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Title: Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus

Abstract

The Southern Ocean houses a diverse and productive community of organisms. Unicellular eukaryotic diatoms are the main primary producers in this environment, where photosynthesis is limited by low concentrations of dissolved iron and large seasonal fluctuations in light, temperature and the extent of sea ice. How diatoms have adapted to this extreme environment is largely unknown. Here we present insights into the genome evolution of a cold-Adapted diatom from the Southern Ocean, Fragilariopsis cylindrus, based on a comparison with temperate diatoms. We find that approximately 24.7 per cent of the diploid F. cylindrus genome consists of genetic loci with alleles that are highly divergent (15.1 megabases of the total genome size of 61.1 megabases). These divergent alleles were differentially expressed across environmental conditions, including darkness, low iron, freezing, elevated temperature and increased CO2. Alleles with the largest ratio of non-synonymous to synonymous nucleotide substitutions also show the most pronounced condition-dependent expression, suggesting a correlation between diversifying selection and allelic differentiation. Divergent alleles may be involved in adaptation to environmental fluctuations in the Southern Ocean.

Authors:
 [1];  [2];  [1];  [3];  [3];  [4];  [2];  [5];  [1];  [6];  [7];  [7];  [8];  [9];  [10];  [1];  [2];  [11];  [5];  [11] more »;  [12];  [13];  [1];  [14];  [13];  [15];  [2];  [14];  [2];  [16];  [17];  [9];  [18];  [19];  [7];  [19];  [20];  [17];  [21];  [10];  [22];  [1];  [1];  [23] « less
+ Show Author Affiliations
  1. Univ. of East Anglia, Norwich (United Kingdom)
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  3. Norwich Research Park (United Kingdom). Earlham Inst.
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
  5. Stazione Zoologica Anton Dohrn, Naples (Italy)
  6. Univ. of East Anglia, Norwich (United Kingdom); Norwich Research Park (United Kingdom). Earlham Inst.
  7. J. Craig Venter Inst., La Jolla, CA (United States)
  8. Alfred-Wegener-Institut Helmholtz-Zentrum fur Polar- and Meeresforschung, Bremerhaven (Germany); Hochschule Bremerhaven (Germany)
  9. Univ. Paris-Saclay, Versailles (France)
  10. PSL Research Univ., Paris (France)
  11. Sorbonne Univ., Paris (France)
  12. Univ. of Cologne (Germany); Leibniz Inst. of Freshwater, Ecology and Inland Fisheries, Berlin (Germany)
  13. Univ. Konstanz (Germany)
  14. Medical Univ. of South Carolina, Charleston, SC (United States)
  15. Univ. of Duisburg-Essen (Germany)
  16. Leibniz Inst. fur Biodiversiat der Tiere, Bonn (Germany)
  17. Univ. of Washington, Seattle, WA (United States)
  18. Univ. of Nevada, Las Vegas, NV (United States)
  19. Alfred-Wegener-Institut Helmholtz-Zentrum fur Polar- and Meeresforschung, Bremerhaven (Germany)
  20. Monterey Bay Aquarium Research Inst., Moss Landing, CA (United States)
  21. Univ. of East Anglia, Norwich (United Kingdom); Norwich Research Park (United Kingdom). Earlham Inst.
  22. Univ. of British Columbia, Vancouver, BC (Canada)
  23. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1436620
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature (London)
Additional Journal Information:
Journal Name: Nature (London); Journal Volume: 541; Journal Issue: 7638; Journal ID: ISSN 0028-0836
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Mock, Thomas, Otillar, Robert P., Strauss, Jan, McMullan, Mark, Paajanen, Pirita, Schmutz, Jeremy, Salamov, Asaf, Sanges, Remo, Toseland, Andrew, Ward, Ben J., Allen, Andrew E., Dupont, Christopher L., Frickenhaus, Stephan, Maumus, Florian, Veluchamy, Alaguraj, Wu, Taoyang, Barry, Kerrie W., Falciatore, Angela, Ferrante, Maria I., Fortunato, Antonio E., Glockner, Gernot, Gruber, Ansgar, Hipkin, Rachel, Janech, Michael G., Kroth, Peter G., Leese, Florian, Lindquist, Erika A., Lyon, Barbara R., Martin, Joel, Mayer, Christoph, Parker, Micaela, Quesneville, Hadi, Raymond, James A., Uhlig, Christiane, Valas, Ruben E., Valentin, Klaus U., Worden, Alexandra Z., Armbrust, E. Virginia, Clark, Matthew D., Bowler, Chris, Green, Beverley R., Moulton, Vincent, van Oosterhout, Cock, and Grigoriev, Igor V. Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus. United States: N. p., 2017. Web. doi:10.1038/nature20803.
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Mock, Thomas, Otillar, Robert P., Strauss, Jan, McMullan, Mark, Paajanen, Pirita, Schmutz, Jeremy, Salamov, Asaf, Sanges, Remo, Toseland, Andrew, Ward, Ben J., Allen, Andrew E., Dupont, Christopher L., Frickenhaus, Stephan, Maumus, Florian, Veluchamy, Alaguraj, Wu, Taoyang, Barry, Kerrie W., Falciatore, Angela, Ferrante, Maria I., Fortunato, Antonio E., Glockner, Gernot, Gruber, Ansgar, Hipkin, Rachel, Janech, Michael G., Kroth, Peter G., Leese, Florian, Lindquist, Erika A., Lyon, Barbara R., Martin, Joel, Mayer, Christoph, Parker, Micaela, Quesneville, Hadi, Raymond, James A., Uhlig, Christiane, Valas, Ruben E., Valentin, Klaus U., Worden, Alexandra Z., Armbrust, E. Virginia, Clark, Matthew D., Bowler, Chris, Green, Beverley R., Moulton, Vincent, van Oosterhout, Cock, & Grigoriev, Igor V. Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus. United States. https://doi.org/10.1038/nature20803
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Mock, Thomas, Otillar, Robert P., Strauss, Jan, McMullan, Mark, Paajanen, Pirita, Schmutz, Jeremy, Salamov, Asaf, Sanges, Remo, Toseland, Andrew, Ward, Ben J., Allen, Andrew E., Dupont, Christopher L., Frickenhaus, Stephan, Maumus, Florian, Veluchamy, Alaguraj, Wu, Taoyang, Barry, Kerrie W., Falciatore, Angela, Ferrante, Maria I., Fortunato, Antonio E., Glockner, Gernot, Gruber, Ansgar, Hipkin, Rachel, Janech, Michael G., Kroth, Peter G., Leese, Florian, Lindquist, Erika A., Lyon, Barbara R., Martin, Joel, Mayer, Christoph, Parker, Micaela, Quesneville, Hadi, Raymond, James A., Uhlig, Christiane, Valas, Ruben E., Valentin, Klaus U., Worden, Alexandra Z., Armbrust, E. Virginia, Clark, Matthew D., Bowler, Chris, Green, Beverley R., Moulton, Vincent, van Oosterhout, Cock, and Grigoriev, Igor V. Thu . "Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus". United States. https://doi.org/10.1038/nature20803. https://www.osti.gov/servlets/purl/1436620.
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@article{osti_1436620,
title = {Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus},
author = {Mock, Thomas and Otillar, Robert P. and Strauss, Jan and McMullan, Mark and Paajanen, Pirita and Schmutz, Jeremy and Salamov, Asaf and Sanges, Remo and Toseland, Andrew and Ward, Ben J. and Allen, Andrew E. and Dupont, Christopher L. and Frickenhaus, Stephan and Maumus, Florian and Veluchamy, Alaguraj and Wu, Taoyang and Barry, Kerrie W. and Falciatore, Angela and Ferrante, Maria I. and Fortunato, Antonio E. and Glockner, Gernot and Gruber, Ansgar and Hipkin, Rachel and Janech, Michael G. and Kroth, Peter G. and Leese, Florian and Lindquist, Erika A. and Lyon, Barbara R. and Martin, Joel and Mayer, Christoph and Parker, Micaela and Quesneville, Hadi and Raymond, James A. and Uhlig, Christiane and Valas, Ruben E. and Valentin, Klaus U. and Worden, Alexandra Z. and Armbrust, E. Virginia and Clark, Matthew D. and Bowler, Chris and Green, Beverley R. and Moulton, Vincent and van Oosterhout, Cock and Grigoriev, Igor V.},
abstractNote = {The Southern Ocean houses a diverse and productive community of organisms. Unicellular eukaryotic diatoms are the main primary producers in this environment, where photosynthesis is limited by low concentrations of dissolved iron and large seasonal fluctuations in light, temperature and the extent of sea ice. How diatoms have adapted to this extreme environment is largely unknown. Here we present insights into the genome evolution of a cold-Adapted diatom from the Southern Ocean, Fragilariopsis cylindrus, based on a comparison with temperate diatoms. We find that approximately 24.7 per cent of the diploid F. cylindrus genome consists of genetic loci with alleles that are highly divergent (15.1 megabases of the total genome size of 61.1 megabases). These divergent alleles were differentially expressed across environmental conditions, including darkness, low iron, freezing, elevated temperature and increased CO2. Alleles with the largest ratio of non-synonymous to synonymous nucleotide substitutions also show the most pronounced condition-dependent expression, suggesting a correlation between diversifying selection and allelic differentiation. Divergent alleles may be involved in adaptation to environmental fluctuations in the Southern Ocean.},
doi = {10.1038/nature20803},
journal = {Nature (London)},
number = 7638,
volume = 541,
place = {United States},
year = {2017},
month = {1}
}
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    • Molecular Biology and Evolution, Vol. 35, Issue 1
    • DOI: 10.1093/molbev/msx268

    The evolution of diatoms and their biogeochemical functions
    journal, July 2017

    • Benoiston, Anne-Sophie; Ibarbalz, Federico M.; Bittner, Lucie
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1728
    • DOI: 10.1098/rstb.2016.0397

    The role of intraspecific variation in the ecological and evolutionary success of diatoms in changing environments
    journal, July 2017

    • Godhe, Anna; Rynearson, Tatiana
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1728
    • DOI: 10.1098/rstb.2016.0399

    Intracellular metabolic pathway distribution in diatoms and tools for genome-enabled experimental diatom research
    journal, July 2017

    • Gruber, Ansgar; Kroth, Peter G.
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1728
    • DOI: 10.1098/rstb.2016.0402

    Modulation of lipid biosynthesis by stress in diatoms
    journal, July 2017

    • Sayanova, Olga; Mimouni, Virginie; Ulmann, Lionel
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1728
    • DOI: 10.1098/rstb.2016.0407

    Relative stability of ploidy in a marine Synechococcus across various growth conditions: Stability of ploidy in a marine Synechococcus
    journal, February 2018

    • Perez-Sepulveda, Blanca; Pitt, Frances; N'Guyen, An N.
    • Environmental Microbiology Reports, Vol. 10, Issue 4
    • DOI: 10.1111/1758-2229.12614

    Digest: Fossils, evolutionary models, and diatoms*
    journal, December 2019

    Downregulation of mitochondrial alternative oxidase affects chloroplast function, redox status and stress response in a marine diatom
    journal, November 2018

    • Murik, Omer; Tirichine, Leila; Prihoda, Judit
    • New Phytologist, Vol. 221, Issue 3
    • DOI: 10.1111/nph.15479

    Microalgae biotechnology in Nordic countries – the potential of local strains
    journal, March 2019

    • Cheregi, Otilia; Ekendahl, Susanne; Engelbrektsson, Johan
    • Physiologia Plantarum, Vol. 166, Issue 1
    • DOI: 10.1111/ppl.12951

    High particulate iron(II) content in glacially sourced dusts enhances productivity of a model diatom
    journal, June 2017

    • Shoenfelt, Elizabeth M.; Sun, Jing; Winckler, Gisela
    • Science Advances, Vol. 3, Issue 6
    • DOI: 10.1126/sciadv.1700314

    Homoeolog expression bias in allopolyploid oleaginous marine diatom Fistulifera solaris
    journal, May 2018

    Non-model model organisms
    journal, June 2017

    Silicanin-1 is a conserved diatom membrane protein involved in silica biomineralization
    journal, July 2017

    A family of silicon transporter structural genes in a pennate diatom Synedra ulna subsp. danica (Kütz.) Skabitsch
    journal, August 2018

    The transcription factor bZIP14 regulates the TCA cycle in the diatom Phaeodactylum tricornutum
    journal, April 2017

    • Matthijs, Michiel; Fabris, Michele; Obata, Toshihiro
    • The EMBO Journal, Vol. 36, Issue 11
    • DOI: 10.15252/embj.201696392

    Diatom Biogeography From the Labrador Sea Revealed Through a Trait-Based Approach
    journal, September 2018

    • Fragoso, Glaucia M.; Poulton, Alex J.; Yashayaev, Igor M.
    • Frontiers in Marine Science, Vol. 5
    • DOI: 10.3389/fmars.2018.00297

    Thermal Niche Differentiation in the Benthic Diatom Cylindrotheca closterium (Bacillariophyceae) Complex
    journal, June 2019

    • Stock, Willem; Vanelslander, Bart; Rüdiger, Franziska
    • Frontiers in Microbiology, Vol. 10
    • DOI: 10.3389/fmicb.2019.01395

    Evolution and Expansion of the Prokaryote-Like Lipoxygenase Family in the Brown Alga Saccharina japonica
    journal, November 2017

    Intraspecific Diversity in the Cold Stress Response of Transposable Elements in the Diatom Leptocylindrus aporus
    journal, December 2019

    • Pargana, Aikaterini; Musacchia, Francesco; Sanges, Remo
    • Genes, Vol. 11, Issue 1
    • DOI: 10.3390/genes11010009

    Marine Natural Products from Microalgae: An -Omics Overview
    journal, May 2019

    • Lauritano, Chiara; Ferrante, Maria Immacolata; Rogato, Alessandra
    • Marine Drugs, Vol. 17, Issue 5
    • DOI: 10.3390/md17050269

    Assessment of genomic changes in a CRISPR/Cas9 Phaeodactylum tricornutum mutant through whole genome resequencing
    journal, January 2018

    • Russo, Monia Teresa; Aiese Cigliano, Riccardo; Sanseverino, Walter
    • PeerJ, Vol. 6
    • DOI: 10.7717/peerj.5507

    Considering the Role of Adaptive Evolution in Models of the Ocean and Climate System
    journal, November 2019

    • Ward, B. A.; Collins, S.; Dutkiewicz, S.
    • Journal of Advances in Modeling Earth Systems, Vol. 11, Issue 11
    • DOI: 10.1029/2018MS001452

    Molecular mechanisms of temperature acclimation and adaptation in marine diatoms
    journal, May 2019

    A genomics approach reveals the global genetic polymorphism, structure, and functional diversity of ten accessions of the marine model diatom Phaeodactylum tricornutum
    journal, October 2019

    • Rastogi, Achal; Vieira, Fabio Rocha Jimenez; Deton-Cabanillas, Anne-Flore
    • The ISME Journal, Vol. 14, Issue 2
    • DOI: 10.1038/s41396-019-0528-3

    DSYB catalyses the key step of dimethylsulfoniopropionate biosynthesis in many phytoplankton
    journal, February 2018

    • Curson, Andrew R. J.; Williams, Beth T.; Pinchbeck, Benjamin J.
    • Nature Microbiology, Vol. 3, Issue 4
    • DOI: 10.1038/s41564-018-0119-5

    Skeletonema marinoi as a new genetic model for marine chain-forming diatoms
    journal, April 2019

    Transcriptomic and proteomic responses of the oceanic diatom Pseudo-nitzschia granii to iron limitation
    journal, August 2018

    • Cohen, Natalie R.; Gong, Weida; Moran, Dawn M.
    • Environmental Microbiology, Vol. 20, Issue 8
    • DOI: 10.1111/1462-2920.14386

    The golden paradox – a new heterokont lineage with chloroplasts surrounded by two membranes
    journal, January 2019

    • Wetherbee, Richard; Jackson, Christopher J.; Repetti, Sonja I.
    • Journal of Phycology, Vol. 55, Issue 2
    • DOI: 10.1111/jpy.12822

    Use of exogenous glycine betaine and its precursor choline as osmoprotectants in Antarctic sea‐ice diatoms 1
    journal, February 2019

    • Torstensson, Anders; Young, Jodi N.; Carlson, Laura T.
    • Journal of Phycology, Vol. 55, Issue 3
    • DOI: 10.1111/jpy.12839

    Dark metabolism: a molecular insight into how the Antarctic sea‐ice diatom Fragilariopsis cylindrus survives long‐term darkness
    journal, May 2019

    • Kennedy, Fraser; Martin, Andrew; Bowman, John P.
    • New Phytologist, Vol. 223, Issue 2
    • DOI: 10.1111/nph.15843

    Structural basis for blue-green light harvesting and energy dissipation in diatoms
    journal, February 2019

    Culturable diversity of Arctic phytoplankton during pack ice melting
    journal, January 2020

    • Gérikas Ribeiro, Catherine; dos Santos, Adriana Lopes; Gourvil, Priscillia
    • Elementa: Science of the Anthropocene, Vol. 8
    • DOI: 10.1525/elementa.401

    A single loss of photosynthesis in the diatom order Bacillariales (Bacillariophyta)
    journal, March 2019

    • Onyshchenko, Anastasiia; Ruck, Elizabeth C.; Nakov, Teofil
    • American Journal of Botany, Vol. 106, Issue 4
    • DOI: 10.1002/ajb2.1267

    The Antarctic psychrophiles Chlamydomonas spp. UWO241 and ICE-MDV exhibit differential restructuring of photosystem I in response to iron
    journal, February 2019

    Non-model model organisms
    text, January 2017

    • M., Tanaka, Elly; A., Lancaster, Madeline; A., Theriot, Julie
    • The University of North Carolina at Chapel Hill University Libraries
    • DOI: 10.17615/az1d-gc50

    Evolutionary genomics can improve prediction of species’ responses to climate change
    text, January 2020

    • Waldvogel, Ann-Marie; Feldmeyer, Barbara; Rolshausen, Gregor
    • Wiley-Blackwell Publishing, Inc.
    • DOI: 10.5167/uzh-189086

    MRP3 is a sex determining gene in the diatom Pseudo-nitzschia multistriata
    journal, November 2018

    Lhcx proteins provide photoprotection via thermal dissipation of absorbed light in the diatom Phaeodactylum tricornutum
    journal, September 2019

    • Buck, Jochen M.; Sherman, Jonathan; Bártulos, Carolina Río
    • Nature Communications, Vol. 10, Issue 1
    • DOI: 10.1038/s41467-019-12043-6

    Proton-pumping rhodopsins are abundantly expressed by microbial eukaryotes in a high-Arctic fjord: Rhodopsin expression in Arctic marine eukaryotes
    journal, January 2018

    • Vader, Anna; Laughinghouse, Haywood D.; Griffiths, Colin
    • Environmental Microbiology, Vol. 20, Issue 2
    • DOI: 10.1111/1462-2920.14035

    Genetic tool development in marine protists: emerging model organisms for experimental cell biology
    text, January 2020

    • Faktorová, Drahomíra; Nisbet, R. Ellen R.; Fernández Robledo, José A.
    • Apollo - University of Cambridge Repository
    • DOI: 10.17863/cam.66602

    High particulate iron(II) content in glacially sourced dusts enhances productivity of a model diatom
    text, January 2017

    • Shoenfelt, Elizabeth M.; Sun, Jing; Winckler, Gisela
    • Columbia University
    • DOI: 10.7916/d83b78f6

    Extensive intraspecific gene order and gene structural variations between Mo17 and other maize genomes
    journal, July 2018

    Evolutionary genomics can improve prediction of species’ responses to climate change
    journal, January 2020

    • Waldvogel, Ann‐Marie; Feldmeyer, Barbara; Rolshausen, Gregor
    • Evolution Letters, Vol. 4, Issue 1
    • DOI: 10.1002/evl3.154

    Genetic tool development in marine protists: emerging model organisms for experimental cell biology
    text, January 2020

    • Faktorová, Drahomíra; Nisbet, R. Ellen R.; Fernández Robledo, José A.
    • Apollo - University of Cambridge Repository
    • DOI: 10.17863/cam.73594
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