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Spiroplasma Display an Intricate Continuum of Infection Heterogeneity and Persistence in Myrmica Ants
Diego Castillo Franco1, Thomas Parmentier1,2, Tessa Van de Walle1
1Department of Biology, Ghent University, Ghent, Belgium.
Abstract:
Many bacterial taxa evolved facultative symbiotic associations with insects and spread through host populations by horizontal and maternal transmission. Co-infection at the individual host level may facilitate or constrain the spread of facultative symbionts. Due to insufficiently detailed genotyping, co-infections of maternally transmitted symbionts often remain hidden, limiting our understanding of (co-)infection dynamics. Spiroplasma bacteria exhibit multiple independent origins of symbiosis with insects and have poorly understood patterns of transmission and co-infection. Here, we examined these traits of Spiroplasma symbiosis using Myrmica ants, a system known for high frequencies of single Spiroplasma infections. Through exhaustive genotyping of 75 colonies across seven Myrmica species, we uncovered multiple cryptic co-infections involving two distinct Spiroplasma clades that display significantly different infection frequencies in workers. Within Myrmica ruginodis, infection heterogeneity was contingent on ant caste and was lower in workers. Remarkably, the sMyr Spiroplasma variant infected four Myrmica species and was widespread in queens and workers. We provide phylogenomic and functional genomic support for an exceptionally stable symbiosis with maternally acquired sMyr, with a predicted infection persistence of seven million years in the Myrmica scabrinodis species group. Our findings reveal that Spiroplasma can display complex infection heterogeneity and evolve an evolutionary stable maternally acquired infection within insect hosts.
Insights
Spiroplasma bacteria in ants can exist in hidden co-infections, with one variant showing a remarkably stable, long-term maternal transmission. This reveals complex infection dynamics in insect symbionts.
Area of Science:
- Microbiology
- Insect Symbiosis
- Genomics
Background:
- Facultative bacterial symbionts spread in insect populations via horizontal and maternal transmission.
- Co-infections can influence the dynamics of symbiont spread, but are often undetected due to limited genotyping.
- Spiroplasma bacteria have diverse symbiotic associations with insects, with unclear transmission and co-infection patterns.
Purpose of the Study:
- To investigate the transmission patterns and co-infection dynamics of Spiroplasma symbionts in Myrmica ants.
- To identify cryptic co-infections and characterize their prevalence and stability.
- To explore the evolutionary stability of Spiroplasma symbiosis in ants.
Main Methods:
- Exhaustive genotyping of Spiroplasma in 75 Myrmica ant colonies across seven species.
- Phylogenomic and functional genomic analyses.
- Assessment of infection frequency variation by ant caste and species.
Main Results:
- Multiple cryptic Spiroplasma co-infections were discovered, involving two distinct clades with differing infection frequencies.
- Infection heterogeneity varied by ant caste, being lower in Myrmica ruginodis workers.
- The sMyr Spiroplasma variant showed widespread infection across four Myrmica species and was prevalent in both queens and workers.
- Phylogenomic data suggest an exceptionally stable symbiosis for sMyr, with an estimated seven-million-year persistence in the Myrmica scabrinodis species group.
Conclusions:
- Spiroplasma symbiosis in ants exhibits complex infection heterogeneity, including cryptic co-infections.
- An evolutionary stable, maternally acquired infection strategy can evolve in Spiroplasma symbionts.
- The sMyr variant represents a long-term, stable insect-microbe association within the Myrmica genus.
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