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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
  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. https://doi.org/10.1038/nature20803.
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
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.
@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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    • Columbia University
    • DOI: 10.7916/d83b78f6

    Response of the sea‐ice diatom Fragilariopsis cylindrus to simulated polar night darkness and return to light
    journal, November 2019

    • Morin, Philippe‐Israël; Lacour, Thomas; Grondin, Pierre‐Luc
    • Limnology and Oceanography, Vol. 65, Issue 5
    • DOI: 10.1002/lno.11368

    Interactive effects of iron and light limitation on the molecular physiology of the Southern Ocean diatom Fragilariopsis kerguelensis
    journal, February 2020

    • Moreno, Carly M.; Gong, Weida; Cohen, Natalie R.
    • Limnology and Oceanography, Vol. 65, Issue 7
    • DOI: 10.1002/lno.11404

    15N photo-CIDNP MAS NMR on both photosystems and magnetic field-dependent 13C photo-CIDNP MAS NMR in photosystem II of the diatom Phaeodactylum tricornutum
    journal, September 2018


    Functional horizontal gene transfer from bacteria to eukaryotes
    journal, November 2017


    Identifying metabolic pathways for production of extracellular polymeric substances by the diatom Fragilariopsis cylindrus inhabiting sea ice
    journal, January 2018


    Physiology and iron modulate diverse responses of diatoms to a warming Southern Ocean
    journal, January 2019


    De novo transcriptome assembly and analysis of the freshwater araphid diatom Fragilaria radians, Lake Baikal
    journal, September 2019

    • Galachyants, Yuri Pavlovich; Zakharova, Yulia Robertovna; Volokitina, Nadezda Antonovna
    • Scientific Data, Vol. 6, Issue 1
    • DOI: 10.1038/s41597-019-0191-6

    Darkness-induced effects on gene expression in Cosmarium crenatum (Zygnematophyceae) from a polar habitat
    journal, July 2019


    Depth-dependent transcriptomic response of diatoms during spring bloom in the western subarctic Pacific Ocean
    journal, October 2019


    Phenomics reveals a novel putative chloroplast fatty acid transporter in the marine diatom Skeletonema marinoi involved in temperature acclimation
    journal, October 2019


    Building a locally diploid genome and transcriptome of the diatom Fragilariopsis cylindrus
    journal, October 2017

    • Paajanen, Pirita; Strauss, Jan; van Oosterhout, Cock
    • Scientific Data, Vol. 4, Issue 1
    • DOI: 10.1038/sdata.2017.149

    Transcriptomic response of the benthic freshwater diatom Nitzschia palea exposed to Few Layer Graphene
    journal, January 2019

    • Garacci, Marion; Barret, Maialen; Folgoas, Clément
    • Environmental Science: Nano, Vol. 6, Issue 5
    • DOI: 10.1039/c8en00987b

    Different iron storage strategies among bloom-forming diatoms
    journal, December 2018

    • Lampe, Robert H.; Mann, Elizabeth L.; Cohen, Natalie R.
    • Proceedings of the National Academy of Sciences, Vol. 115, Issue 52
    • DOI: 10.1073/pnas.1805243115

    Recurrent Loss, Horizontal Transfer, and the Obscure Origins of Mitochondrial Introns in Diatoms (Bacillariophyta)
    journal, May 2018

    • Guillory, Wilson X.; Onyshchenko, Anastasiia; Ruck, Elizabeth C.
    • Genome Biology and Evolution, Vol. 10, Issue 6
    • DOI: 10.1093/gbe/evy103

    The Parallel Molecular Adaptations to the Antarctic Cold Environment in Two Psychrophilic Green Algae
    journal, May 2019

    • Zhang, Zhenhua; Qu, Changfeng; Yao, Ru
    • Genome Biology and Evolution, Vol. 11, Issue 7
    • DOI: 10.1093/gbe/evz104

    First Estimation of the Spontaneous Mutation Rate in Diatoms
    journal, June 2019

    • Krasovec, Marc; Sanchez-Brosseau, Sophie; Piganeau, Gwenael
    • Genome Biology and Evolution, Vol. 11, Issue 7
    • DOI: 10.1093/gbe/evz130

    Signal, Uncertainty, and Conflict in Phylogenomic Data for a Diverse Lineage of Microbial Eukaryotes (Diatoms, Bacillariophyta)
    journal, October 2017

    • Parks, Matthew B.; Wickett, Norman J.; Alverson, Andrew J.
    • Molecular Biology and Evolution, Vol. 35, Issue 1
    • DOI: 10.1093/molbev/msx268

    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

    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

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


    Non-model model organisms
    journal, June 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

    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

    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