Was the Last Bacterial Common Ancestor a Monoderm after All?

Raphaël R Léonard,Damien Sirjacobs,Paulette Charlier,Valérian Lupo,Amandine Perrin,Denis Baurain,Frédéric Kerff,Eric Sauvage

doi:10.3390/genes13020376

Raphaël R Léonard, Damien Sirjacobs + Show 6 more

Open Access

https://doi.org/10.3390/genes13020376

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Abstract

The very nature of the last bacterial common ancestor (LBCA), in particular the characteristics of its cell wall, is a critical issue to understand the evolution of life on earth. Although knowledge of the relationships between bacterial phyla has made progress with the advent of phylogenomics, many questions remain, including on the appearance or disappearance of the outer membrane of diderm bacteria (also called Gram-negative bacteria). The phylogenetic transition between monoderm (Gram-positive bacteria) and diderm bacteria, and the associated peptidoglycan expansion or reduction, requires clarification. Herein, using a phylogenomic tree of cultivated and characterized bacteria as an evolutionary framework and a literature review of their cell-wall characteristics, we used Bayesian ancestral state reconstruction to infer the cell-wall architecture of the LBCA. With the same phylogenomic tree, we further revisited the evolution of the division and cell-wall synthesis (dcw) gene cluster using homology- and model-based methods. Finally, extensive similarity searches were carried out to determine the phylogenetic distribution of the genes involved with the biosynthesis of the outer membrane in diderm bacteria. Quite unexpectedly, our analyses suggest that all cultivated and characterized bacteria might have evolved from a common ancestor with a monoderm cell-wall architecture. If true, this would indicate that the appearance of the outer membrane was not a unique event and that selective forces have led to the repeated adoption of such an architecture. Due to the lack of phenotypic information, our methodology cannot be applied to all extant bacteria. Consequently, our conclusion might change once enough information is made available to allow the use of an even more diverse organism selection.

Highlights

Introduction iationsCell-wall architecture has always been an important morphological character for bacterial classification [1]
With the growing availability of fully sequenced genomes, phylogenomics has developed as a discipline using the tools of phylogenetics but applied to tens to hundreds, or even thousands, sequences of broadly conserved genes [55]
Phylogenomic trees can either be inferred from supermatrices of concatenated genes [56] or through combination of single-gene trees into supertrees [57]

Summary

Introduction

Cell-wall architecture has always been an important morphological character for bacterial classification [1]. Two main types of cell wall exist: the monoderm and the diderm architectures. While monoderm bacteria are generally surrounded by a thick peptidoglycan (and are positive to Gram coloration), in diderm bacteria, a thin peptidoglycan layer is sandwiched between the cytoplasmic membrane and the outer membrane (and are negative to Gram coloration) [2,3]. Cell-wall features are insufficient to yield a classification that would correlate with phylogenetic trees based on molecular data [4]. Distantly related phyla may have apparently identical cell walls (e.g., Negativicutes and Proteobacteria), whereas closely related phyla or families may present variations in their peptidoglycan thickness or composition, and even in the number of surrounding membranes (e.g., Negativicutes and Halanaerobiales compared to other Firmicutes) [5].

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