Comparison of Metabolic Capacities and Inference of Gene Content Evolution in Mosquito-Associated Spiroplasma diminutum and S. taiwanense

Abstract

Mosquitoes are hosts of several Spiroplasma species that belong to different serogroups. To investigate the genetic mechanisms that may be involved in the utilization of similar hosts in these phylogenetically distinct bacteria, we determined the complete genome sequences of Spiroplasma diminutum and S. taiwanense for comparative analysis. The genome alignment indicates that their chromosomal organization is highly conserved, which is in sharp contrast to the elevated genome instabilities observed in other Spiroplasma lineages. Examination of the substrate utilization strategies revealed that S. diminutum can use a wide range of carbohydrates, suggesting that it is well suited to living in the gut (and possibly the circulatory system) of its mosquito hosts. In comparison, S. taiwanense has lost several carbohydrate utilization genes and acquired additional sets of oligopeptide transporter genes through tandem duplications, suggesting that proteins from digested blood meal or lysed host cells may be an important nutrient source. Moreover, one glycerol-3-phosphate oxidase gene (glpO) was found in S. taiwanense but not S. diminutum. This gene is linked to the production of reactive oxygen species and has been shown to be a major virulence factor in Mycoplasma mycoides. This finding may explain the pathogenicity of S. taiwanense observed in previous artificial infection experiments, while no apparent effect was found for S. diminutum. To infer the gene content evolution at deeper divergence levels, we incorporated other Mollicutes genomes for comparative analyses. The results suggest that the losses of biosynthetic pathways are a recurrent theme in these host-associated bacteria.

Spiroplasma – an emerging arthropod-borne pathogen?

“…They are restricted to the gut and may be regarded as commensals (benefits only bacterium) or, less often, as mutualists when both bacterium and insect benefit. For example, some spiroplasmas can provide protection against parasitic nematodes, parasitoid wasps, or fungal pathogens in their Drosophila or aphid hosts [19]. Another example is the infection of leafhopper Dalbulus maidis by Spiroplasma kunkelii that enhances the insect's ability to survive cold winter periods without its plant host being available [6].…”

“…From the human viewpoint, the most harmful are the honeybee pathogens Spiroplasma melliferum and Spiroplasma apis, which multiply abundantly in the haemolymph and kill the bee [12,16,19]. The plant species Spiroplasma floricola may cause the lethargy disease of cockchafer (Melolontha melolontha).…”

“…Spiroplasma poulsonii infects the neotropical species of Drosophila, is transmitted transovarially and kills the male progeny of an infected female fly, hence the name gender-ratio spiroplasma. A number of other spiroplasmas in a variety of insect hosts, including beetles and butterflies, have been also identified as causative agents of such gender-ratio distortions [9,6,19]. Some insect-derived spiroplasmas are also found on plant surfaces; for instance, Spiroplasma apis was cultured from the surfaces of flowers growing in the vicinity of affected beehives.…”

“…Spiroplasma strains have been isolated from a number of blood-sucking insects, including tabanids (horseflies and deerflies) [20] and mosquitoes [19,21]. Spiroplasmas have been isolated from mosquitoes in the USA, France, and Taiwan.…”

“…Spiroplasmas have been isolated from mosquitoes in the USA, France, and Taiwan. To-date, 4 Spiroplasma species have been isolated from mosquitoes, including S. culicicola from the salt marsh mosquito Aedes sollicitans, collected in New Jersey, USA, S. sabaudiense from a mixed pool of A. sticticus and A. vexans, collected in the French Northern Alps, and 2 species from mosquitoes collected in Taiwan: S. taiwanense from Culex tritaeniorhynchus and S. diminutum from C. annulus and C. tritaeniorhynchus [19]. Of these, 2 speies (S. culicicola and S. taiwanense) appeared pathogenic for mosquitoes, which creates the possibility for using them as biocontrol agents for combating these insect pests [19].…”