An updated phylogeny of the Alphaproteobacteria reveals that the parasitic Rickettsiales and Holosporales have independent origins

Abstract

The Alphaproteobacteria is an extraordinarily diverse and ancient group of bacteria. Previous attempts to infer its deep phylogeny have been plagued with methodological artefacts. To overcome this, we analyzed a dataset of 200 single-copy and conserved genes and employed diverse strategies to reduce compositional artefacts. Such strategies include using novel dataset-specific profile mixture models and recoding schemes, and removing sites, genes and taxa that are compositionally biased. We show that the Rickettsiales and Holosporales (both groups of intracellular parasites of eukaryotes) are not sisters to each other, but instead, the Holosporales has a derived position within the Rhodospirillales. A synthesis of our results also leads to an updated proposal for the higher-level taxonomy of the Alphaproteobacteria. Our robust consensus phylogeny will serve as a framework for future studies that aim to place mitochondria, and novel environmental diversity, within the Alphaproteobacteria.

Data availability

The genome of 'Candidatus Finniella inopinata', endosymbiont of Peranema trichophorum strain CCAP 1260/1B and endosymbiont of Stachyamoeba lipophora strain ATCC 50324 were deposited in NCBI GenBank under the BioProject PRJNA501864. Raw sequencing reads were deposited on the NCBI SRA archive under the BioProject PRJNA501864. Multi-gene datasets as well as phylogenetic trees inferred in this study were deposited at Mendeley Data under the DOI: http://dx.doi.org/10.17632/75m68dxd83.1.

The following data sets were generated

Article and author information

Author details

  1. Sergio A Muñoz-Gómez

    Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Canada
    Competing interests
    The authors declare that no competing interests exist.
  2. Sebastian Hess

    Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Gertraud Burger

    Department of Biochemistry, Université de Montréal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. B Franz Lang

    Department of Biochemistry, Université de Montréal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Edward Susko

    Centre for Comparative Genomics and Evolutionary Bioinformatics, Dalhousie University, Halifax, Canada
    Competing interests
    The authors declare that no competing interests exist.
  6. Claudio H Slamovits

    Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Canada
    Competing interests
    The authors declare that no competing interests exist.
  7. Andrew J Roger

    Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Canada
    For correspondence
    Andrew.Roger@Dal.Ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1370-9820

Funding

Natural Sciences and Engineering Research Council of Canada

  • Gertraud Burger
  • B Franz Lang
  • Claudio H Slamovits
  • Andrew J Roger

Killam Trusts

  • Sergio A Muñoz-Gómez

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

Copyright

© 2019, Muñoz-Gómez 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

  • 9,160
    views
  • 814
    downloads
  • 93
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. Sergio A Muñoz-Gómez
  2. Sebastian Hess
  3. Gertraud Burger
  4. B Franz Lang
  5. Edward Susko
  6. Claudio H Slamovits
  7. Andrew J Roger
(2019)
An updated phylogeny of the Alphaproteobacteria reveals that the parasitic Rickettsiales and Holosporales have independent origins
eLife 8:e42535.
https://doi.org/10.7554/eLife.42535

Share this article

https://doi.org/10.7554/eLife.42535

Further reading

    1. Ecology
    2. Evolutionary Biology
    Rebecca D Tarvin, Jeffrey L Coleman ... Richard W Fitch
    Research Article

    Understanding the origins of novel, complex phenotypes is a major goal in evolutionary biology. Poison frogs of the family Dendrobatidae have evolved the novel ability to acquire alkaloids from their diet for chemical defense at least three times. However, taxon sampling for alkaloids has been biased towards colorful species, without similar attention paid to inconspicuous ones that are often assumed to be undefended. As a result, our understanding of how chemical defense evolved in this group is incomplete. Here, we provide new data showing that, in contrast to previous studies, species from each undefended poison frog clade have measurable yet low amounts of alkaloids. We confirm that undefended dendrobatids regularly consume mites and ants, which are known sources of alkaloids. Thus, our data suggest that diet is insufficient to explain the defended phenotype. Our data support the existence of a phenotypic intermediate between toxin consumption and sequestration — passive accumulation — that differs from sequestration in that it involves no derived forms of transport and storage mechanisms yet results in low levels of toxin accumulation. We discuss the concept of passive accumulation and its potential role in the origin of chemical defenses in poison frogs and other toxin-sequestering organisms. In light of ideas from pharmacokinetics, we incorporate new and old data from poison frogs into an evolutionary model that could help explain the origins of acquired chemical defenses in animals and provide insight into the molecular processes that govern the fate of ingested toxins.

    1. Computational and Systems Biology
    2. Evolutionary Biology
    Pierre Barrat-Charlaix, Richard A Neher
    Research Article

    As pathogens spread in a population of hosts, immunity is built up, and the pool of susceptible individuals are depleted. This generates selective pressure, to which many human RNA viruses, such as influenza virus or SARS-CoV-2, respond with rapid antigenic evolution and frequent emergence of immune evasive variants. However, the host’s immune systems adapt, and older immune responses wane, such that escape variants only enjoy a growth advantage for a limited time. If variant growth dynamics and reshaping of host-immunity operate on comparable time scales, viral adaptation is determined by eco-evolutionary interactions that are not captured by models of rapid evolution in a fixed environment. Here, we use a Susceptible/Infected model to describe the interaction between an evolving viral population in a dynamic but immunologically diverse host population. We show that depending on strain cross-immunity, heterogeneity of the host population, and durability of immune responses, escape variants initially grow exponentially, but lose their growth advantage before reaching high frequencies. Their subsequent dynamics follows an anomalous random walk determined by future escape variants and results in variant trajectories that are unpredictable. This model can explain the apparent contradiction between the clearly adaptive nature of antigenic evolution and the quasi-neutral dynamics of high-frequency variants observed for influenza viruses.