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Evolution and Diversity of Inherited Spiroplasma Symbionts in Myrmica Ants.

Abstract

Microbial partners play important roles in the biology and ecology of animals. In insects, maternally transmitted symbionts are especially common and can have host effects ranging from reproductive manipulation to nutrient provisioning and defense against natural enemies. In this study, we report a genus-wide association of Myrmica ants with the inherited bacterial symbiont Spiroplasma We screen Myrmica ants collected from the wild, including the invasive European fire ant, Myrmica rubra, and find an extraordinarily high prevalence of this symbiont-8 of 9 species, 42 of 43 colonies, and 250 of 276 individual workers harbored Spiroplasma-only one host species was uninfected. In our screens, each host species carried a distinct Spiroplasma strain, and none were infected with more than one strain. All symbionts belong to the citri clade, allied most closely with pathogenic strains of Spiroplasma infecting corn crops and honeybees, and there is strong evidence of host-symbiont persistence across evolutionary time scales. Genome sequencing of two Spiroplasma symbionts revealed candidate genes that may play a part in the symbiosis, a nutrient transporter absent from other Spiroplasma strains, and a ribosome-inactivating protein previously implicated in parasite defense. These results together suggest long-term, likely mutualistic, relationships atypical of Spiroplasma-insect associations with potential significance for broad ecological interactions with MyrmicaIMPORTANCE Animal-associated microbial symbionts can dramatically affect the biology of their hosts. The identification and characterization of these intimate partnerships remain an essential component of describing and predicting species interactions, especially for invasive host species. Ants perform crucial ecological functions as ecosystem engineers, scavengers, and predators, and ants in the genus Myrmica can be aggressive resource competitors and reach high densities in their native and invaded habitats. In this study, a novel symbiosis is identified between Myrmica ants and the facultative bacterial symbiont Spiroplasma Broad host distribution, high frequencies of infection, and host-symbiont codivergence over evolutionary time scales, an uncommon feature of Spiroplasma associations, suggest an important likely mutualistic interaction. Genome sequencing identified highly divergent gene candidates that may contribute to Spiroplasma's role as a possible defensive or nutritional partner in Myrmica.

Authors+Show Affiliations

Department of Biology, University of Victoria, Victoria, BC, Canada mattball@uvic.ca.Department of Biology, University of Victoria, Victoria, BC, Canada.Department of Biology, University of Victoria, Victoria, BC, Canada.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

29196290

Citation

Ballinger, Matthew J., et al. "Evolution and Diversity of Inherited Spiroplasma Symbionts in Myrmica Ants." Applied and Environmental Microbiology, vol. 84, no. 4, 2018.
Ballinger MJ, Moore LD, Perlman SJ. Evolution and Diversity of Inherited Spiroplasma Symbionts in Myrmica Ants. Appl Environ Microbiol. 2018;84(4).
Ballinger, M. J., Moore, L. D., & Perlman, S. J. (2018). Evolution and Diversity of Inherited Spiroplasma Symbionts in Myrmica Ants. Applied and Environmental Microbiology, 84(4), doi:10.1128/AEM.02299-17.
Ballinger MJ, Moore LD, Perlman SJ. Evolution and Diversity of Inherited Spiroplasma Symbionts in Myrmica Ants. Appl Environ Microbiol. 2018 02 15;84(4) PubMed PMID: 29196290.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Evolution and Diversity of Inherited Spiroplasma Symbionts in Myrmica Ants. AU - Ballinger,Matthew J, AU - Moore,Logan D, AU - Perlman,Steve J, Y1 - 2018/01/31/ PY - 2017/10/17/received PY - 2017/11/27/accepted PY - 2017/12/3/pubmed PY - 2019/1/31/medline PY - 2017/12/3/entrez KW - defensive symbiosis KW - facultative symbiont KW - mutualism KW - ribosome-inactivating proteins KW - symbiosis JF - Applied and environmental microbiology JO - Appl. Environ. Microbiol. VL - 84 IS - 4 N2 - Microbial partners play important roles in the biology and ecology of animals. In insects, maternally transmitted symbionts are especially common and can have host effects ranging from reproductive manipulation to nutrient provisioning and defense against natural enemies. In this study, we report a genus-wide association of Myrmica ants with the inherited bacterial symbiont Spiroplasma We screen Myrmica ants collected from the wild, including the invasive European fire ant, Myrmica rubra, and find an extraordinarily high prevalence of this symbiont-8 of 9 species, 42 of 43 colonies, and 250 of 276 individual workers harbored Spiroplasma-only one host species was uninfected. In our screens, each host species carried a distinct Spiroplasma strain, and none were infected with more than one strain. All symbionts belong to the citri clade, allied most closely with pathogenic strains of Spiroplasma infecting corn crops and honeybees, and there is strong evidence of host-symbiont persistence across evolutionary time scales. Genome sequencing of two Spiroplasma symbionts revealed candidate genes that may play a part in the symbiosis, a nutrient transporter absent from other Spiroplasma strains, and a ribosome-inactivating protein previously implicated in parasite defense. These results together suggest long-term, likely mutualistic, relationships atypical of Spiroplasma-insect associations with potential significance for broad ecological interactions with MyrmicaIMPORTANCE Animal-associated microbial symbionts can dramatically affect the biology of their hosts. The identification and characterization of these intimate partnerships remain an essential component of describing and predicting species interactions, especially for invasive host species. Ants perform crucial ecological functions as ecosystem engineers, scavengers, and predators, and ants in the genus Myrmica can be aggressive resource competitors and reach high densities in their native and invaded habitats. In this study, a novel symbiosis is identified between Myrmica ants and the facultative bacterial symbiont Spiroplasma Broad host distribution, high frequencies of infection, and host-symbiont codivergence over evolutionary time scales, an uncommon feature of Spiroplasma associations, suggest an important likely mutualistic interaction. Genome sequencing identified highly divergent gene candidates that may contribute to Spiroplasma's role as a possible defensive or nutritional partner in Myrmica. SN - 1098-5336 UR - https://www.unboundmedicine.com/medline/citation/29196290/Evolution_and_Diversity_of_Inherited_Spiroplasma_Symbionts_in_Myrmica_Ants_ L2 - http://aem.asm.org/cgi/pmidlookup?view=long&pmid=29196290 DB - PRIME DP - Unbound Medicine ER -