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Assessing Biosynthetic Gene Cluster Diversity of Specialized Metabolites in the Conserved Gut Symbionts of Herbivorous Turtle Ants.

ABSTRACT: Cephalotes are herbivorous ants (>115 species) feeding on low-nitrogen food sources, and they rely on gut symbionts to supplement their diet by recycling nitrogen food waste into amino acids. These conserved gut symbionts, which encompass five bacterial orders, have been studied previously for their primary nitrogen metabolism; however, little is known about their ability to biosynthesize specialized metabolites which can play a role in bacterial interactions between communities living in close proximity in the gut. To evaluate the biosynthetic potential of their gut symbionts, we mine 14 cultured isolate genomes and gut metagenomes across 17 Cephalotes species to explore the biodiversity of biosynthetic gene clusters (BGCs) producing specialized metabolites. The diversity of BGCs across Cephalotes phylogeny was analyzed using sequence similarity networking and BGC phylogenetic reconstruction. Our results reveal that the conserved gut symbionts involved in the nutritional symbiosis possess 80% of all the 233 BGCs retrieved in this work. Furthermore, the phylogenetic analysis of BGCs reveals different patterns of distribution, suggesting different mechanisms of conservation. A siderophore BGC shows high similarity in a single symbiont across different ant host species, whereas a BGC encoding the production of non-ribosomal peptides (NRPs) found different symbionts within a single host species. Additionally, BGCs were abundant in four of the five bacterial orders of conserved symbionts co-occurring in the hindgut. However, one major symbiont localized alone in the midgut lack BGCs. Because the spatial isolation prevents direct interaction with other symbionts, this result supports the idea that BGCs are maintained in bacteria living in close proximity but are dispensable for an alone-living symbiont. These findings together pave the way for studying the mechanisms of BGC conservation and evolution in gut bacterial genomes associated with Cephalotes. This work also provides a genetic background for further study, aiming to characterize bacterial specialized metabolites and to understand their functional role in multipartite mutualisms between conserved gut symbionts and Cephalotes turtle ants.

SUBMITTER: Chanson A

PROVIDER: S-EPMC8277422 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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.

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Assessing Biosynthetic Gene Cluster Diversity of Specialized Metabolites in the Conserved Gut Symbionts of Herbivorous Turtle Ants.

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