Genome Mosaicism in Field Strains of Mycoplasma bovis as Footprints of In-Host Horizontal Chromosomal Transfer

García-Galán, Ana; Baranowski, Éric; Hygonenq, Marie-Claude; Walch, Mathilda; Croville, Guillaume; Citti, Christine; Fe, Christian de la; Nouvel, Laurent-Xavier

doi:10.1128/aem.01661-21

Cited by 11 publications

(4 citation statements)

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“…Our study argues strongly for using the polC gene fragment as a reliable subtyping marker, as it has few discrepancies with the genomic data (Fig. S2), possibly due to homologous recombination or mycoplasma chromosomal transfer events [33, 59]. However, our results also show that within one subtype, the polC marker failed to identify lineages, and their dynamics of evolution and replacement.…”

Section: Discussionmentioning

confidence: 61%

“…We collated all the genomic data publicly available from the National Center for Biotechnology Information (NCBI, last accessed July 2022), including 138 complete and near-complete genomes (including two French M. bovis st2 complete genomes, strain L15762 [24] and strain RM16 [33]), 373 assembled draft genomes (whole-genome shotgun; WGS) and 950 raw read datasets (Short-Read Archive; SRA). For each category, we retrieved, when available, the isolate name, country of origin and date of collection.…”

Section: Methodsmentioning

confidence: 99%

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Genome-wide phylodynamic approach reveals the epidemic dynamics of the main Mycoplasma bovis subtype circulating in France

et al. 2023

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Mycoplasma bovis is a major aetiological agent of bovine respiratory disease worldwide. Genome-based analyses are increasingly being used to monitor the genetic diversity and global distribution of M. bovis , complementing existing subtyping schemes based on locus sequencing. However, these analyses have so far provided limited information on the spatiotemporal and population dynamics of circulating subtypes. Here we applied a genome-wide phylodynamic approach to explore the epidemic dynamics of 88 French M. bovis strains collected between 2000 and 2019 in France and belonging to the currently dominant polC subtype 2 (st2). A strong molecular clock signal detected in the genomic data enabled robust phylodynamic inferences, which estimated that the M. bovis st2 population in France is composed of two lineages that successively emerged from independent introductions of international strains. The first lineage appeared around 2000 and supplanted the previously established antimicrobial-susceptible polC subtype 1. The second lineage, which is likely more transmissible, progressively replaced the first M. bovis st2 lineage population from 2005 onward and became predominant after 2010. Analyses also showed a brief decline in this second M. bovis st2 lineage population in around 2011, possibly due to the challenge from the concurrent emergence of M. bovis polC subtype 3 in France. Finally, we identified non-synonymous mutations in genes associated with lineages, which raises prospects for identifying new surveillance molecular markers. A genome-wide phylodynamic approach provides valuable resources for monitoring the evolution and epidemic dynamics of circulating M. bovis subtypes, and may prove critical for developing more effective surveillance systems and disease control strategies.

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Section: Discussionmentioning

confidence: 61%

Section: Methodsmentioning

confidence: 99%

Genome-wide phylodynamic approach reveals the epidemic dynamics of the main Mycoplasma bovis subtype circulating in France

et al. 2023

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“…Related to the resistance to FQN, the analysis of the QRDR region of ST-1 strains circulating in Spain has shown the presence of mutations that could be related to resistence in some of them, but also in other areas of the genes analyzed. Previous studies evidenced that with the same number of in vitro passages, ST-1 biotypes failed to acquire substitutions in these targets [ 7 ], although the presence of these mutations could be the result of the pressure exerted by the use of fluoroquinolones or even the presence of new, unanalyzed resistance mechanisms acquired through various mechanisms such as horizontal transfer or others, whose presence has recently been demonstrated in vivo in Spanish strains [ 23 ].…”

Section: Discussionmentioning

confidence: 99%

A Set of Multiresistant Isolates of Mycoplasma bovis Subtype ST-1 with a Variable Susceptibility to Quinolones Are Also Circulating in Spain

Corrales,

Sánchez,

Hernández

et al. 2024

Pathogens

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Mycoplasma bovis (M. bovis) is one of the worldwide most important infectious agents involved in respiratory complex diseases (RCD). In Spain, the endemic presence of subtypes ST-2 and ST-3 with phenotypic differences linked to their susceptibility to fluoroquinolones opened the way to develop control strategies focused on previous diagnosis of the subtype and the use of directed therapies when M. bovis were involved in RCD. Surprisingly, microbiological studies conducted during 2023 evidenced for the first time the presence of Spanish isolates of a new polC-subtype, previously classified as ST-1, recovered from calves with respiratory symptoms and pneumonia in different areas of the country (n = 16). Curiously, the minimum inhibitory concentration (MIC) to a panel of antimicrobials revealed phenotypic differences between these ST-1 isolates when using fluoroquinolones (FLQ). There is no geographical correlation between MIC profiles even for a set of 8 isolates recovered from different animals in the same flock. Sequencing of 4 genes (gyrA, gyrB, parC and parE) encoding quinolone resistance-determining regions (QRDR) evidenced the presence of accumulate mutations in 2 ST-1 isolates with high FLQ MICs, but not in all them (n = 3), thus suggesting that, as previously recorded for ST-2 isolates, other mechanisms should be involved in the acquisition of resistence to these antimicrobials. Additionally, as previously detected in the Spanish ST-2 and ST-3, subtype ST-1 isolates are also resistant to macrolides or lincosamides.

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“…Furthermore, our genomic analyses argue for the pertinence of polC subtyping or other MLST schemes for disease surveillance purposes. MLST schemes have recently come under criticism as CTs could result in a modified subtype-associated allele without a complete change of the genomic background [ 47 ]. However, we believe that the benefit–cost ratio of MLST remains sound, as the technique is easy to handle and relatively inexpensive, and connects up nicely with the other genomic features and evolutionary history of lineages.…”

Section: Discussionmentioning

confidence: 99%

Genomic features of Mycoplasma bovis subtypes currently circulating in France

et al. 2022

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Background Mycoplasma (M.) bovis is a major etiological agent of bovine respiratory disease, which is the most economically costly disease of cattle worldwide. Cattle disease surveillance on M. bovis is increasingly using gene-based techniques, such as multilocus sequence typing (MLST), or genome-based techniques such as core genome MLST that both require only partial genomic data. However, accurate up-to-date surveillance also demands complete, circular genomes that can be used as reference to track the evolution of the different lineages. Yet, in France, two of the main subtypes currently circulating still have no representing genome in public databases. Here, to address this gap, we provide and compare three new complete M. bovis genomes obtained from recent clinical isolates that represent major subtypes circulating in France and Europe. Results Genomes were obtained using a hybrid assembly strategy (Illumina and Nanopore) with fine-tuning of settings and inputs used in the Unicycler assembly pipeline, such as size selection of reads and quality trimming of the FASTQ files. The main characteristics and synteny of the genomes were compared. The three genomes mainly differed by their content in terms of mobile genetic elements, i.e. integrative conjugative elements (ICE) and insertion sequences (IS), a feature that impacts their structure. For instance, strain L15527, representing subtype3 (st3), harbours an exceptionally high number of ICEs, which results in a bigger-sized genome than all those previously described and could be associated with the propensity of st3 to gain and fix mutations through chromosomal transfer mechanisms. In contrast, strain F9160, of st1, is very close to the PG45 type strain isolated in 1961 in the USA, and harbours a huge number of IS. These features may be associated with an evolution towards a host-restricted state or in a “closed” host or environment reservoir until a recent re-emergence. Conclusions Whole-genome comparison of the three French M. bovis subtypes provides valuable resources for future studies combining epidemiology, phylogenetic data, and phylodynamic methods.

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Genome Mosaicism in Field Strains of Mycoplasma bovis as Footprints of In-Host Horizontal Chromosomal Transfer

Abstract: Mycoplasma bovis is a major pathogen of cattle that has significant detrimental effects on economics and animal welfare in cattle rearing worldwide. Understanding the evolution and the adaptative potential of pathogenic mycoplasma species in the natural host is essential to combating them.

Cited by 11 publications

References 56 publications

Genome-wide phylodynamic approach reveals the epidemic dynamics of the main Mycoplasma bovis subtype circulating in France

Genome-wide phylodynamic approach reveals the epidemic dynamics of the main Mycoplasma bovis subtype circulating in France

A Set of Multiresistant Isolates of Mycoplasma bovis Subtype ST-1 with a Variable Susceptibility to Quinolones Are Also Circulating in Spain

Genomic features of Mycoplasma bovis subtypes currently circulating in France

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