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Title: Finding a partner in the ocean: molecular and evolutionary bases of the response to sexual cues in a planktonic diatom

Abstract

Microalgae play a major role as primary producers in aquatic ecosystems. Cell signalling regulates their interactions with the environment and other organisms, yet this process in phytoplankton is poorly defined. Using the marine planktonic diatom Pseudo-nitzschia multistriata, we investigated the cell response to cues released during sexual reproduction, an event that demands strong regulatory mechanisms and impacts on population dynamics. We sequenced the genome of P. multistriata and performed phylogenomic and transcriptomic analyses, which allowed the definition of gene gains and losses, horizontal gene transfers, conservation and evolutionary rate of sex-related genes. We also identified a small number of conserved noncoding elements. Sexual reproduction impacted on cell cycle progression and induced an asymmetric response of the opposite mating types. G protein-coupled receptors and cyclic guanosine monophosphate (cGMP) are implicated in the response to sexual cues, which overall entails a modulation of cell cycle, meiosis-related and nutrient transporter genes, suggesting a fine control of nutrient uptake even under nutrient-replete conditions. The controllable life cycle and the genome sequence of P. multistriata allow the reconstruction of changes occurring in diatoms in a key phase of their life cycle, providing hints on the evolution and putative function of their genes and empowering studiesmore » on sexual reproduction« less

Authors:
 [1];  [1];  [2];  [1];  [1];  [1];  [3];  [1];  [4];  [2];  [1];  [5];  [1]
  1. Integrative Marine Ecology, Stazione Zoologica Anton Dohrn, Villa Comunale 1 Naples 80121 Italy
  2. Earlham Institute, Norwich Research Park, Norwich NR4 7UG UK
  3. URGI, INRA, Université Paris-Saclay, 78026 Versailles France
  4. School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ UK
  5. Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn, Villa Comunale 1 Naples 80121 Italy
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1625916
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
New Phytologist
Additional Journal Information:
Journal Volume: 215; Journal Issue: 1; Journal ID: ISSN 0028-646X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
Plant Sciences; algae; diatom; genomics; matingtype; phytoplankton,Pseudo-nitzschia multistriata; sexual reproduction; signal transduction

Citation Formats

Basu, Swaraj, Patil, Shrikant, Mapleson, Daniel, Russo, Monia Teresa, Vitale, Laura, Fevola, Cristina, Maumus, Florian, Casotti, Raffaella, Mock, Thomas, Caccamo, Mario, Montresor, Marina, Sanges, Remo, and Ferrante, Maria Immacolata. Finding a partner in the ocean: molecular and evolutionary bases of the response to sexual cues in a planktonic diatom. United States: N. p., 2017. Web. doi:10.1111/nph.14557.
Basu, Swaraj, Patil, Shrikant, Mapleson, Daniel, Russo, Monia Teresa, Vitale, Laura, Fevola, Cristina, Maumus, Florian, Casotti, Raffaella, Mock, Thomas, Caccamo, Mario, Montresor, Marina, Sanges, Remo, & Ferrante, Maria Immacolata. Finding a partner in the ocean: molecular and evolutionary bases of the response to sexual cues in a planktonic diatom. United States. https://doi.org/10.1111/nph.14557
Basu, Swaraj, Patil, Shrikant, Mapleson, Daniel, Russo, Monia Teresa, Vitale, Laura, Fevola, Cristina, Maumus, Florian, Casotti, Raffaella, Mock, Thomas, Caccamo, Mario, Montresor, Marina, Sanges, Remo, and Ferrante, Maria Immacolata. Fri . "Finding a partner in the ocean: molecular and evolutionary bases of the response to sexual cues in a planktonic diatom". United States. https://doi.org/10.1111/nph.14557. https://www.osti.gov/servlets/purl/1625916.
@article{osti_1625916,
title = {Finding a partner in the ocean: molecular and evolutionary bases of the response to sexual cues in a planktonic diatom},
author = {Basu, Swaraj and Patil, Shrikant and Mapleson, Daniel and Russo, Monia Teresa and Vitale, Laura and Fevola, Cristina and Maumus, Florian and Casotti, Raffaella and Mock, Thomas and Caccamo, Mario and Montresor, Marina and Sanges, Remo and Ferrante, Maria Immacolata},
abstractNote = {Microalgae play a major role as primary producers in aquatic ecosystems. Cell signalling regulates their interactions with the environment and other organisms, yet this process in phytoplankton is poorly defined. Using the marine planktonic diatom Pseudo-nitzschia multistriata, we investigated the cell response to cues released during sexual reproduction, an event that demands strong regulatory mechanisms and impacts on population dynamics. We sequenced the genome of P. multistriata and performed phylogenomic and transcriptomic analyses, which allowed the definition of gene gains and losses, horizontal gene transfers, conservation and evolutionary rate of sex-related genes. We also identified a small number of conserved noncoding elements. Sexual reproduction impacted on cell cycle progression and induced an asymmetric response of the opposite mating types. G protein-coupled receptors and cyclic guanosine monophosphate (cGMP) are implicated in the response to sexual cues, which overall entails a modulation of cell cycle, meiosis-related and nutrient transporter genes, suggesting a fine control of nutrient uptake even under nutrient-replete conditions. The controllable life cycle and the genome sequence of P. multistriata allow the reconstruction of changes occurring in diatoms in a key phase of their life cycle, providing hints on the evolution and putative function of their genes and empowering studies on sexual reproduction},
doi = {10.1111/nph.14557},
journal = {New Phytologist},
number = 1,
volume = 215,
place = {United States},
year = {Fri Apr 21 00:00:00 EDT 2017},
month = {Fri Apr 21 00:00:00 EDT 2017}
}

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Highly conserved elements discovered in vertebrates are present in non-syntenic loci of tunicates, act as enhancers and can be transcribed during development
journal, February 2013

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journal, November 2013

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journal, November 2000


Aligning Multiple Genomic Sequences With the Threaded Blockset Aligner
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Oil Accumulation by the Oleaginous Diatom Fistulifera solaris as Revealed by the Genome and Transcriptome
journal, January 2015

  • Tanaka, Tsuyoshi; Maeda, Yoshiaki; Veluchamy, Alaguraj
  • The Plant Cell, Vol. 27, Issue 1
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The dynamics of sexual phase in the marine diatom Pseudo-nitzschia multistriata (Bacillariophyceae)
journal, September 2014

  • Scalco, Eleonora; Stec, Krzysztof; Iudicone, Daniele
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Pheromone signaling during sexual reproduction in algae
journal, May 2014

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Sex in marine planktonic diatoms: insights and challenges [Sex in marine planktonic diatoms: insights and challenges]
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Potential impact of stress activated retrotransposons on genome evolution in a marine diatom
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Identification of G protein-coupled receptor signaling pathway proteins in marine diatoms using comparative genomics
journal, January 2013


The origin and early evolution of eukaryotes in the light of phylogenomics
journal, January 2010


Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire
journal, January 2010


Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation
journal, January 2012


Highly Conserved Non-Coding Sequences Are Associated with Vertebrate Development
journal, November 2004


Combined Evidence Annotation of Transposable Elements in Genome Sequences
journal, January 2005


Considering Transposable Element Diversification in De Novo Annotation Approaches
journal, January 2011


Novel Sex Cells and Evidence for Sex Pheromones in Diatoms
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Evolution of reproductive proteins from animals and plants
journal, January 2006

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  • Brunson, John K.; McKinnie, Shaun M. K.; Chekan, Jonathan R.
  • Science, Vol. 361, Issue 6409
  • DOI: 10.1126/science.aau0382

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


Collective sinking promotes selective cell pairing in planktonic pennate diatoms
journal, July 2019

  • Font-Muñoz, Joan S.; Jeanneret, Raphaël; Arrieta, Jorge
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 32
  • DOI: 10.1073/pnas.1904837116

Decision-making of the benthic diatom Seminavis robusta searching for inorganic nutrients and pheromones
journal, October 2018

  • Bondoc, Karen Grace V.; Lembke, Christine; Lang, Stefan N.
  • The ISME Journal, Vol. 13, Issue 2
  • DOI: 10.1038/s41396-018-0299-2

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


Accelerated diversification is related to life history and locomotion in a hyperdiverse lineage of microbial eukaryotes (Diatoms, Bacillariophyta)
journal, April 2018

  • Nakov, Teofil; Beaulieu, Jeremy M.; Alverson, Andrew J.
  • New Phytologist, Vol. 219, Issue 1
  • DOI: 10.1111/nph.15137

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

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


Grazer-induced transcriptomic and metabolomic response of the chain-forming diatom Skeletonema marinoi
journal, March 2018


Paleolimnology and resurrection ecology: The future of reconstructing the past
journal, December 2017

  • Burge, David R. L.; Edlund, Mark B.; Frisch, Dagmar
  • Evolutionary Applications, Vol. 11, Issue 1
  • DOI: 10.1111/eva.12556

Divergent gene expression among phytoplankton taxa in response to upwelling: Divergent phytoplankton responses to upwelling
journal, August 2018

  • Lampe, Robert H.; Cohen, Natalie R.; Ellis, Kelsey A.
  • Environmental Microbiology, Vol. 20, Issue 8
  • DOI: 10.1111/1462-2920.14361

Transcriptomic responses to grazing reveal the metabolic pathway leading to the biosynthesis of domoic acid and highlight different defense strategies in diatoms
journal, February 2019

  • Harðardóttir, Sara; Wohlrab, Sylke; Hjort, Ditte Marie
  • BMC Molecular Biology, Vol. 20, Issue 1
  • DOI: 10.1186/s12867-019-0124-0

Clonal expansion behind a marine diatom bloom
journal, November 2017

  • Ruggiero, Maria Valeria; D'Alelio, Domenico; Ferrante, Maria Immacolata
  • The ISME Journal, Vol. 12, Issue 2
  • DOI: 10.1038/ismej.2017.181

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

Genome editing in diatoms: achievements and goals
journal, August 2018


De novo transcriptome of the cosmopolitan dinoflagellate Amphidinium carterae to identify enzymes with biotechnological potential
journal, September 2017


Divergent gene expression among phytoplankton taxa in response to upwelling
posted_content, June 2018

  • Lampe, Robert H.; Cohen, Natalie R.; Ellis, Kelsey A.
  • DOI: 10.1101/286138

Time series and beyond: multifaceted plankton research at a marine Mediterranean LTER site
journal, May 2019


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

Chemical ecology of the marine plankton
journal, January 2013

  • Roy, Jessie S.; Poulson-Ellestad, Kelsey L.; Drew Sieg, R.
  • Natural Product Reports, Vol. 30, Issue 11
  • DOI: 10.1039/c3np70056a

Decision-making of the benthic diatom Seminavis robusta searching for inorganic nutrients and pheromones
journal, October 2018

  • Bondoc, Karen Grace V.; Lembke, Christine; Lang, Stefan N.
  • The ISME Journal, Vol. 13, Issue 2
  • DOI: 10.1038/s41396-018-0299-2

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


De novo transcriptome of the cosmopolitan dinoflagellate Amphidinium carterae to identify enzymes with biotechnological potential
journal, September 2017


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


Divergent gene expression among phytoplankton taxa in response to upwelling
posted_content, June 2018

  • Lampe, Robert H.; Cohen, Natalie R.; Ellis, Kelsey A.
  • DOI: 10.1101/286138

A single loss of photosynthesis in diatoms
posted_content, April 2018

  • Onyshchenko, Anastasiia; Ruck, Elizabeth C.; Nakov, Teofil
  • DOI: 10.1101/298810

Diatom Molecular Research Comes of Age: Model Species for Studying Phytoplankton Biology and Diversity
journal, December 2019

  • Falciatore, Angela; Jaubert, Marianne; Bouly, Jean-Pierre
  • The Plant Cell, Vol. 32, Issue 3
  • DOI: 10.1105/tpc.19.00158

Paleolimnology and resurrection ecology: The future of reconstructing the past
journal, December 2017

  • Burge, David R. L.; Edlund, Mark B.; Frisch, Dagmar
  • Evolutionary Applications, Vol. 11, Issue 1
  • DOI: 10.1111/eva.12556

Accelerated diversification is related to life history and locomotion in a hyperdiverse lineage of microbial eukaryotes (Diatoms, Bacillariophyta)
journal, April 2018

  • Nakov, Teofil; Beaulieu, Jeremy M.; Alverson, Andrew J.
  • New Phytologist, Vol. 219, Issue 1
  • DOI: 10.1111/nph.15137

Transcriptomic responses to grazing reveal the metabolic pathway leading to the biosynthesis of domoic acid and highlight different defense strategies in diatoms
journal, February 2019

  • Harðardóttir, Sara; Wohlrab, Sylke; Hjort, Ditte Marie
  • BMC Molecular Biology, Vol. 20, Issue 1
  • DOI: 10.1186/s12867-019-0124-0

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