Abstract
The bacterium Mycoplasma agalactiae is responsible for contagious agalactia (CA) in small domestic ruminants, a syndrome listed by the World Organization for Animal Health and responsible for severe damage to the dairy industry. Recently, we frequently isolated this pathogen from lung lesions of ibexes during a mortality episode in the French Alps. This situation was unusual in terms of host specificity and tissue tropism, raising the question of M. agalactiae emergence in wildlife. To address this issue, the ibex isolates were characterized using a combination of approaches that included antigenic profiles, molecular typing, optical mapping, and whole-genome sequencing. Genome analyses showed the presence of a new, large prophage containing 35 coding sequences (CDS) that was detected in most but not all ibex strains and has a homolog in Mycoplasma conjunctivae, a species causing keratoconjunctivitis in wild ungulates. This and the presence in all strains of large integrated conjugative elements suggested highly dynamic genomes. Nevertheless, M. agalactiae strains circulating in the ibex population were shown to be highly related, most likely originating from a single parental clone that has also spread to another wild ungulate species of the same geographical area, the chamois. These strains clearly differ from strains described in Europe so far, including those found nearby, before CA eradication a few years ago. While M. agalactiae pathogenicity in ibexes remains unclear, our data showed the emergence of atypical strains in Alpine wild ungulates, raising the question of a role for the wild fauna as a potential reservoir of pathogenic mycoplasmas.
Highlights
Mycoplasma agalactiae is a wall-less bacterium responsible for contagious agalactia (CA) in small ruminants, a syndrome that causes important economic losses to the dairy industry and is listed as a notifiable disease by the World Organization for Animal Health (OIE)
The situation observed in Alpine ibexes suggests that the associated M. agalactiae strains are atypical in their tissue tropism and virulence, yet the direct role of this pathogen in lung lesions observed during the mortality episode cannot be experimentally addressed in this protected species
Genomic and proteomic data were already available for two M. agalactiae strains, PG2 and 5632, both of which were isolated from small ruminants with CA
Summary
Mycoplasma agalactiae is a wall-less bacterium responsible for contagious agalactia (CA) in small ruminants, a syndrome that causes important economic losses to the dairy industry and is listed as a notifiable disease by the World Organization for Animal Health (OIE). The Alps are known to shelter native populations of Alpine ibex (Capra ibex ibex), a wild ungulate endemic to Europe that is protected by European or national legislation in most European Union countries In these populations, several keratoconjunctivitis outbreaks that were associated with Mycoplasma conjunctivae in Switzerland [31], or with other Mycoplasma species in Italy [10], were reported, but never any associated with M. agalactiae. Repetitive isolations of M. agalactiae from the lungs of Alpine ibexes with severe pneumonia lesions by our group raised the question of the emergence and circulation of new M. agalactiae strains among protected wildlife To address this issue, we undertook fine characterization of these ibex strains using a number of approaches, including genome sequencing of a representative strain, optical mapping, and molecular typing. Genome analyses led to the discovery in ibex strains of a new, large mobile genetic element that displays phage features and is absent from the M. agalactiae genomes published so far
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