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

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

doi:10.1038/ismej.2015.260

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

Journal Article · Tue Jan 19 00:00:00 EST 2016 · The ISME Journal

DOI:https://doi.org/10.1038/ismej.2015.260· OSTI ID:1379540

Eiler, Alexander ^[1];

^[1]; Sinclair, Lucas ^[1]; Fernandez-Vidal, Leyden ^[1]; Scofield, Douglas G. ^[2]; Schwientek, Patrick ^[3]; Martinez-Garcia, Manuel ^[4]; Torrents, David ^[5]; McMahon, Katherine D. ^[6]; Andersson, Siv G. E. ^[7];

^[4]; Woyke, Tanja ^[3]; Bertilsson, Stefan ^[1]

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

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1379540

Journal Information:: The ISME Journal, Vol. 10, Issue 8; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 27 works

Citation information provided by
Web of Science

References (68)

The sRNA SorY confers resistance during photooxidative stress by affecting a metabolite transporter in Rhodobacter sphaeroides Adnan, Fazal; Weber, Lennart; Klug, Gabriele Taylor & Francis https://doi.org/10.6084/m9.figshare.1378764.v2	text	January 2015
Resourceful heterotrophs make the most of light in the coastal ocean Moran, Mary Ann; Miller, William L. Nature Reviews Microbiology, Vol. 5, Issue 10 https://doi.org/10.1038/nrmicro1746	journal	October 2007
Energy Starved Candidatus Pelagibacter Ubique Substitutes Light-Mediated ATP Production for Endogenous Carbon Respiration Steindler, Laura; Schwalbach, Michael S.; Smith, Daniel P. PLoS ONE, Vol. 6, Issue 5 https://doi.org/10.1371/journal.pone.0019725	journal	May 2011
The sRNA SorY confers resistance during photooxidative stress by affecting a metabolite transporter in Rhodobacter sphaeroides Adnan, Fazal; Weber, Lennart; Klug, Gabriele RNA Biology, Vol. 12, Issue 5 https://doi.org/10.1080/15476286.2015.1031948	journal	March 2015
Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis Castresana, J. Molecular Biology and Evolution, Vol. 17, Issue 4 https://doi.org/10.1093/oxfordjournals.molbev.a026334	journal	April 2000
Natural variation in SAR11 marine bacterioplankton genomes inferred from metagenomic data Wilhelm, Larry J.; Tripp, H. James; Givan, Scott A. Biology Direct, Vol. 2, Issue 1 https://doi.org/10.1186/1745-6150-2-27	journal	January 2007
Comparative and Phylogenomic Evidence That the Alphaproteobacterium HIMB59 Is Not a Member of the Oceanic SAR11 Clade Viklund, Johan; Martijn, Joran; Ettema, Thijs J. G. PLoS ONE, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pone.0078858	journal	November 2013
The Evolution of Two-Component Systems in Bacteria Reveals Different Strategies for Niche Adaptation Alm, Eric; Huang, Katherine; Arkin, Adam PLoS Computational Biology, Vol. 2, Issue 11 https://doi.org/10.1371/journal.pcbi.0020143	journal	January 2006
Single cell genomics of deep ocean bacteria Zhao, Weizhou; Andersson, Siv G. E. Trends in Microbiology, Vol. 22, Issue 5 https://doi.org/10.1016/j.tim.2014.03.002	journal	May 2014
Evolution by leaps: gene duplication in bacteria Serres, Margrethe H.; Kerr, Alastair RW; McCormack, Thomas J. Biology Direct, Vol. 4, Issue 1 https://doi.org/10.1186/1745-6150-4-46	journal	January 2009
Contribution of SAR11 Bacteria to Dissolved Dimethylsulfoniopropionate and Amino Acid Uptake in the North Atlantic Ocean Malmstrom, R. R.; Kiene, R. P.; Cottrell, M. T. Applied and Environmental Microbiology, Vol. 70, Issue 7 https://doi.org/10.1128/aem.70.7.4129-4135.2004	journal	July 2004
High-resolution SAR11 ecotype dynamics at the Bermuda Atlantic Time-series Study site by phylogenetic placement of pyrosequences Vergin, Kevin L.; Beszteri, Bánk; Monier, Adam The ISME Journal, Vol. 7, Issue 7 https://doi.org/10.1038/ismej.2013.32	journal	March 2013
Pyrosequencing reveals contrasting seasonal dynamics of taxa within Baltic Sea bacterioplankton communities Andersson, Anders F.; Riemann, Lasse; Bertilsson, Stefan The ISME Journal, Vol. 4, Issue 2 https://doi.org/10.1038/ismej.2009.108	journal	October 2009
Directed networks reveal genomic barriers and DNA repair bypasses to lateral gene transfer among prokaryotes Popa, O.; Hazkani-Covo, E.; Landan, G. Genome Research, Vol. 21, Issue 4 https://doi.org/10.1101/gr.115592.110	journal	January 2011
Dynamics of the SAR11 bacterioplankton lineage in relation to environmental conditions in the oligotrophic North Pacific subtropical gyre Eiler, Alexander; Hayakawa, Darin H.; Church, Matthew J. Environmental Microbiology, Vol. 11, Issue 9 https://doi.org/10.1111/j.1462-2920.2009.01954.x	journal	September 2009
Nutrient requirements for growth of the extreme oligotroph ‘Candidatus Pelagibacter ubique’ HTCC1062 on a defined medium Carini, Paul; Steindler, Laura; Beszteri, Sara The ISME Journal, Vol. 7, Issue 3 https://doi.org/10.1038/ismej.2012.122	journal	October 2012
An H-NS-like Stealth Protein Aids Horizontal DNA Transmission in Bacteria Doyle, M.; Fookes, M.; Ivens, A. Science, Vol. 315, Issue 5809 https://doi.org/10.1126/science.1137550	journal	January 2007
Bacterial Species and Speciation Cohan, Frederick M. Systematic Biology, Vol. 50, Issue 4 https://doi.org/10.1080/10635150118398	journal	August 2001
The Entner-Doudoroff pathway: history, physiology and molecular biology Conway, Tyrrell FEMS Microbiology Letters, Vol. 103, Issue 1 https://doi.org/10.1111/j.1574-6968.1992.tb05822.x	journal	September 1992
SAR11 clade dominates ocean surface bacterioplankton communities Morris, Robert M.; Rappé, Michael S.; Connon, Stephanie A. Nature, Vol. 420, Issue 6917 https://doi.org/10.1038/nature01240	journal	December 2002
SAR11 marine bacteria require exogenous reduced sulphur for growth Tripp, H. James; Kitner, Joshua B.; Schwalbach, Michael S. Nature, Vol. 452, Issue 7188 https://doi.org/10.1038/nature06776	journal	March 2008
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
Estimating the Population Size for Capture-Recapture Data with Unequal Catchability Chao, Anne Biometrics, Vol. 43, Issue 4 https://doi.org/10.2307/2531532	journal	December 1987
Selfish operons: the evolutionary impact of gene clustering in prokaryotes and eukaryotes Lawrence, Jeffrey Current Opinion in Genetics & Development, Vol. 9, Issue 6 https://doi.org/10.1016/S0959-437X(99)00025-8	journal	December 1999
One Carbon Metabolism in SAR11 Pelagic Marine Bacteria Sun, Jing; Steindler, Laura; Thrash, J. Cameron PLoS ONE, Vol. 6, Issue 8 https://doi.org/10.1371/journal.pone.0023973	journal	August 2011
The size and continuity of DNA segments integrated in Bacillus transformation. Zawadzki, P.; Cohan, F. M. Genetics, Vol. 141, Issue 4 https://doi.org/10.1093/genetics/141.4.1231	journal	December 1995
Infrequent marine–freshwater transitions in the microbial world Logares, Ramiro; Bråte, Jon; Bertilsson, Stefan Trends in Microbiology, Vol. 17, Issue 9 https://doi.org/10.1016/j.tim.2009.05.010	journal	September 2009
Implications of streamlining theory for microbial ecology Giovannoni, Stephen J.; Cameron Thrash, J.; Temperton, Ben The ISME Journal, Vol. 8, Issue 8 https://doi.org/10.1038/ismej.2014.60	journal	April 2014
Discovery of a SAR11 growth requirement for thiamin’s pyrimidine precursor and its distribution in the Sargasso Sea Carini, Paul; Campbell, Emily O.; Morré, Jeff The ISME Journal, Vol. 8, Issue 8 https://doi.org/10.1038/ismej.2014.61	journal	April 2014
Single-cell enabled comparative genomics of a deep ocean SAR11 bathytype Cameron Thrash, J.; Temperton, Ben; Swan, Brandon K. The ISME Journal, Vol. 8, Issue 7 https://doi.org/10.1038/ismej.2013.243	journal	January 2014
La enhances IRES-mediated translation of laminin B1 during malignant epithelial to mesenchymal transition Petz, Michaela; Them, Nicole; Huber, Heidemarie Nucleic Acids Research, Vol. 40, Issue 1 https://doi.org/10.1093/nar/gkr717	journal	September 2011
Metabolic potential of a single cell belonging to one of the most abundant lineages in freshwater bacterioplankton Garcia, Sarahi L.; McMahon, Katherine D.; Martinez-Garcia, Manuel The ISME Journal, Vol. 7, Issue 1 https://doi.org/10.1038/ismej.2012.86	journal	July 2012
Bacterial Catabolism of Dimethylsulfoniopropionate (DMSP) Reisch, Chris R.; Moran, Mary Ann; Whitman, William B. Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00172	journal	January 2011
The Pfam protein families database Punta, M.; Coggill, P. C.; Eberhardt, R. Y. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1065	journal	November 2011
The Passive Yet Successful Way of Planktonic Life: Genomic and Experimental Analysis of the Ecology of a Free-Living Polynucleobacter Population Hahn, Martin W.; Scheuerl, Thomas; Jezberová, Jitka PLoS ONE, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pone.0032772	journal	March 2012
An efficient algorithm for large-scale detection of protein families Enright, A. J. Nucleic Acids Research, Vol. 30, Issue 7 https://doi.org/10.1093/nar/30.7.1575	journal	April 2002
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean Swan, B. K.; Tupper, B.; Sczyrba, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 28 https://doi.org/10.1073/pnas.1304246110	journal	June 2013
Productivity and salinity structuring of the microplankton revealed by comparative freshwater metagenomics: Comparative freshwater metagenomics Eiler, Alexander; Zaremba-Niedzwiedzka, Katarzyna; Martínez-García, Manuel Environmental Microbiology, Vol. 16, Issue 9 https://doi.org/10.1111/1462-2920.12301	journal	November 2013
High-throughput single-cell sequencing identifies photoheterotrophs and chemoautotrophs in freshwater bacterioplankton Martinez-Garcia, Manuel; Swan, Brandon K.; Poulton, Nicole J. The ISME Journal, Vol. 6, Issue 1 https://doi.org/10.1038/ismej.2011.84	journal	June 2011
Seasonal bloom dynamics and ecophysiology of the freshwater sister clade of SAR11 bacteria 'that rule the waves' (LD12) Salcher, M. M.; Pernthaler, J.; Posch, T. Nature Publishing Group https://doi.org/10.5167/uzh-59995	text	January 2011
The Entner-Doudoroff pathway: history, physiology and molecular biology Conway, T. FEMS Microbiology Letters, Vol. 103, Issue 1 https://doi.org/10.1016/0378-1097(92)90334-k	journal	September 1992
Bacterial Species and Speciation Cohan, Frederick M. Systematic Biology, Vol. 50, Issue 4 https://doi.org/10.1080/106351501750435077	journal	August 2001
Bacteria are different: Observations, interpretations, speculations, and opinions about the mechanisms of adaptive evolution in prokaryotes Levin, B. R.; Bergstrom, C. T. Proceedings of the National Academy of Sciences, Vol. 97, Issue 13 https://doi.org/10.1073/pnas.97.13.6981	journal	June 2000
Unique glycine-activated riboswitch linked to glycine-serine auxotrophy in SAR11 Tripp, H. James; Schwalbach, Michael S.; Meyer, Michelle M. Environmental Microbiology, Vol. 11, Issue 1 https://doi.org/10.1111/j.1462-2920.2008.01758.x	journal	January 2009
The presence of the glycolysis operon in SAR11 genomes is positively correlated with ocean productivity Schwalbach, M. S.; Tripp, H. J.; Steindler, L. Environmental Microbiology, Vol. 12, Issue 2 https://doi.org/10.1111/j.1462-2920.2009.02092.x	journal	February 2010
Single-cell genomics reveal low recombination frequencies in freshwater bacteria of the SAR11 clade Zaremba-Niedzwiedzka, Katarzyna; Viklund, Johan; Zhao, Weizhou Genome Biology, Vol. 14, Issue 11 https://doi.org/10.1186/gb-2013-14-11-r130	journal	January 2013
Auxotrophy and intrapopulation complementary in the ‘interactome’ of a cultivated freshwater model community Garcia, Sarahi L.; Buck, Moritz; McMahon, Katherine D. Molecular Ecology, Vol. 24, Issue 17 https://doi.org/10.1111/mec.13319	journal	August 2015
The effect of nitrogen limitation on cellular DMSP and DMS release in marine phytoplankton: climate feedback implications Sunda, William G.; Hardison, Rance; Kiene, Ronald P. Aquatic Sciences, Vol. 69, Issue 3 https://doi.org/10.1007/s00027-007-0887-0	journal	August 2007
Involvement of the compatible solutes trehalose and sucrose in the response to salt stress of a cyanobacterial Scytonema species isolated from desert soils Page-Sharp, Madhu; Behm, Carolyn A.; Smith, Geoffrey D. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1472, Issue 3 https://doi.org/10.1016/s0304-4165(99)00155-5	journal	November 1999
High intraspecific recombination rate in a native population of Candidatus Pelagibacter ubique (SAR11) Vergin, Kevin L.; Tripp, H. James; Wilhelm, Larry J. Environmental Microbiology, Vol. 9, Issue 10 https://doi.org/10.1111/j.1462-2920.2007.01361.x	journal	October 2007
Single-Cell Genomics Reveals Hundreds of Coexisting Subpopulations in Wild Prochlorococcus Kashtan, N.; Roggensack, S. E.; Rodrigue, S. Science, Vol. 344, Issue 6182 https://doi.org/10.1126/science.1248575	journal	April 2014
Photochemical transformation of dissolved organic matter in lakes Bertilsson, Stefan; Tranvik, Lars J. Limnology and Oceanography, Vol. 45, Issue 4 https://doi.org/10.4319/lo.2000.45.4.0753	journal	June 2000
Dynamics of the response of cyanobacteria to salt stress: Deciphering the molecular events Joset, Francoise; Jeanjean, Robert; Hagemann, Martin Physiologia Plantarum, Vol. 96, Issue 4 https://doi.org/10.1111/j.1399-3054.1996.tb00251.x	journal	April 1996
Explaining microbial genomic diversity in light of evolutionary ecology Cordero, Otto X.; Polz, Martin F. Nature Reviews Microbiology, Vol. 12, Issue 4 https://doi.org/10.1038/nrmicro3218	journal	March 2014
Functional Tradeoffs Underpin Salinity-Driven Divergence in Microbial Community Composition Dupont, Chris L.; Larsson, John; Yooseph, Shibu PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0089549	journal	February 2014
Genome Streamlining in a Cosmopolitan Oceanic Bacterium Giovannoni, S. J. Science, Vol. 309, Issue 5738 https://doi.org/10.1126/science.1114057	journal	August 2005
IMG: the integrated microbial genomes database and comparative analysis system Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1044	journal	December 2011
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models Stamatakis, Alexandros Bioinformatics, Vol. 22, Issue 21 https://doi.org/10.1093/bioinformatics/btl446	journal	August 2006
Seasonal bloom dynamics and ecophysiology of the freshwater sister clade of SAR11 bacteria ‘that rule the waves’ (LD12) Salcher, Michaela M.; Pernthaler, Jakob; Posch, Thomas The ISME Journal, Vol. 5, Issue 8 https://doi.org/10.1038/ismej.2011.8	journal	March 2011
Metagenomic Insights into the Evolution, Function, and Complexity of the Planktonic Microbial Community of Lake Lanier, a Temperate Freshwater Ecosystem Oh, Seungdae; Caro-Quintero, Alejandro; Tsementzi, Despina Applied and Environmental Microbiology, Vol. 77, Issue 17 https://doi.org/10.1128/aem.00107-11	journal	July 2011
Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea Carlson, Craig A.; Morris, Robert; Parsons, Rachel The ISME Journal, Vol. 3, Issue 3 https://doi.org/10.1038/ismej.2008.117	journal	December 2008
A Guide to the Natural History of Freshwater Lake Bacteria Newton, R. J.; Jones, S. E.; Eiler, A. Microbiology and Molecular Biology Reviews, Vol. 75, Issue 1 https://doi.org/10.1128/mmbr.00028-10	journal	March 2011
Proteorhodopsin in the ubiquitous marine bacterium SAR11 Giovannoni, Stephen J.; Bibbs, Lisa; Cho, Jang-Cheon Nature, Vol. 438, Issue 7064 https://doi.org/10.1038/nature04032	journal	November 2005
Seasonality and environmental control of freshwater SAR11 (LD12) in a temperate lake (Lake Erken, Sweden) Heinrich, F.; Eiler, A.; Bertilsson, S. Aquatic Microbial Ecology, Vol. 70, Issue 1 https://doi.org/10.3354/ame01637	journal	August 2013
Nearly Identical 16S rRNA Sequences Recovered from Lakes in North America and Europe Indicate the Existence of Clades of Globally Distributed Freshwater Bacteria Zwart, Gabriel; Hiorns, William D.; Methé, Barbara A. Systematic and Applied Microbiology, Vol. 21, Issue 4 https://doi.org/10.1016/s0723-2020(98)80067-2	journal	December 1998
The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific Rusch, Douglas B.; Halpern, Aaron L.; Sutton, Granger PLoS Biology, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pbio.0050077	journal	March 2007
Glucose and Gluconic acid Oxidation of Pseudomonas Saccharophila Entner, Nathan; Doudoroff, Michael Journal of Biological Chemistry, Vol. 196, Issue 2 https://doi.org/10.1016/s0021-9258(19)52415-2	journal	June 1952

Cited By (18)

Bacterial succession along a sediment porewater gradient at Lake Neusiedl in Austria von Hoyningen-Huene, Avril Jean Elisabeth; Schneider, Dominik; Fussmann, Dario Scientific Data, Vol. 6, Issue 1 https://doi.org/10.1038/s41597-019-0172-9	journal	August 2019
Hidden in plain sight—highly abundant and diverse planktonic freshwater Chloroflexi Mehrshad, Maliheh; Salcher, Michaela M.; Okazaki, Yusuke BioMed Central https://doi.org/10.5167/uzh-163119	text	January 2018
Model communities hint at promiscuous metabolic linkages between ubiquitous free-living freshwater bacteria Garcia, Sarahi L.; Buck, Moritz; Hamilton, Joshua J. Universität Potsdam https://doi.org/10.25932/publishup-42729	text	January 2019
Cultivation and genomics of the first freshwater SAR11 (LD12) isolate Henson, Michael W.; Lanclos, V. Celeste; Faircloth, Brant C. The ISME Journal, Vol. 12, Issue 7 https://doi.org/10.1038/s41396-018-0092-2	journal	March 2018
Model Communities Hint at Promiscuous Metabolic Linkages between Ubiquitous Free-Living Freshwater Bacteria Garcia, Sarahi L.; Buck, Moritz; Hamilton, Joshua J. mSphere, Vol. 3, Issue 3 https://doi.org/10.1128/msphere.00202-18	journal	May 2018
Hidden in plain sight—highly abundant and diverse planktonic freshwater Chloroflexi Mehrshad, Maliheh; Salcher, Michaela M.; Okazaki, Yusuke Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0563-8	journal	October 2018
Wide Distribution of Phage That Infect Freshwater SAR11 Bacteria Chen, Lin-Xing; Zhao, Yanlin; McMahon, Katherine D. mSystems, Vol. 4, Issue 5 https://doi.org/10.1128/msystems.00410-19	journal	October 2019
Freshwater carbon and nutrient cycles revealed through reconstructed population genomes Linz, Alexandra M.; He, Shaomei; Stevens, Sarah L. R. PeerJ, Vol. 6 https://doi.org/10.7717/peerj.6075	journal	January 2018
Niche-specific metabolic adaptation in biotrophic and necrotrophic oomycetes is manifested in differential use of nutrients, variation in gene content, and enzyme evolution Ah-Fong, Audrey M. V.; Kagda, Meenakshi S.; Abrahamian, Melania PLOS Pathogens, Vol. 15, Issue 4 https://doi.org/10.1371/journal.ppat.1007729	journal	April 2019
Repeated evolutionary transitions of flavobacteria from marine to non-marine habitats: Repeated evolutionary transitions Zhang, Hao; Yoshizawa, Susumu; Sun, Ying Environmental Microbiology, Vol. 21, Issue 2 https://doi.org/10.1111/1462-2920.14509	journal	January 2019
Correction for Props et al., “Gene Expansion and Positive Selection as Bacterial Adaptations to Oligotrophic Conditions” Props, Ruben; Monsieurs, Pieter; Vandamme, Peter mSphere, Vol. 5, Issue 6 https://doi.org/10.1128/msphere.01143-20	journal	December 2020
Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake Okazaki, Yusuke; Nishimura, Yosuke; Yoshida, Takashi Environmental Microbiology, Vol. 21, Issue 12 https://doi.org/10.1111/1462-2920.14816	journal	September 2019
Prokaryotic Population Dynamics and Viral Predation in a Marine Succession Experiment Using Metagenomics Haro-Moreno, Jose M.; Rodriguez-Valera, Francisco; López-Pérez, Mario Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02926	journal	December 2019
Gene Expansion and Positive Selection as Bacterial Adaptations to Oligotrophic Conditions Props, Ruben; Monsieurs, Pieter; Vandamme, Peter mSphere, Vol. 4, Issue 1 https://doi.org/10.1128/mspheredirect.00011-19	journal	February 2019
Metabolic evolution and the self-organization of ecosystems Braakman, Rogier; Follows, Michael J.; Chisholm, Sallie W. Proceedings of the National Academy of Sciences, Vol. 114, Issue 15 https://doi.org/10.1073/pnas.1619573114	journal	March 2017
Competition and niche separation of pelagic bacteria in freshwater habitats Pernthaler, Jakob Wiley-Blackwell Publishing, Inc. https://doi.org/10.5167/uzh-147652	text	January 2017
Genomes from uncultivated prokaryotes: a comparison of metagenome-assembled and single-amplified genomes Alneberg, Johannes; Karlsson, Christofer M. G.; Divne, Anna-Maria Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0550-0	journal	September 2018
Competition and niche separation of pelagic bacteria in freshwater habitats: Niches of freshwater bacterioplankton Pernthaler, Jakob Environmental Microbiology, Vol. 19, Issue 6 https://doi.org/10.1111/1462-2920.13742	journal	May 2017

Similar Records

Reevaluating the Salty Divide: Phylogenetic Specificity of Transitions between Marine and Freshwater Systems

Journal Article · Tue Nov 13 00:00:00 EST 2018 · mSystems · OSTI ID:1379540

Paver, Sara F.; Muratore, Daniel; Newton, Ryan J.; +1 more

Evolutionary Divergence of Marinobacter Strains in Cryopeg Brines as Revealed by Pangenomics

Journal Article · Mon Jun 06 00:00:00 EDT 2022 · Frontiers in Microbiology · OSTI ID:1379540

Cooper, Zachary S.; Rapp, Josephine Z.; Shoemaker, Anna M. D.; +3 more

Contrasting patterns of genome-level diversity across distinct co-occurring bacterial populations

Journal Article · Fri Dec 08 00:00:00 EST 2017 · The ISME Journal · OSTI ID:1379540

Garcia, Sarahi L.; Stevens, Sarah L. R.; Crary, Benjamin; +8 more

Related Subjects

54 ENVIRONMENTAL SCIENCES
59 BASIC BIOLOGICAL SCIENCES

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

Citation Formats

References (68)

Cited By (18)

Similar Records

Related Subjects