Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus

Thomas Mock; Robert P. Otillar; Jan Strauss; Mark McMullan; Pirita Paajanen; Jeremy Schmutz; Asaf Salamov; Remo Sanges; Andrew Toseland; Ben J. Ward; Andrew E. Allen; Christopher L. Dupont; Stephan Frickenhaus; Florian Maumus; Alaguraj Veluchamy; Taoyang Wu; Kerrie W. Barry; Angela Falciatore; Maria I. Ferrante; Antonio E. Fortunato; Gernot Glöckner; Ansgar Gruber; Rachel Hipkin; Michael G. Janech; Peter G. Kroth; Florian Leese; Erika A. Lindquist; Barbara R. Lyon; Joel Martin; Christoph Mayer; Micaela Parker; Hadi Quesneville; James A. Raymond; Christiane Uhlig; Ruben E. Valas; Klaus U. Valentin; Alexandra Z. Worden; E. Virginia Armbrust; Matthew D. Clark; Chris Bowler; Beverley R. Green; Vincent Moulton; Cock van Oosterhout; Igor V. Grigoriev

doi:10.1038/nature20803

Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus

Thomas Mock, Robert P. Otillar, Jan Strauss, Mark McMullan, Pirita Paajanen, Jeremy Schmutz, Asaf Salamov, Remo Sanges, Andrew Toseland, Ben J. Ward, Andrew E. Allen, Christopher L. Dupont, Stephan Frickenhaus, Florian Maumus, Alaguraj Veluchamy, Taoyang Wu, Kerrie W. Barry, Angela Falciatore, Maria I. Ferrante, Antonio E. FortunatoGernot Glöckner, Ansgar Gruber, Rachel Hipkin, Michael G. Janech, Peter G. Kroth, Florian Leese, Erika A. Lindquist, Barbara R. Lyon, Joel Martin, Christoph Mayer, Micaela Parker, Hadi Quesneville, James A. Raymond, Christiane Uhlig, Ruben E. Valas, Klaus U. Valentin, Alexandra Z. Worden, E. Virginia Armbrust, Matthew D. Clark, Chris Bowler, Beverley R. Green, Vincent Moulton, Cock van Oosterhout, Igor V. Grigoriev

Biological, Environmental Sciences and Engineering

Research output: Contribution to journal › Article › peer-review

280 Scopus citations

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.

Original language	English (US)
Pages (from-to)	536-540
Number of pages	5
Journal	Nature
Volume	541
Issue number	7638
DOIs	https://doi.org/10.1038/nature20803
State	Published - Jan 16 2017

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: We thank A. Stecher and K. Schmidt for extracting and providing environmental DNA samples and the Natural Environment Research Council UK (NERC) Biomolecular Analysis Facility (NBAF) for conducting transcriptome sequencing and providing bioinformatics support. C.B. acknowledges funding from the ERC Advanced Grant ERC-2011-ADG (Diatomite). The work conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, was supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. PacBio sequencing and library construction was delivered via the BBSRC National Capability in Genomics (BB/J010375/1) at the Earlham Institute (formerly The Genome Analysis Centre, Norwich), by members of the Platforms and Pipelines Group, PacBio assembly and sequence analysis was strategically funded by the BBSRC, Institute Strategic Programme Grant (BB/J004669/1). Additional funding for this work was provided by NERC under grants NE/I001751/1, NE/K004530/1, MGF (NBAF) grant 197, The Royal Society grant RG090774 and the Earth & Life Systems Alliance in Norwich.

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https://repository.kaust.edu.sa/bitstream/10754/622831/1/nature20803.pdf

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Mock, T., Otillar, R. P., Strauss, J., McMullan, M., Paajanen, P., Schmutz, J., Salamov, A., Sanges, R., Toseland, A., Ward, B. J., Allen, A. E., Dupont, C. L., Frickenhaus, S., Maumus, F., Veluchamy, A., Wu, T., Barry, K. W., Falciatore, A., Ferrante, M. I., ... Grigoriev, I. V. (2017). Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus. Nature, 541(7638), 536-540. https://doi.org/10.1038/nature20803

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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.",

author = "Thomas Mock and Otillar, {Robert P.} and Jan Strauss and Mark McMullan and Pirita Paajanen and Jeremy Schmutz and Asaf Salamov and Remo Sanges and Andrew Toseland and Ward, {Ben J.} and Allen, {Andrew E.} and Dupont, {Christopher L.} and Stephan Frickenhaus and Florian Maumus and Alaguraj Veluchamy and Taoyang Wu and Barry, {Kerrie W.} and Angela Falciatore and Ferrante, {Maria I.} and Fortunato, {Antonio E.} and Gernot Gl{\"o}ckner and Ansgar Gruber and Rachel Hipkin and Janech, {Michael G.} and Kroth, {Peter G.} and Florian Leese and Lindquist, {Erika A.} and Lyon, {Barbara R.} and Joel Martin and Christoph Mayer and Micaela Parker and Hadi Quesneville and Raymond, {James A.} and Christiane Uhlig and Valas, {Ruben E.} and Valentin, {Klaus U.} and Worden, {Alexandra Z.} and Armbrust, {E. Virginia} and Clark, {Matthew D.} and Chris Bowler and Green, {Beverley R.} and Vincent Moulton and Oosterhout, {Cock van} and Grigoriev, {Igor V.}",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank A. Stecher and K. Schmidt for extracting and providing environmental DNA samples and the Natural Environment Research Council UK (NERC) Biomolecular Analysis Facility (NBAF) for conducting transcriptome sequencing and providing bioinformatics support. C.B. acknowledges funding from the ERC Advanced Grant ERC-2011-ADG (Diatomite). The work conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, was supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. PacBio sequencing and library construction was delivered via the BBSRC National Capability in Genomics (BB/J010375/1) at the Earlham Institute (formerly The Genome Analysis Centre, Norwich), by members of the Platforms and Pipelines Group, PacBio assembly and sequence analysis was strategically funded by the BBSRC, Institute Strategic Programme Grant (BB/J004669/1). Additional funding for this work was provided by NERC under grants NE/I001751/1, NE/K004530/1, MGF (NBAF) grant 197, The Royal Society grant RG090774 and the Earth & Life Systems Alliance in Norwich.",

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doi = "10.1038/nature20803",

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volume = "541",

pages = "536--540",

journal = "Nature",

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Mock, T, Otillar, RP, Strauss, J, McMullan, M, Paajanen, P, Schmutz, J, Salamov, A, Sanges, R, Toseland, A, Ward, BJ, Allen, AE, Dupont, CL, Frickenhaus, S, Maumus, F, Veluchamy, A, Wu, T, Barry, KW, Falciatore, A, Ferrante, MI, Fortunato, AE, Glöckner, G, Gruber, A, Hipkin, R, Janech, MG, Kroth, PG, Leese, F, Lindquist, EA, Lyon, BR, Martin, J, Mayer, C, Parker, M, Quesneville, H, Raymond, JA, Uhlig, C, Valas, RE, Valentin, KU, Worden, AZ, Armbrust, EV, Clark, MD, Bowler, C, Green, BR, Moulton, V, Oosterhout, CV & Grigoriev, IV 2017, 'Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus', Nature, vol. 541, no. 7638, pp. 536-540. https://doi.org/10.1038/nature20803

TY - JOUR

T1 - Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus

AU - Mock, Thomas

AU - Otillar, Robert P.

AU - Strauss, Jan

AU - McMullan, Mark

AU - Paajanen, Pirita

AU - Schmutz, Jeremy

AU - Salamov, Asaf

AU - Sanges, Remo

AU - Toseland, Andrew

AU - Ward, Ben J.

AU - Allen, Andrew E.

AU - Dupont, Christopher L.

AU - Frickenhaus, Stephan

AU - Maumus, Florian

AU - Veluchamy, Alaguraj

AU - Wu, Taoyang

AU - Barry, Kerrie W.

AU - Falciatore, Angela

AU - Ferrante, Maria I.

AU - Fortunato, Antonio E.

AU - Glöckner, Gernot

AU - Gruber, Ansgar

AU - Hipkin, Rachel

AU - Janech, Michael G.

AU - Kroth, Peter G.

AU - Leese, Florian

AU - Lindquist, Erika A.

AU - Lyon, Barbara R.

AU - Martin, Joel

AU - Mayer, Christoph

AU - Parker, Micaela

AU - Quesneville, Hadi

AU - Raymond, James A.

AU - Uhlig, Christiane

AU - Valas, Ruben E.

AU - Valentin, Klaus U.

AU - Worden, Alexandra Z.

AU - Armbrust, E. Virginia

AU - Clark, Matthew D.

AU - Bowler, Chris

AU - Green, Beverley R.

AU - Moulton, Vincent

AU - Oosterhout, Cock van

AU - Grigoriev, Igor V.

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank A. Stecher and K. Schmidt for extracting and providing environmental DNA samples and the Natural Environment Research Council UK (NERC) Biomolecular Analysis Facility (NBAF) for conducting transcriptome sequencing and providing bioinformatics support. C.B. acknowledges funding from the ERC Advanced Grant ERC-2011-ADG (Diatomite). The work conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, was supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. PacBio sequencing and library construction was delivered via the BBSRC National Capability in Genomics (BB/J010375/1) at the Earlham Institute (formerly The Genome Analysis Centre, Norwich), by members of the Platforms and Pipelines Group, PacBio assembly and sequence analysis was strategically funded by the BBSRC, Institute Strategic Programme Grant (BB/J004669/1). Additional funding for this work was provided by NERC under grants NE/I001751/1, NE/K004530/1, MGF (NBAF) grant 197, The Royal Society grant RG090774 and the Earth & Life Systems Alliance in Norwich.

PY - 2017/1/16

Y1 - 2017/1/16

N2 - 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.

AB - 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.

UR - http://hdl.handle.net/10754/622831

UR - http://www.nature.com/nature/journal/v541/n7638/full/nature20803.html

UR - http://www.scopus.com/inward/record.url?scp=85016137064&partnerID=8YFLogxK

U2 - 10.1038/nature20803

DO - 10.1038/nature20803

M3 - Article

C2 - 28092920

SN - 0028-0836

VL - 541

SP - 536

EP - 540

JO - Nature

JF - Nature

IS - 7638

ER -

Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus

Abstract

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