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Ancient origin and constrained evolution of the division and cell wall gene cluster in Bacteria

Nature Microbiology volume 7, pages 2114–2127 (2022)Cite this article

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Abstract

The division and cell wall (dcw) gene cluster in Bacteria comprises 17 genes encoding key steps in peptidoglycan synthesis and cytokinesis. To understand the origin and evolution of this cluster, we analysed its presence in over 1,000 bacterial genomes. We show that the dcw gene cluster is strikingly conserved in both gene content and gene order across all Bacteria and has undergone only a few rearrangements in some phyla, potentially linked to cell envelope specificities, but not directly to cell shape. A large concatenation of the 12 most conserved dcw cluster genes produced a robust tree of Bacteria that is largely consistent with recent phylogenies based on frequently used markers. Moreover, evolutionary divergence analyses show that the dcw gene cluster offers advantages in defining high-rank taxonomic boundaries and indicate at least two main phyla in the Candidate Phyla Radiation (CPR) matching a sharp dichotomy in dcw gene cluster arrangement. Our results place the origin of the dcw gene cluster in the Last Bacterial Common Ancestor and show that it has evolved vertically for billions of years, similar to major cellular machineries such as the ribosome. The strong phylogenetic signal, combined with conserved genomic synteny at large evolutionary distances, makes the dcw gene cluster a robust alternative set of markers to resolve the ever-growing tree of Bacteria.

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Fig. 1: Proteins involved in PG synthesis and cell division and the dcw genomic locus.
Fig. 2: Conservation of the dcw cluster across Bacteria.
Fig. 3: Dcw gene cluster in selected taxa of the Firmicutes displaying different phenotypes.
Fig. 4: Scenario for the evolution of the dcw cluster.
Fig. 5: Organization of the dcw cluster across the CPR.
Fig. 6: Phylogeny of Bacteria based on the dcw cluster and comparison with frequently used sets of markers.

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Data availability

All data used to produce our results are provided as supporting data and can be found in ref. 19 (https://doi.org/10.17632/4y5mzppzmb.1).

Code availability

All code used to produce our results can be found in ref. 19 (https://doi.org/10.17632/4y5mzppzmb.1).

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Acknowledgements

This work was supported by funding from the French National Research Agency (ANR) (grant no. Fir-OM ANR-16-CE12-0010), the Institut Pasteur ‘Programmes Transversaux de Recherche’ (grant no. PTR 39-16), the French government’s Investissement d’Avenir Program, Laboratoire d’Excellence ‘Integrative Biology of Emerging Infectious Diseases’ (grant no. ANR-10-LABX-62-IBEID) and Moore Foundation (grant no. 71785). D.M. was supported by the Pasteur-Paris University (PPU) International PhD Program. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. This work used the computational and storage services (TARS cluster) provided by the IT department at Institut Pasteur, Paris. We thank the Innovative Genomics Institute at UC Berkeley. We also thank C. Rodrigues at the University of Warwick for discussions about the B. subtilis dcw cluster.

Author information

Author notes

  1. Daniela Megrian

    Present address: Unité de Microbiologie Structurale, Institut Pasteur, CNRS UMR 3528, Université Paris, Paris, France

Authors and Affiliations

  1. Evolutionary Biology of the Microbial Cell Institut Pasteur, Université Paris Cité, Paris, France

    Daniela Megrian, Najwa Taib & Simonetta Gribaldo

  2. Collège Doctoral Sorbonne Université, Paris, France

    Daniela Megrian

  3. Bioinformatics and Biostatistics Hub, Institut Pasteur, Université Paris Cité, Paris, France

    Najwa Taib

  4. Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA, USA

    Alexander L. Jaffe & Jillian F. Banfield

  5. Innovative Genomics Institute, University of California, Berkeley, Berkeley, CA, USA

    Jillian F. Banfield

  6. Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, CA, USA

    Jillian F. Banfield

  7. Department of Environmental Science, Policy, and Management, University of California, Berkeley, Berkeley, CA, USA

    Jillian F. Banfield

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Contributions

D.M., N.T. and A.L.J. performed the analyses. N.T. and S.G. supervised the study. D.M., N.T., A.L.J., J.F.B. and S.G. wrote the paper. All authors contributed to the final version of the manuscript.

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Correspondence to Najwa Taib or Simonetta Gribaldo.

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Supplementary Tables 1–3

1. Dcw cluster homologues in DB-SMALL (387 taxa). For each taxon, we provide the NCBI TaxID, taxonomy and the NCBI Genbank accession numbers of the homologues identified for 15 dcw cluster proteins (MraZ, MraW, FtsI, MurE, MurF, MraY, MurD, FtsW, MurG, MurC, MurB, MurA, DdlB, FtsA and FtsZ) and proteins MrdA and RodA. For each protein, there is one column that corresponds to the hits obtained with HMMSEARCH (‘_HMMSEARCH’) and one column that corresponds to the hits obtained with MacSyFinder (‘_DCW’ and ‘_cluster’). The hits were manually curated using alignments, phylogenies and synteny. This table is a reduced and cleaned version of Supplementary Table 2. 2. Dcw cluster homologues in DB-LARGE (1081 taxa). For each taxon, we provide the NCBI TaxID, organism name, NCBI assembly accession, NCBI RefSeq category of the assembly, assembly level, taxonomy and the NCBI Genbank accession numbers of the homologues identified for 15 dcw cluster proteins (MraZ, MraW, FtsI, MurE, MurF, MraY, MurD, FtsW, MurG, MurC, MurB, MurA, DdlB, FtsA and FtsZ). For each protein, there is one column that corresponds to the hits obtained with HMMSEARCH (‘_HMMSEARCH’) and one column that corresponds to the hits obtained with MacSyFinder (‘_DCW’). A separate sheet contains the dcw cluster homologues in the CPR only (279 taxa). 3. MurJ homologues in DB-SMALL (387 taxa) obtained using HMMSEARCH. For each taxon, we provide the NCBI TaxID, taxonomy and the NCBI Genbank accession numbers of the homologues.

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Megrian, D., Taib, N., Jaffe, A.L. et al. Ancient origin and constrained evolution of the division and cell wall gene cluster in Bacteria. Nat Microbiol 7, 2114–2127 (2022). https://doi.org/10.1038/s41564-022-01257-y

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