1. Cell Biology
  2. Evolutionary Biology

Phylogenomics: Leaving negative ancestors behind

https://doi.org/10.7554/eLife.20061
  • Download
  • Cite
  • CommentOpen annotations (there are currently 0 annotations on this page).
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS
  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).

Figure 1
Download asset Open asset
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 …

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

  3. 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

  • 4,297
    views
  • 314
    downloads
  • 3
    citations

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

Download links

Categories and tags

    1. Related to

    Phylogenomic analysis supports the ancestral presence of LPS-outer membranes in the Firmicutes

    Luisa CS Antunes, Daniel Poppleton ... Simonetta Gribaldo
  2. Further reading

Further reading

    1. Cell Biology
    2. Evolutionary Biology

    Phylogenomic analysis supports the ancestral presence of LPS-outer membranes in the Firmicutes

    Luisa CS Antunes, Daniel Poppleton ... Simonetta Gribaldo
    Research Article

    One of the major unanswered questions in evolutionary biology is when and how the transition between diderm (two membranes) and monoderm (one membrane) cell envelopes occurred in Bacteria. The Negativicutes and the Halanaerobiales belong to the classically monoderm Firmicutes, but possess outer membranes with lipopolysaccharide (LPS-OM). Here, we show that they form two phylogenetically distinct lineages, each close to different monoderm relatives. In contrast, their core LPS biosynthesis enzymes were inherited vertically, as in the majority of bacterial phyla. Finally, annotation of key OM systems in the Halanaerobiales and the Negativicutes shows a puzzling combination of monoderm and diderm features. Together, these results support the hypothesis that the LPS-OMs of Negativicutes and Halanaerobiales are remnants of an ancient diderm cell envelope that was present in the ancestor of the Firmicutes, and that the monoderm phenotype in this phylum is a derived character that arose multiple times independently through OM loss.

    1. Cancer Biology
    2. Cell Biology

    Changes in local mineral homeostasis facilitate the formation of benign and malignant testicular microcalcifications

    Ida Marie Boisen, Nadia Krarup Knudsen ... Martin Blomberg Jensen
    Research Article

    Testicular microcalcifications consist of hydroxyapatite and have been associated with an increased risk of testicular germ cell tumors (TGCTs) but are also found in benign cases such as loss-of-function variants in the phosphate transporter SLC34A2. Here, we show that fibroblast growth factor 23 (FGF23), a regulator of phosphate homeostasis, is expressed in testicular germ cell neoplasia in situ (GCNIS), embryonal carcinoma (EC), and human embryonic stem cells. FGF23 is not glycosylated in TGCTs and therefore cleaved into a C-terminal fragment which competitively antagonizes full-length FGF23. Here, Fgf23 knockout mice presented with marked calcifications in the epididymis, spermatogenic arrest, and focally germ cells expressing the osteoblast marker Osteocalcin (gene name: Bglap, protein name). Moreover, the frequent testicular microcalcifications in mice with no functional androgen receptor and lack of circulating gonadotropins are associated with lower Slc34a2 and higher Bglap/Slc34a1 (protein name: NPT2a) expression compared with wild-type mice. In accordance, human testicular specimens with microcalcifications also have lower SLC34A2 and a subpopulation of germ cells express phosphate transporter NPT2a, Osteocalcin, and RUNX2 highlighting aberrant local phosphate handling and expression of bone-specific proteins. Mineral disturbance in vitro using calcium or phosphate treatment induced deposition of calcium phosphate in a spermatogonial cell line and this effect was fully rescued by the mineralization inhibitor pyrophosphate. In conclusion, testicular microcalcifications arise secondary to local alterations in mineral homeostasis, which in combination with impaired Sertoli cell function and reduced levels of mineralization inhibitors due to high alkaline phosphatase activity in GCNIS and TGCTs facilitate osteogenic-like differentiation of testicular cells and deposition of hydroxyapatite.

    1. Cell Biology
    2. Genetics and Genomics

    Pyruvate and related energetic metabolites modulate resilience against high genetic risk for glaucoma

    Keva Li, Nicholas Tolman ... UK Biobank Eye and Vision Consortium
    Research Article

    A glaucoma polygenic risk score (PRS) can effectively identify disease risk, but some individuals with high PRS do not develop glaucoma. Factors contributing to this resilience remain unclear. Using 4,658 glaucoma cases and 113,040 controls in a cross-sectional study of the UK Biobank, we investigated whether plasma metabolites enhanced glaucoma prediction and if a metabolomic signature of resilience in high-genetic-risk individuals existed. Logistic regression models incorporating 168 NMR-based metabolites into PRS-based glaucoma assessments were developed, with multiple comparison corrections applied. While metabolites weakly predicted glaucoma (Area Under the Curve = 0.579), they offered marginal prediction improvement in PRS-only-based models (p=0.004). We identified a metabolomic signature associated with resilience in the top glaucoma PRS decile, with elevated glycolysis-related metabolites—lactate (p=8.8E-12), pyruvate (p=1.9E-10), and citrate (p=0.02)—linked to reduced glaucoma prevalence. These metabolites combined significantly modified the PRS-glaucoma relationship (Pinteraction = 0.011). Higher total resilience metabolite levels within the highest PRS quartile corresponded to lower glaucoma prevalence (Odds Ratiohighest vs. lowest total resilience metabolite quartile=0.71, 95% Confidence Interval = 0.64–0.80). As pyruvate is a foundational metabolite linking glycolysis to tricarboxylic acid cycle metabolism and ATP generation, we pursued experimental validation for this putative resilience biomarker in a human-relevant Mus musculus glaucoma model. Dietary pyruvate mitigated elevated intraocular pressure (p=0.002) and optic nerve damage (p<0.0003) in Lmx1bV265D mice. These findings highlight the protective role of pyruvate-related metabolism against glaucoma and suggest potential avenues for therapeutic intervention.