8
Discovery of a SAR11 growth requirement for thiamin’s pyrimidine precursor and its distribution in the Sargasso Sea
journal, April 2014
- Carini, Paul; Campbell, Emily O.; Morré, Jeff
- The ISME Journal, Vol. 8, Issue 8
Genome Streamlining in a Cosmopolitan Oceanic Bacterium
journal, August 2005
- Giovannoni, S. J.
- Science, Vol. 309, Issue 5738
Single-cell enabled comparative genomics of a deep ocean SAR11 bathytype
journal, January 2014
- Cameron Thrash, J.; Temperton, Ben; Swan, Brandon K.
- The ISME Journal, Vol. 8, Issue 7
Metabolic potential of a single cell belonging to one of the most abundant lineages in freshwater bacterioplankton
journal, July 2012
- Garcia, Sarahi L.; McMahon, Katherine D.; Martinez-Garcia, Manuel
- The ISME Journal, Vol. 7, Issue 1
Functional Tradeoffs Underpin Salinity-Driven Divergence in Microbial Community Composition
journal, February 2014
- Dupont, Chris L.; Larsson, John; Yooseph, Shibu
- PLoS ONE, Vol. 9, Issue 2
Directed networks reveal genomic barriers and DNA repair bypasses to lateral gene transfer among prokaryotes
journal, January 2011
- Popa, O.; Hazkani-Covo, E.; Landan, G.
- Genome Research, Vol. 21, Issue 4
Bacterial Catabolism of Dimethylsulfoniopropionate (DMSP)
journal, January 2011
- Reisch, Chris R.; Moran, Mary Ann; Whitman, William B.
- Frontiers in Microbiology, Vol. 2
An H-NS-like Stealth Protein Aids Horizontal DNA Transmission in Bacteria
journal, January 2007
- Doyle, M.; Fookes, M.; Ivens, A.
- Science, Vol. 315, Issue 5809
The Pfam protein families database
journal, November 2011
- Punta, M.; Coggill, P. C.; Eberhardt, R. Y.
- Nucleic Acids Research, Vol. 40, Issue D1
The Passive Yet Successful Way of Planktonic Life: Genomic and Experimental Analysis of the Ecology of a Free-Living Polynucleobacter Population
journal, March 2012
- Hahn, Martin W.; Scheuerl, Thomas; Jezberová, Jitka
- PLoS ONE, Vol. 7, Issue 3
An efficient algorithm for large-scale detection of protein families
journal, April 2002
- Enright, A. J.
- Nucleic Acids Research, Vol. 30, Issue 7
High intraspecific recombination rate in a native population of Candidatus Pelagibacter ubique (SAR11)
journal, October 2007
- Vergin, Kevin L.; Tripp, H. James; Wilhelm, Larry J.
- Environmental Microbiology, Vol. 9, Issue 10
MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004
- Edgar, R. C.
- Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
Comparative and Phylogenomic Evidence That the Alphaproteobacterium HIMB59 Is Not a Member of the Oceanic SAR11 Clade
journal, November 2013
- Viklund, Johan; Martijn, Joran; Ettema, Thijs J. G.
- PLoS ONE, Vol. 8, Issue 11
Involvement of the compatible solutes trehalose and sucrose in the response to salt stress of a cyanobacterial Scytonema species isolated from desert soils
journal, November 1999
- Page-Sharp, Madhu; Behm, Carolyn A.; Smith, Geoffrey D.
- Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1472, Issue 3
Auxotrophy and intrapopulation complementary in the ‘interactome’ of a cultivated freshwater model community
journal, August 2015
- Garcia, Sarahi L.; Buck, Moritz; McMahon, Katherine D.
- Molecular Ecology, Vol. 24, Issue 17
Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean
journal, June 2013
- Swan, B. K.; Tupper, B.; Sczyrba, A.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 28
Productivity and salinity structuring of the microplankton revealed by comparative freshwater metagenomics: Comparative freshwater metagenomics
journal, November 2013
- Eiler, Alexander; Zaremba-Niedzwiedzka, Katarzyna; Martínez-García, Manuel
- Environmental Microbiology, Vol. 16, Issue 9
Nearly Identical 16S rRNA Sequences Recovered from Lakes in North America and Europe Indicate the Existence of Clades of Globally Distributed Freshwater Bacteria
journal, December 1998
- Zwart, Gabriel; Hiorns, William D.; Methé, Barbara A.
- Systematic and Applied Microbiology, Vol. 21, Issue 4
High-throughput single-cell sequencing identifies photoheterotrophs and chemoautotrophs in freshwater bacterioplankton
journal, June 2011
- Martinez-Garcia, Manuel; Swan, Brandon K.; Poulton, Nicole J.
- The ISME Journal, Vol. 6, Issue 1
The presence of the glycolysis operon in SAR11 genomes is positively correlated with ocean productivity
journal, February 2010
- Schwalbach, M. S.; Tripp, H. J.; Steindler, L.
- Environmental Microbiology, Vol. 12, Issue 2
Bacterial Species and Speciation
journal, August 2001
- Cohan, Frederick M.
- Systematic Biology, Vol. 50, Issue 4
The Entner-Doudoroff pathway: history, physiology and molecular biology
journal, September 1992
- Conway, T.
- FEMS Microbiology Letters, Vol. 103, Issue 1
Works referencing / citing this record:
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
Bacterial succession along a sediment porewater gradient at Lake Neusiedl in Austria
journal, August 2019
- von Hoyningen-Huene, Avril Jean Elisabeth; Schneider, Dominik; Fussmann, Dario
- Scientific Data, Vol. 6, Issue 1
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: Niches of freshwater bacterioplankton
journal, May 2017
- Pernthaler, Jakob
- Environmental Microbiology, Vol. 19, Issue 6
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
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
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
Wide Distribution of Phage That Infect Freshwater SAR11 Bacteria
journal, October 2019
- Chen, Lin-Xing; Zhao, Yanlin; McMahon, Katherine D.
- mSystems, Vol. 4, Issue 5
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
Hidden in plain sight—highly abundant and diverse planktonic freshwater Chloroflexi
journal, October 2018
- Mehrshad, Maliheh; Salcher, Michaela M.; Okazaki, Yusuke
- Microbiome, Vol. 6, Issue 1
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
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
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