Abstract
BackgroundSpiroplasma is a widely distributed endosymbiont of insects, arthropods, and plants. In insects, Spiroplasma colonizes the gut, hemolymph, and reproductive organs of the host. Previous metagenomic surveys of the domesticated carmine cochineal Dactylopius coccus and the wild cochineal D. opuntiae reported sequences of Spiroplasma associated with these insects. However, there is no analysis of the genomic capabilities and the interaction of this Spiroplasma with Dactylopius.ResultsHere we present three Spiroplasma genomes independently recovered from metagenomes of adult males and females of D. coccus, from two different populations, as well as from adult females of D. opuntiae. Single-copy gene analysis showed that these genomes were > 92% complete. Phylogenomic analyses classified these genomes as new members of Spiroplasma ixodetis.Comparative genome analysis indicated that they exhibit fewer genes involved in amino acid and carbon catabolism compared to other spiroplasmas. Moreover, virulence factor-encoding genes (i.e., glpO, spaid and rip2) were found incomplete in these S. ixodetis genomes. We also detected an enrichment of genes encoding the type IV secretion system (T4SS) in S. ixodetis genomes of Dactylopius. A metratranscriptomic analysis of D. coccus showed that some of these T4SS genes (i.e., traG, virB4 and virD4) in addition to the superoxide dismutase sodA of S. ixodetis were overexpressed in the ovaries.ConclusionThe symbiont S. ixodetis is a new member of the bacterial community of D. coccus and D. opuntiae. The recovery of incomplete virulence factor-encoding genes in S. ixodetis of Dactylopius suggests that this bacterium is a non-pathogenic symbiont. A high number of genes encoding the T4SS, in the S. ixodetis genomes and the overexpression of these genes in the ovary and hemolymph of the host suggest that S. ixodetis use the T4SS to interact with the Dactylopius cells. Moreover, the transcriptional differences of S. ixodetis among the gut, hemolymph and ovary tissues of D. coccus indicate that this bacterium can respond and adapt to the different conditions (e.g., oxidative stress) present within the host. All this evidence proposes that there is a strong interaction and molecular signaling in the symbiosis between S. ixodetis and the carmine cochineal Dactylopius.
Highlights
Spiroplasma is a widely distributed endosymbiont of insects, arthropods, and plants
New Spiroplasma ixodetis symbiont is present in multiple Dactylopius spp. metagenomic samples Mollicute-related metagenome-assembly genomes (MAGs) were recovered in metagenomic assembled and binned samples from adult males and females of the domesticated carmine cochineal D. coccus from two different populations, as well as in the metagenome from adult females of the wild cochineal species D. opuntiae
There are multiple microbes within a single insect, and that is the case of Dactylopius spp. which is associated with the diazotroph bacterium Candidatus Dactylopiibacterium carminicum and two Wolbachia strains
Summary
Spiroplasma is a widely distributed endosymbiont of insects, arthropods, and plants. In insects, Spiroplasma colonizes the gut, hemolymph, and reproductive organs of the host. The genus Spiroplasma comprises wall-less, motile, and helical bacteria of the class Mollicutes These bacteria are mainly associated with insects but there are reports of Spiroplasma in arachnids, crustaceans and plants [2, 3]. Spiroplasma associated with insects consist of mutualists, commensals, male-killing reproductive parasites and pathogens [6]. In addition to lethal pathogenicity, two other phenotypes are induced by spiroplasmas in insects such as protection against parasites (wasps and nematodes) and male-killing. Both phenotypes are produced by Spiroplasma poulsonii in Drosophila [9,10,11]. A plasmid-encoded protein (Spaid) seems to be involved in D. melanogaster male-killing phenotype produced by S. poulsonii [11, 14]
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