Unpicking the mysterious symbiosis ofMycoplasmain salmonids

Abstract

Lacking a peptidoglycan cell wall, mycoplasmas are the smallest self-replicating life forms. Members of this bacterial genus are known to parasitise a wide array of metazoans including vertebrates. Whilst much research has been significant targeted at parasitic mammalian mycoplasmas, very little is known about their role in other vertebrates. In the current study, we aim to explore the biology and evolution of Mycoplasma in salmonids, including cellular niche, genome size structure and gene content. Using Fluorescence in-situ hybridisation (FISH), mycoplasmas were identified in epithelial tissues across the digestive tract (stomach, pyloric caecum and midgut) during the developmental stages (eggs, parr, subadult) of farmed Atlantic salmon (Salmo salar), showing a high abundance in acidic compartments. With high throughput sequencing from subadults farmed Atlantic salmon, we assembled a nearly complete genome (~0.53 MB) via shotgun-metagenomics. The phylogenetic inference from the recovered genome revealed successful taxonomic proximity to Mycoplasma penetrans (~1.36 Mb) from the recovered genome. Although no significant correlation between genome size and its phylogeny was observed, we recovered functional signatures, especially, riboflavin encoding genes pathway and sugars transporters, suggesting a symbiotic relationship between Mycoplasma and the host. Though 247 strains of Mycoplasma are available in public databases, to the best of our knowledge, this is the first study to demonstrate an ecological and functional association between Mycoplasma and Salmo salar which delineates symbiotic reductive evolution and genome erosion primarily and also serves as a proxy for salmonid health in aquaculture processes (cell lines, in vitro gut models).

Differential response of digesta- and mucosa-associated intestinal microbiota to dietary insect meal during the seawater phase of Atlantic salmon

“…Due to its small compact genome and limited biosynthesis capacities, Mycoplasma typically forms obligate parasitic or commensal relationships with its host to obtain necessary nutrients such as amino acids, fatty acids and sterols [67]. Recent shotgunmetagenomic sequencing of the Atlantic salmon Mycoplasma revealed that it is closely related to Mycoplasma penetrans [33,68]. It was suggested that the presence of ribo avin encoding genes and lack of pathogenicity factors in the metagenome-assembled Mycoplasma genome is indicative of a symbiotic relationship between the Mycoplasma and Atlantic salmon [68].…”

“…Recent shotgunmetagenomic sequencing of the Atlantic salmon Mycoplasma revealed that it is closely related to Mycoplasma penetrans [33,68]. It was suggested that the presence of ribo avin encoding genes and lack of pathogenicity factors in the metagenome-assembled Mycoplasma genome is indicative of a symbiotic relationship between the Mycoplasma and Atlantic salmon [68].…”

Differential response of digesta- and mucosa-associated intestinal microbiota to dietary black soldier fly (Hermetia illucens) larvae meal in seawater phase Atlantic salmon (Salmo salar)

“…Due to its small compact genome and limited biosynthesis capacities, Mycoplasma typically forms obligate parasitic or commensal relationships with its host to obtain necessary nutrients such as amino acids, fatty acids and sterols [67]. Recent shotgun-metagenomic sequencing of the Atlantic salmon Mycoplasma revealed that it is closely related to Mycoplasma penetrans [33,68]. It was suggested that the presence of ribo avin encoding genes and lack of pathogenicity factors in the metagenome-assembled Mycoplasma genome is indicative of a symbiotic relationship between the Mycoplasma and Atlantic salmon [68].…”

“…Recent shotgun-metagenomic sequencing of the Atlantic salmon Mycoplasma revealed that it is closely related to Mycoplasma penetrans [33,68]. It was suggested that the presence of ribo avin encoding genes and lack of pathogenicity factors in the metagenome-assembled Mycoplasma genome is indicative of a symbiotic relationship between the Mycoplasma and Atlantic salmon [68].…”

This preprint has been taken down.

“…Despite the observed dominance of Mycoplasma in salmonid hosts, very little is known about Mycoplasma and its functional potential in salmonids and other teleosts 20 . To increase knowledge of this interaction between Mycoplasma and their salmonid hosts, we present a study including three novel candidates of Mycoplasma, characterised using genome-resolved metagenomics from three different salmonid species.…”