Support for a clade of Placozoa and Cnidaria in genes with minimal compositional bias

  1. Christopher E Laumer  Is a corresponding author
  2. Harald Gruber-Vodicka
  3. Michael G Hadfield
  4. Vicki B Pearse
  5. Ana Riesgo
  6. John C Marioni
  7. Gonzalo Giribet
  1. Wellcome Trust Sanger Institute, United Kingdom
  2. Max Planck Institute for Marine Microbiology, Germany
  3. University of Hawaii at Manoa, United States
  4. University of California, Santa Cruz, United States
  5. The Natural History Museum, United Kingdom
  6. Harvard University, United States

Abstract

The phylogenetic placement of the morphologically simple placozoans is crucial to understanding the evolution of complex animal traits. Here, we examine the influence of adding new genomes from placozoans to a large dataset designed to study the deepest splits in the animal phylogeny. Using site-heterogeneous substitution models, we show that it is possible to obtain strong support, in both amino acid and reduced-alphabet matrices, for either a sister-group relationship between Cnidaria and Placozoa, or for Cnidaria and Bilateria as seen in most published work to date, depending on the orthologues selected to construct the matrix. We demonstrate that a majority of genes show evidence of compositional heterogeneity, and that support for the Cnidaria+Bilateria clade can be assigned to this source of systematic error. In interpreting these results, we caution against a peremptory reading of placozoans as secondarily reduced forms of little relevance to broader discussions of early animal evolution.

Data availability

SRA accession codes, where used, and all alternative sources for sequence data (e.g. individually hosted websites, personal communications), are listed above in the Materials and Methods section. A DataDryad accession is available at https://doi.org/10.5061/dryad.6cm1166, which makes available all helper scripts, orthogroups, multiple sequence alignments, phylogenetic program output, and raw host proteomes inputted to OrthoFinder. Metagenomic bins containing placozoan host contigs and raw RNA reads used to derive gene annotations from H4, H6 and H11 isolates are also provided in this accession. PhyloBayes .chain files, due to their large size, are separately accessioned at in Zenodo at https://doi.org/10.5281/zenodo.1197272.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Christopher E Laumer

    Wellcome Trust Sanger Institute, Hinxton, United Kingdom
    For correspondence
    claumer@ebi.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8097-8516
  2. Harald Gruber-Vodicka

    Max Planck Institute for Marine Microbiology, Bremen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Michael G Hadfield

    Kewalo Marine Laboratory, Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Vicki B Pearse

    Institute of Marine Sciences, University of California, Santa Cruz, Santa Cruz, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Ana Riesgo

    Life Sciences, Invertebrate Division, The Natural History Museum, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. John C Marioni

    Wellcome Trust Sanger Institute, Hinxton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9092-0852
  7. Gonzalo Giribet

    Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

Max-Planck-Institute fuer Marine Microbiologie

  • Harald Gruber-Vodicka

EMBL-European Bioinformatics Institute

  • John C Marioni

Harvard University Faculty of Arts and Sciences

  • Gonzalo Giribet

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

Reviewing Editor

  1. Antonis Rokas, Vanderbilt University, United States

Version history

  1. Received: February 27, 2018
  2. Accepted: October 11, 2018
  3. Accepted Manuscript published: October 30, 2018 (version 1)
  4. Version of Record published: December 3, 2018 (version 2)

Copyright

© 2018, Laumer 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.

Metrics

  • 4,977
    Page views
  • 701
    Downloads
  • 65
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Christopher E Laumer
  2. Harald Gruber-Vodicka
  3. Michael G Hadfield
  4. Vicki B Pearse
  5. Ana Riesgo
  6. John C Marioni
  7. Gonzalo Giribet
(2018)
Support for a clade of Placozoa and Cnidaria in genes with minimal compositional bias
eLife 7:e36278.
https://doi.org/10.7554/eLife.36278

Share this article

https://doi.org/10.7554/eLife.36278

Further reading

    1. Evolutionary Biology
    Jordan Little, Maria Chikina, Nathan L Clark
    Research Article

    Co-functional proteins tend to have rates of evolution that covary over time. This correlation between evolutionary rates can be measured over the branches of a phylogenetic tree through methods such as evolutionary rate covariation (ERC), and then used to construct gene networks by the identification of proteins with functional interactions. The cause of this correlation has been hypothesized to result from both compensatory coevolution at physical interfaces and nonphysical forces such as shared changes in selective pressure. This study explores whether coevolution due to compensatory mutations has a measurable effect on the ERC signal. We examined the difference in ERC signal between physically interacting protein domains within complexes compared to domains of the same proteins that do not physically interact. We found no generalizable relationship between physical interaction and high ERC, although a few complexes ranked physical interactions higher than nonphysical interactions. Therefore, we conclude that coevolution due to physical interaction is weak, but present in the signal captured by ERC, and we hypothesize that the stronger signal instead comes from selective pressures on the protein as a whole and maintenance of the general function.

    1. Computational and Systems Biology
    2. Evolutionary Biology
    Roee Ben Nissan, Eliya Milshtein ... Ron Milo
    Research Article

    Synthetic autotrophy is a promising avenue to sustainable bioproduction from CO2. Here, we use iterative laboratory evolution to generate several distinct autotrophic strains. Utilising this genetic diversity, we identify that just three mutations are sufficient for Escherichia coli to grow autotrophically, when introduced alongside non-native energy (formate dehydrogenase) and carbon-fixing (RuBisCO, phosphoribulokinase, carbonic anhydrase) modules. The mutated genes are involved in glycolysis (pgi), central-carbon regulation (crp), and RNA transcription (rpoB). The pgi mutation reduces the enzyme’s activity, thereby stabilising the carbon-fixing cycle by capping a major branching flux. For the other two mutations, we observe down-regulation of several metabolic pathways and increased expression of native genes associated with the carbon-fixing module (rpiB) and the energy module (fdoGH), as well as an increased ratio of NADH/NAD+ - the cycle’s electron-donor. This study demonstrates the malleability of metabolism and its capacity to switch trophic modes using only a small number of genetic changes and could facilitate transforming other heterotrophic organisms into autotrophs.