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Title: 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 » 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:
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)
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}
}

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Works referenced in this record:

Contribution of SAR11 Bacteria to Dissolved Dimethylsulfoniopropionate and Amino Acid Uptake in the North Atlantic Ocean
journal, July 2004


Energy Starved Candidatus Pelagibacter Ubique Substitutes Light-Mediated ATP Production for Endogenous Carbon Respiration
journal, May 2011


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
  • DOI: 10.1073/pnas.97.13.6981

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
  • DOI: 10.1186/gb-2013-14-11-r130

Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis
journal, April 2000


The effect of nitrogen limitation on cellular DMSP and DMS release in marine phytoplankton: climate feedback implications
journal, August 2007


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
  • DOI: 10.1186/1745-6150-4-46

Single-Cell Genomics Reveals Hundreds of Coexisting Subpopulations in Wild Prochlorococcus
journal, April 2014


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
  • DOI: 10.1038/ismej.2013.32

Photochemical transformation of dissolved organic matter in lakes
journal, June 2000


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
  • DOI: 10.1038/nrmicro3218

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
  • DOI: 10.1038/ismej.2009.108

Dynamics of the SAR11 bacterioplankton lineage in relation to environmental conditions in the oligotrophic North Pacific subtropical gyre
journal, September 2009


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
  • DOI: 10.1128/MMBR.00028-10

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
  • DOI: 10.1093/nar/gkr1044

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
  • DOI: 10.1038/ismej.2012.122

RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006


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
  • DOI: 10.1038/ismej.2011.8

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
  • DOI: 10.1038/ismej.2008.117

Proteorhodopsin in the ubiquitous marine bacterium SAR11
journal, November 2005

  • Giovannoni, Stephen J.; Bibbs, Lisa; Cho, Jang-Cheon
  • Nature, Vol. 438, Issue 7064
  • DOI: 10.1038/nature04032

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
  • DOI: 10.1128/AEM.00107-11

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
  • DOI: 10.3354/ame01637

One Carbon Metabolism in SAR11 Pelagic Marine Bacteria
journal, August 2011


SAR11 clade dominates ocean surface bacterioplankton communities
journal, December 2002

  • Morris, Robert M.; Rappé, Michael S.; Connon, Stephanie A.
  • Nature, Vol. 420, Issue 6917
  • DOI: 10.1038/nature01240

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
  • DOI: 10.1038/nature06776

The Entner-Doudoroff pathway: history, physiology and molecular biology
journal, September 1992


The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific
journal, March 2007


Accelerated Profile HMM Searches
journal, October 2011


Estimating the Population Size for Capture-Recapture Data with Unequal Catchability
journal, December 1987


Streamlining and Core Genome Conservation among Highly Divergent Members of the SAR11 Clade
journal, September 2012


Infrequent marine–freshwater transitions in the microbial world
journal, September 2009


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
  • DOI: 10.1038/ismej.2014.60

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
  • DOI: 10.1038/ismej.2014.61

Genome Streamlining in a Cosmopolitan Oceanic Bacterium
journal, August 2005


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
  • DOI: 10.1038/ismej.2013.243

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
  • DOI: 10.1038/ismej.2012.86

Functional Tradeoffs Underpin Salinity-Driven Divergence in Microbial Community Composition
journal, February 2014


Directed networks reveal genomic barriers and DNA repair bypasses to lateral gene transfer among prokaryotes
journal, January 2011


The Pfam protein families database
journal, November 2011

  • Punta, M.; Coggill, P. C.; Eberhardt, R. Y.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1065

An efficient algorithm for large-scale detection of protein families
journal, April 2002


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
  • DOI: 10.1093/nar/gkh340

Comparative and Phylogenomic Evidence That the Alphaproteobacterium HIMB59 Is Not a Member of the Oceanic SAR11 Clade
journal, November 2013


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
  • DOI: 10.1016/S0304-4165(99)00155-5

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
  • DOI: 10.1073/pnas.1304246110

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
  • DOI: 10.1111/1462-2920.12301

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
  • DOI: 10.1016/S0723-2020(98)80067-2

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
  • DOI: 10.1038/ismej.2011.84

The presence of the glycolysis operon in SAR11 genomes is positively correlated with ocean productivity
journal, February 2010