The genomes of polyextremophilic Cyanidiales contain 1% horizontally transferred genes with diverse adaptive functions

  1. Alessandro W Rossoni
  2. Dana C Price
  3. Mark Seger
  4. Dagmar Lyska
  5. Peter Lammers
  6. Debashish Bhattacharya
  7. Andreas P M Weber  Is a corresponding author
  1. Heinrich Heine University, Germany
  2. Rutgers University, United States
  3. Arizona State University, United States

Abstract

The role and extent of horizontal gene transfer (HGT) in eukaryotes are hotly disputed topics that impact our understanding of the origin of metabolic processes and the role of organelles in cellular evolution. We addressed this issue by analyzing 10 novel Cyanidiales genomes and determined that 1% of their gene inventory is HGT-derived. Numerous HGT candidates share a close phylogenetic relationship with prokaryotes that live in similar habitats as the Cyanidiales and encode functions related to polyextremophily. HGT candidates differ from native genes in GC-content, number of splice sites, and gene expression. HGT candidates are more prone to loss, which may explain the absence of a eukaryotic pan-genome. Therefore, the lack of a pan-genome and cumulative effects fail to provide substantive arguments against our hypothesis of recurring HGT followed by differential loss in eukaryotes. The maintenance of 1% HGTs, even under selection for genome reduction, underlines the importance of non-endosymbiosis related foreign gene acquisition.

Data availability

The genomic, chloroplast and mitochondrial sequences of the 10 novel genomes, as well as gene models, ESTs, protein sequences, and gene annotations are available at http://porphyra.rutgers.edu.Raw PacBio RSII reads, and also the genomic, chloroplast and mitochondrial sequences, have been submitted to the NCBI and are retrievable via BioProject ID PRJNA512382.

The following data sets were generated

Article and author information

Author details

  1. Alessandro W Rossoni

    Institute of Plant Biochemistry, Heinrich Heine University, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Dana C Price

    Department of Plant Biology, Rutgers University, New Brunswick, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Mark Seger

    Arizona Center for Algae Technology and Innovation, Arizona State University, Mesa, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Dagmar Lyska

    Institute of Plant Biochemistry, Heinrich Heine University, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Peter Lammers

    Arizona Center for Algae Technology and Innovation, Arizona State University, Mesa, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Debashish Bhattacharya

    Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Andreas P M Weber

    Institute of Plant Biochemistry, Heinrich Heine University, Düsseldorf, Germany
    For correspondence
    andreas.weber@uni-duesseldorf.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0970-4672

Funding

Deutsche Forschungsgemeinschaft (EXC 1028)

  • Andreas P M Weber

Heinrich-Heine-Universität Düsseldorf

  • Andreas P M Weber

Deutsche Forschungsgemeinschaft (WE 2231/21-1)

  • Andreas P M Weber

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Paul B Rainey, Max Planck Institute for Evolutionary Biology, Germany

Publication history

  1. Received: January 10, 2019
  2. Accepted: May 30, 2019
  3. Accepted Manuscript published: May 31, 2019 (version 1)
  4. Version of Record published: July 15, 2019 (version 2)

Copyright

© 2019, Rossoni et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Alessandro W Rossoni
  2. Dana C Price
  3. Mark Seger
  4. Dagmar Lyska
  5. Peter Lammers
  6. Debashish Bhattacharya
  7. Andreas P M Weber
(2019)
The genomes of polyextremophilic Cyanidiales contain 1% horizontally transferred genes with diverse adaptive functions
eLife 8:e45017.
https://doi.org/10.7554/eLife.45017
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