Large-Scale Analysis of the Mycoplasma bovis Genome Identified Non-essential, Adhesion- and Virulence-Related Genes

Josi, Christoph; Bürki, Sibylle; Vidal, Sara; Dordet‐Frisoni, Emilie; Citti, Christine; Falquet, Laurent; Pilo, Paola

doi:10.3389/fmicb.2019.02085

Cited by 21 publications

(18 citation statements)

References 88 publications

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“…A more recent rlmD loss was observed for some species, including M. pulmonis, and subgroups of species including M. ovipneumoniae and M. hyopneumoniae (node 19). A recent gene-essentiality study based on transposon mutagenesis in M. bovis indicated that rlmD (MBOVJF4278_00748) was not necessary [67], reinforcing the dispensability of these rRNA methylases.…”

Section: Discussionmentioning

confidence: 99%

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Reductive Evolution and Diversification of C5-Uracil Methylation in the Nucleic Acids of Mollicutes

et al. 2020

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The C5-methylation of uracil to form 5-methyluracil (m5U) is a ubiquitous base modification of nucleic acids. Four enzyme families have converged to catalyze this methylation using different chemical solutions. Here, we investigate the evolution of 5-methyluracil synthase families in Mollicutes, a class of bacteria that has undergone extensive genome erosion. Many mollicutes have lost some of the m5U methyltransferases present in their common ancestor. Cases of duplication and subsequent shift of function are also described. For example, most members of the Spiroplasma subgroup use the ancestral tetrahydrofolate-dependent TrmFO enzyme to catalyze the formation of m5U54 in tRNA, while a TrmFO paralog (termed RlmFO) is responsible for m5U1939 formation in 23S rRNA. RlmFO has replaced the S-adenosyl-L-methionine (SAM)-enzyme RlmD that adds the same modification in the ancestor and which is still present in mollicutes from the Hominis subgroup. Another paralog of this family, the TrmFO-like protein, has a yet unidentified function that differs from the TrmFO and RlmFO homologs. Despite having evolved towards minimal genomes, the mollicutes possess a repertoire of m5U-modifying enzymes that is highly dynamic and has undergone horizontal transfer.

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Section: Discussionmentioning

confidence: 99%

“…In another study, a transposon library of M. bovis strain JF-4278 was recently shown to include a trmFO-like disrupted mutant whose ability to bind to primary bovine mammary gland epithelial (bMec) cells was reduced, suggesting this gene is a virulence factor in M. bovis [67].…”

Section: Discussionmentioning

confidence: 99%

Reductive Evolution and Diversification of C5-Uracil Methylation in the Nucleic Acids of Mollicutes

et al. 2020

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“…These laboratory conditions have largely contributed to the understanding of the biology of these minimal bacteria but provided only limited information on the strategies these organisms have evolved to secure their survival in the animal host and get access to essential nutritional resources. In the absence of small animal models, eukaryotic cell cultures as re-emerged as a valuable environment to revisit the minimal cell concept at the light of host-pathogen interactions [30][31][32][33]44]. Our functional genomic study with the genome-reduced pathogen M. bovis revealed that phosphodiesterases involved in cyclic dinucleotides and nanoRNAs degradation are critical for survival under cell culture conditions, while dispensable in axenic medium.…”

Section: Discussionmentioning

confidence: 99%

An emerging role for cyclic dinucleotide phosphodiesterase and nanoRNase activities in Mycoplasma bovis: Securing survival in cell culture

et al. 2020

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Mycoplasmas are host-restricted prokaryotes with a nearly minimal genome. To overcome their metabolic limitations, these wall-less bacteria establish intimate interactions with epithelial cells at mucosal surfaces. The alarming rate of antimicrobial resistance among pathogenic species is of particular concern in the medical and veterinary fields. Taking advantage of the reduced mycoplasma genome, random transposon mutagenesis was combined with high-throughput screening in order to identify key determinants of mycoplasma survival in the host-cell environment and potential targets for drug development. With the use of the ruminant pathogen Mycoplasma bovis as a model, three phosphodiesterases of the DHH superfamily were identified as essential for the proliferation of this species under cell culture conditions, while dispensable for axenic growth. Despite a similar domain architecture, recombinant Mbov_0327 and Mbov_0328 products displayed different substrate specificities. While rMbovP328 protein exhibited activity towards cyclic dinucleotides and nanoR-NAs, rMbovP327 protein was only able to degrade nanoRNAs. The Mbov_0276 product was identified as a member of the membrane-associated GdpP family of phosphodiesterases that was found to participate in cyclic dinucleotide and nanoRNA degradation, an activity which might therefore be redundant in the genome-reduced M. bovis. Remarkably, all these enzymes were able to convert their substrates into mononucleotides, and medium supplementation with nucleoside monophosphates or nucleosides fully restored the capacity of a Mbov_0328/0327 knockout mutant to grow under cell culture conditions. Since mycoplasmas are unable to synthesize DNA/RNA precursors de novo, cyclic dinucleotide and nanoRNA degradation are likely contributing to the survival of M. bovis by securing the recycling of purines and pyrimidines. These results point toward proteins of the DHH

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“…A more recent rlmD loss was observed for some species, including M. pulmonis, and subgroups of species including M. ovipneumoniae and M. hyopneumoniae (node 19). A recent gene-essentiality study based on transposon mutagenesis in M. bovis indicated that rlmD (MBOVJF4278_00748) was not essential [67] reinforcing the dispensability of these rRNA methylases.…”

Section: Discussionmentioning

confidence: 99%

“…Their conclusion was mainly driven by the demonstration of a fibronectinbinding activity of TrmFO-like using ELISA and direct adhesion assays on embryonic bovine lung (EBL) cells, including inhibition by anti-TrmFO-like polyclonal antibiodies. In another study, a transposon library of M. bovis strain JF-4278 was recently shown to include a trmFO-like disrupted mutant which ability to bind to primary bovine mammary gland epithelial (bMec) cells was reduced, suggesting this gene is a virulence factor in M. bovis [67].…”

Section: Discussionmentioning

confidence: 99%

Reductive Evolution and Diversification of C5-Uracil Methylation in the Nucleic Acids of Mollicutes

Sirand‐Pugnet¹,

Brégeon²,

Béven³

et al. 2020

Preprint

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The C5-methylation of uracil to form 5-methyluracil (m 5 U) is a ubiquitous base modification of nucleic acids. Four enzyme families have converged to catalyze this methylation using different chemical solutions. Here, we investigate the evolution of 5-methyluracil synthase families in Mollicutes, a class of bacteria that has undergone extensive genome erosion. Many mollicutes have lost some of the m 5 U methyltransferases present in their common ancestor. Cases of duplication and subsequent shift of function are also described. For example, most members of the Spiroplasma subgroup, use the ancestral tetrahydrofolate-dependent TrmFO enzyme, to catalyze the formation of m 5 U54 in tRNA, while a TrmFO paralog (termed RlmFO) is responsible for m 5 U1939 formation in 23S RNA. RlmFO has replaced the S-adenosyl-l-methionine (SAM)enzyme RlmD that adds the same modification in the ancestor and which is still present in mollicutes from the Hominis subgroup. Another paralog of this family, the TrmFO-like protein, has a yet unidentified function that differs from the TrmFO and RlmFO homologs. Despite having evolved towards minimal genomes, the mollicutes possess a repertoire of m 5 U modifying enzymes that is highly dynamic and has undergone horizontal transfer. This emphasizes the necessity for combining bioinformatics predictions with empirical testing and structural information to get a reliable functional annotation of these enzymes.

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Large-Scale Analysis of the Mycoplasma bovis Genome Identified Non-essential, Adhesion- and Virulence-Related Genes

Cited by 21 publications

References 88 publications

Reductive Evolution and Diversification of C5-Uracil Methylation in the Nucleic Acids of Mollicutes

Reductive Evolution and Diversification of C5-Uracil Methylation in the Nucleic Acids of Mollicutes

An emerging role for cyclic dinucleotide phosphodiesterase and nanoRNase activities in Mycoplasma bovis: Securing survival in cell culture

Reductive Evolution and Diversification of C5-Uracil Methylation in the Nucleic Acids of Mollicutes

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