Phylogenomics: Leaving negative ancestors behind

  1. Sergio A Muñoz-Gómez  Is a corresponding author
  2. Andrew J Roger  Is a corresponding author
  1. Dalhousie University, Canada

For more than a century bacteriologists have used the Gram stain reaction to classify bacteria. The Gram stain is a violet-colored dye that is retained by Gram-positive bacteria but not by Gram-negative bacteria. These different reactions to the stain reflect fundamental differences in the cell envelopes of these bacteria: Gram-positive bacteria usually have a single cell membrane that is encased by a thick wall made of a polymer called peptidoglycan, whereas Gram-negative bacteria tend to have two membranes with a thin wall of peptidoglycan sandwiched between them.

The tree of life contains about 30 bacterial phyla, but only three of them contain bacteria that are surrounded by a single cell membrane, which are also known as “monoderms”. The remaining phyla contain bacteria with two cell membranes, and most of these “diderms” have large molecules called lipopolysaccharides (LPS) in their outer membranes. However, at least two phyla comprise diderms that do not have LPS.

The evolutionary relationships between monoderms and diderms have remained uncertain for many years. It is generally thought that the monodermic cell plan evolved from the more complex didermic cell plan in a single simplification event (see, for example, Cavalier-Smith, 2006). However, it is possible that diderms could have evolved from monoderms (Dawes, 1981; Tocheva, 2011). Now, in eLife, Simonetta Gribaldo of the Institut Pasteur and co-workers – including Luísa Antunes and Daniel Poppleton as joint first authors – report that monodermic bacteria evolved from ancestral didermic bacteria not once but multiple times by losing the outer membrane from their cell envelopes (Antunes et al., 2016).

Antunes et al. focused on the Firmicutes, a phylum that contains a mixture of monoderms and diderms. By analyzing the genomes of more than 200 members of the phylum, they showed that the two didermic groups – the Negativicutes and the Halanaerobiales – are not each other's closest relatives and are, instead, more closely related to one or more of the monodermic groups. Furthermore, they demonstrate that the biosynthetic machinery for synthesizing their LPS has not been transferred between them nor acquired from elsewhere. Instead, the outer membrane of the didermic firmicutes appears to have been inherited vertically from a distant ancestor. These results suggest that the monodermic firmicutes evolved at least five times from an ancestral and more complex didermic cell plan (Figure 1).

Evolution of the Firmicutes phylum. 

(A) Didermic firmicutes have a cytoplasmic membrane (shown in blue), a peptidoglycan cell wall (gray) and an outer membrane (green), whereas monodermic firmicutes have a cytoplasmic membrane and a peptidoglycan cell wall, but no outer membrane. Antunes et al. show that the ancestral didermic cell plan of the Firmicutes phylum has been lost at least five times. Most lineages lost their outer membranes to become monoderms (thick gray lines), but the Negativicutes and the Halanaerobiales retained the ancestral didermic cell plan (thick green lines). (B) Major transitions between bacterial cell plans within the Firmicutes phylum. Ancestral sporulating diderms (similar to the Negativicutes and the Halanaerobiales) convergently gave rise to classical sporulating monoderms (e.g., Bacillus and Clostridium), which lost the capacity to form endospores in some linages (e.g., Lactobacillus). Endospores are shown as cells within cells.

Comparative analyses of the genomes of Negativicutes and Halanaerobiales also allowed Antunes et al. to make inferences about the nature and evolution of their didermic envelopes. Notably, and unusually, most of the genes required for the biogenesis of the outer membrane clustered in a large genomic region in both groups. Moreover, these two groups have envelope appendages (such as flagella and pili) that resemble the envelope appendages of other diderms (in other phyla) more than they resemble those of their close monodermic relatives. Finally, didermic firmicutes appear to retain ancestral systems for the biogenesis of their outer membranes.

The root of the bacterial tree of life remains a mystery and we do not know whether the last common ancestor of all bacteria was a monoderm or a diderm, and whether it produced endospores or not. It is reasonable to assume that the classical diderms that contain LPS have a single origin (Sutcliffe, 2010; Tocheva et al., 2016; Sutcliffe and Dover, 2016), and that they plausibly evolved via an endospore released by an ancestral monoderm (Dawes, 1981; Vollmer, 2012; Tocheva et al., 2011). And now the work of Antunes et al. suggests that most Firmicutes lineages became secondarily monodermic on multiple occasions. Is the same true for the Actinobacteria and the Chloroflexi, the other two phyla that contain monoderms? It is also noteworthy that the three monodermic phyla tend to cluster in many analyses, and are relatively close to the presumed root of the bacterial tree of life (Raymann et al., 2015; Hug et al., 2016), although resolution remains poor at the deepest phylogenetic levels. A more robust phylogenetic framework for bacteria is needed to make sense of these observations.

To better understand the large-scale evolutionary history of bacteria, we need to answer why, how and when the major structural differences among the prokaryotes (bacteria and archaea) came to be. Antunes et al. have provided some answers to the last question (and also shown that a given major structural change can happen more than once), and planted the seeds to answer the first two questions with regard to the evolution of monodermic bacteria. Future biochemical, ultrastructural and genomic characterization of novel prokaryotic lineages, such as the CPR taxa (short for candidate phyla radiation taxa; Hug et al., 2016), will provide more raw material to reconstruct the phenotypic evolution of prokaryotes. The syntheses of these data, together with a robust phylogenetic tree of the prokaryotes, will no doubt provide new insights into the major changes in cell evolution and help to clarify the nature of the last common ancestor of bacteria.

References

  1. Book
    1. Dawes IW
    (1981)
    Sporulation in evolution
    In: Carlile MJ, Collins JF, Moseley BEB, editors. Cellular and Molecular Aspects of Microbial Evolution. Cambridge: Cambridge University Press. pp. 85–130.

Article and author information

Author details

  1. Sergio A Muñoz-Gómez

    Centre for Comparative Genomics and Evolutionary Bioinformatics, CIFAR Program in Integrated Microbial Biodiversity and the Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Canada
    For correspondence
    sergio.munoz@dal.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6200-474X
  2. Andrew J Roger

    Centre for Comparative Genomics and Evolutionary Bioinformatics, CIFAR Program in Integrated Microbial Biodiversity and the 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.

Publication history

  1. Version of Record published:
  2. Version of Record updated:

Copyright

© 2016, Muñoz-Gómez et al.

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

Metrics

  • 4,118
    views
  • 308
    downloads
  • 2
    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. Andrew J Roger
(2016)
Phylogenomics: Leaving negative ancestors behind
eLife 5:e20061.
https://doi.org/10.7554/eLife.20061
  1. Further reading

Further reading

    1. Cell Biology
    2. Developmental Biology
    Evgenia Leikina, Jarred M Whitlock ... Leonid Chernomordik
    Research Article

    The bone-resorbing activity of osteoclasts plays a critical role in the life-long remodeling of our bones that is perturbed in many bone loss diseases. Multinucleated osteoclasts are formed by the fusion of precursor cells, and larger cells – generated by an increased number of cell fusion events – have higher resorptive activity. We find that osteoclast fusion and bone resorption are promoted by reactive oxygen species (ROS) signaling and by an unconventional low molecular weight species of La protein, located at the osteoclast surface. Here, we develop the hypothesis that La’s unique regulatory role in osteoclast multinucleation and function is controlled by an ROS switch in La trafficking. Using antibodies that recognize reduced or oxidized species of La, we find that differentiating osteoclasts enrich an oxidized species of La at the cell surface, which is distinct from the reduced La species conventionally localized within cell nuclei. ROS signaling triggers the shift from reduced to oxidized La species, its dephosphorylation and delivery to the surface of osteoclasts, where La promotes multinucleation and resorptive activity. Moreover, intracellular ROS signaling in differentiating osteoclasts oxidizes critical cysteine residues in the C-terminal half of La, producing this unconventional La species that promotes osteoclast fusion. Our findings suggest that redox signaling induces changes in the location and function of La and may represent a promising target for novel skeletal therapies.

    1. Cell Biology
    Xiaojiao Hua, Chen Zhao ... Yan Zhou
    Research Article

    The β-catenin-dependent canonical Wnt signaling is pivotal in organ development, tissue homeostasis, and cancer. Here, we identified an upstream enhancer of Ctnnb1 – the coding gene for β-catenin, named ieCtnnb1 (intestinal enhancer of Ctnnb1), which is crucial for intestinal homeostasis. ieCtnnb1 is predominantly active in the base of small intestinal crypts and throughout the epithelia of large intestine. Knockout of ieCtnnb1 led to a reduction in Ctnnb1 transcription, compromising the canonical Wnt signaling in intestinal crypts. Single-cell sequencing revealed that ieCtnnb1 knockout altered epithelial compositions and potentially compromised functions of small intestinal crypts. While deletion of ieCtnnb1 hampered epithelial turnovers in physiologic conditions, it prevented occurrence and progression of Wnt/β-catenin-driven colorectal cancers. Human ieCTNNB1 drove reporter gene expression in a pattern highly similar to mouse ieCtnnb1. ieCTNNB1 contains a single-nucleotide polymorphism associated with CTNNB1 expression levels in human gastrointestinal epithelia. The enhancer activity of ieCTNNB1 in colorectal cancer tissues was stronger than that in adjacent normal tissues. HNF4α and phosphorylated CREB1 were identified as key trans-factors binding to ieCTNNB1 and regulating CTNNB1 transcription. Together, these findings unveil an enhancer-dependent mechanism controlling the dosage of Wnt signaling and homeostasis in intestinal epithelia.