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Title: Designer diatom episomes delivered by bacterial conjugation

Abstract

Eukaryotic microalgae hold great promise for the bioproduction of fuels and higher value chemicals. However, compared with model genetic organisms such as Escherichia coli and Saccharomyces cerevisiae, characterization of the complex biology and biochemistry of algae and strain improvement has been hampered by the inefficient genetic tools. To date, many algal species are transformable only via particle bombardment, and the introduced DNA is integrated randomly into the nuclear genome. Here we describe the first nuclear episomal vector for diatoms and a plasmid delivery method via conjugation from Escherichia coli to the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana. We identify a yeast-derived sequence that enables stable episome replication in these diatoms even in the absence of antibiotic selection and show that episomes are maintained as closed circles at copy number equivalent to native chromosomes. This highly efficient genetic system facilitates high-throughput functional characterization of algal genes and accelerates molecular phytoplankton research.

Authors:
 [1];  [2];  [3];  [3];  [1];  [1];  [1];  [3];  [4];  [3];  [3];  [3];  [4];  [1];  [1];  [1];  [5];  [2];  [3];  [1]
+ Show Author Affiliations
  1. J. Craig Venter Inst., La Jolla, CA (United States). Synthetic Biology and Bioenergy Group
  2. J. Craig Venter Inst., La Jolla, CA (United States). Microbial and Environmental Genomics Group; Univ. of California, San Diego, CA (United States). Integrative Oceanography Division. Scripps Inst. of Oceanography
  3. J. Craig Venter Inst., La Jolla, CA (United States). Microbial and Environmental Genomics Group
  4. Univ. of California, San Diego, CA (United States). National Center for Microscopy and Imaging Research
  5. J. Craig Venter Inst., La Jolla, CA (United States). Synthetic Biology and Bioenergy Group. Microbial and Environmental Genomics Group
Publication Date:
Research Org.:
J. Craig Venter Inst., La Jolla, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Synthetic Genomics Inc. (United States); Gordon and Betty Moore Foundation (United States); Natural Sciences and Engineering Research Council of Canada (NSERC)
OSTI Identifier:
1455147
Grant/Contract Number:  
SC0008593; GBMF3828
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Karas, Bogumil J., Diner, Rachel E., Lefebvre, Stephane C., McQuaid, Jeff, Phillips, Alex P. R., Noddings, Chari M., Brunson, John K., Valas, Ruben E., Deerinck, Thomas J., Jablanovic, Jelena, Gillard, Jeroen T. F., Beeri, Karen, Ellisman, Mark H., Glass, John I., Hutchison, Clyde A., Smith, Hamilton O., Venter, J. Craig, Allen, Andrew E., Dupont, Christopher L., and Weyman, Philip D. Designer diatom episomes delivered by bacterial conjugation. United States: N. p., 2015. Web. doi:10.1038/ncomms7925.
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Karas, Bogumil J., Diner, Rachel E., Lefebvre, Stephane C., McQuaid, Jeff, Phillips, Alex P. R., Noddings, Chari M., Brunson, John K., Valas, Ruben E., Deerinck, Thomas J., Jablanovic, Jelena, Gillard, Jeroen T. F., Beeri, Karen, Ellisman, Mark H., Glass, John I., Hutchison, Clyde A., Smith, Hamilton O., Venter, J. Craig, Allen, Andrew E., Dupont, Christopher L., & Weyman, Philip D. Designer diatom episomes delivered by bacterial conjugation. United States. https://doi.org/10.1038/ncomms7925
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Karas, Bogumil J., Diner, Rachel E., Lefebvre, Stephane C., McQuaid, Jeff, Phillips, Alex P. R., Noddings, Chari M., Brunson, John K., Valas, Ruben E., Deerinck, Thomas J., Jablanovic, Jelena, Gillard, Jeroen T. F., Beeri, Karen, Ellisman, Mark H., Glass, John I., Hutchison, Clyde A., Smith, Hamilton O., Venter, J. Craig, Allen, Andrew E., Dupont, Christopher L., and Weyman, Philip D. Tue . "Designer diatom episomes delivered by bacterial conjugation". United States. https://doi.org/10.1038/ncomms7925. https://www.osti.gov/servlets/purl/1455147.
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@article{osti_1455147,
title = {Designer diatom episomes delivered by bacterial conjugation},
author = {Karas, Bogumil J. and Diner, Rachel E. and Lefebvre, Stephane C. and McQuaid, Jeff and Phillips, Alex P. R. and Noddings, Chari M. and Brunson, John K. and Valas, Ruben E. and Deerinck, Thomas J. and Jablanovic, Jelena and Gillard, Jeroen T. F. and Beeri, Karen and Ellisman, Mark H. and Glass, John I. and Hutchison, Clyde A. and Smith, Hamilton O. and Venter, J. Craig and Allen, Andrew E. and Dupont, Christopher L. and Weyman, Philip D.},
abstractNote = {Eukaryotic microalgae hold great promise for the bioproduction of fuels and higher value chemicals. However, compared with model genetic organisms such as Escherichia coli and Saccharomyces cerevisiae, characterization of the complex biology and biochemistry of algae and strain improvement has been hampered by the inefficient genetic tools. To date, many algal species are transformable only via particle bombardment, and the introduced DNA is integrated randomly into the nuclear genome. Here we describe the first nuclear episomal vector for diatoms and a plasmid delivery method via conjugation from Escherichia coli to the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana. We identify a yeast-derived sequence that enables stable episome replication in these diatoms even in the absence of antibiotic selection and show that episomes are maintained as closed circles at copy number equivalent to native chromosomes. This highly efficient genetic system facilitates high-throughput functional characterization of algal genes and accelerates molecular phytoplankton research.},
doi = {10.1038/ncomms7925},
journal = {Nature Communications},
number = ,
volume = 6,
place = {United States},
year = {Tue Apr 21 00:00:00 EDT 2015},
month = {Tue Apr 21 00:00:00 EDT 2015}
}
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https://doi.org/10.1038/ncomms7925
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Enzymatic assembly of DNA molecules up to several hundred kilobases
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Conjugative DNA transfer into human cells by the VirB/VirD4 type IV secretion system of the bacterial pathogen Bartonella henselae
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journal, February 2009

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journal, October 2006

Inactivation of Phaeodactylum tricornutum urease gene using transcription activator-like effector nuclease-based targeted mutagenesis
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Repetitive DNA is associated with centromeric domains in Trypanosoma brucei but not Trypanosoma cruzi
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Highly Efficient Transformation of the Diatom Phaeodactylum tricornutum by Multi-Pulse Electroporation
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  • Miyahara, Mado; Aoi, Masaki; Inoue-Kashino, Natsuko
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Centromere Plasmid: A New Genetic Tool for the Study of Plasmodium falciparum
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    • Apollo - University of Cambridge Repository
    • DOI: 10.17863/cam.11327

    Trans-Kingdom Conjugation within Solid Media from Escherichia coli to Saccharomyces cerevisiae
    journal, October 2019

    • Soltysiak, Maximillian P. M.; Meaney, Rebecca S.; Hamadache, Samir
    • International Journal of Molecular Sciences, Vol. 20, Issue 20
    • DOI: 10.3390/ijms20205212

    Blasticidin-S deaminase, a new selection marker for genetic transformation of the diatom Phaeodactylum tricornutum
    journal, January 2018

    • Buck, Jochen M.; Río Bártulos, Carolina; Gruber, Ansgar
    • PeerJ, Vol. 6
    • DOI: 10.7717/peerj.5884

    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

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

    • Faktorová, Drahomíra; Nisbet, Ellen; Fernández Robledo, José A.
    • Apollo - University of Cambridge Repository
    • DOI: 10.17863/cam.53013

    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

    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

    Non-model model organisms
    text, January 2021

    Efficient inter-species conjugative transfer of a CRISPR nuclease for targeted bacterial killing
    journal, October 2019

    • Hamilton, Thomas A.; Pellegrino, Gregory M.; Therrien, Jasmine A.
    • Nature Communications, Vol. 10, Issue 1
    • DOI: 10.1038/s41467-019-12448-3

    A novel endogenous selection marker for the diatom Phaeodactylum tricornutum based on a unique mutation in phytoene desaturase 1
    journal, June 2019

    Characterization of marine diatom-infecting virus promoters in the model diatom Phaeodactylum tricornutum
    journal, December 2015

    • Kadono, Takashi; Miyagawa-Yamaguchi, Arisa; Kira, Nozomu
    • Scientific Reports, Vol. 5, Issue 1
    • DOI: 10.1038/srep18708

    Multisignal control of expression of the LHCX protein family in the marine diatomPhaeodactylum tricornutum
    journal, May 2016

    • Taddei, Lucilla; Stella, Giulio Rocco; Rogato, Alessandra
    • Journal of Experimental Botany, Vol. 67, Issue 13
    • DOI: 10.1093/jxb/erw198

    Universal loop assembly: open, efficient and cross-kingdom DNA fabrication
    journal, January 2020

    • Pollak, Bernardo; Matute, Tamara; Nuñez, Isaac
    • Synthetic Biology, Vol. 5, Issue 1
    • DOI: 10.1093/synbio/ysaa001

    High-yield secretion of recombinant proteins from the microalga Chlamydomonas reinhardtii
    journal, April 2017

    • Ramos-Martinez, Erick Miguel; Fimognari, Lorenzo; Sakuragi, Yumiko
    • Plant Biotechnology Journal, Vol. 15, Issue 9
    • DOI: 10.1111/pbi.12710

    Genome and methylome of the oleaginous diatom Cyclotella cryptica reveal genetic flexibility toward a high lipid phenotype
    journal, November 2016

    • Traller, Jesse C.; Cokus, Shawn J.; Lopez, David A.
    • Biotechnology for Biofuels, Vol. 9, Issue 1
    • DOI: 10.1186/s13068-016-0670-3

    Current status and perspectives of genome editing technology for microalgae
    journal, November 2017

    Designer Sinorhizobium meliloti strains and multi-functional vectors enable direct inter-kingdom DNA transfer
    journal, June 2019

    Non-model model organisms
    text, January 2021

    Refinement of the Diatom Episome Maintenance Sequence and Improvement of Conjugation-Based DNA Delivery Methods
    journal, August 2016

    • Diner, Rachel E.; Bielinski, Vincent A.; Dupont, Christopher L.
    • Frontiers in Bioengineering and Biotechnology, Vol. 4
    • DOI: 10.3389/fbioe.2016.00065

    Genetic Manipulation of Competition for Nitrate between Heterotrophic Bacteria and Diatoms
    journal, June 2016

    Engineering Strategies to Decode and Enhance the Genomes of Coral Symbionts
    journal, June 2017

    • Levin, Rachel A.; Voolstra, Christian R.; Agrawal, Shobhit
    • Frontiers in Microbiology, Vol. 8
    • DOI: 10.3389/fmicb.2017.01220

    Transgene Expression in Microalgae—From Tools to Applications
    journal, April 2016

    Trans-Kingdom Conjugation within Solid Media from Escherichia coli to Saccharomyces cerevisiae
    journal, October 2019

    • Soltysiak, Maximillian P. M.; Meaney, Rebecca S.; Hamadache, Samir
    • International Journal of Molecular Sciences, Vol. 20, Issue 20
    • DOI: 10.3390/ijms20205212

    Algal Cell Factories: Approaches, Applications, and Potentials
    journal, December 2016

    • Fu, Weiqi; Chaiboonchoe, Amphun; Khraiwesh, Basel
    • Marine Drugs, Vol. 14, Issue 12
    • DOI: 10.3390/md14120225
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