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Gut bacteria are essential for normal cuticle development in herbivorous turtle ants.

ABSTRACT: Across the evolutionary history of insects, the shift from nitrogen-rich carnivore/omnivore diets to nitrogen-poor herbivorous diets was made possible through symbiosis with microbes. The herbivorous turtle ants Cephalotes possess a conserved gut microbiome which enriches the nutrient composition by recycling nitrogen-rich metabolic waste to increase the production of amino acids. This enrichment is assumed to benefit the host, but we do not know to what extent. To gain insights into nitrogen assimilation in the ant cuticle we use gut bacterial manipulation, ¹⁵N isotopic enrichment, isotope-ratio mass spectrometry, and ¹⁵N nuclear magnetic resonance spectroscopy to demonstrate that gut bacteria contribute to the formation of proteins, catecholamine cross-linkers, and chitin in the cuticle. This study identifies the cuticular components which are nitrogen-enriched by gut bacteria, highlighting the role of symbionts in insect evolution, and provides a framework for understanding the nitrogen flow from nutrients through bacteria into the insect cuticle.

SUBMITTER: Duplais C

PROVIDER: S-EPMC7846594 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Gut bacteria are essential for normal cuticle development in herbivorous turtle ants.

Duplais Christophe C Sarou-Kanian Vincent V Massiot Dominique D Hassan Alia A Perrone Barbara B Estevez Yannick Y Wertz John T JT Martineau Estelle E Farjon Jonathan J Giraudeau Patrick P Moreau Corrie S CS

Nature communications 20210129 1

Across the evolutionary history of insects, the shift from nitrogen-rich carnivore/omnivore diets to nitrogen-poor herbivorous diets was made possible through symbiosis with microbes. The herbivorous turtle ants Cephalotes possess a conserved gut microbiome which enriches the nutrient composition by recycling nitrogen-rich metabolic waste to increase the production of amino acids. This enrichment is assumed to benefit the host, but we do not know to what extent. To gain insights into nitrogen as ...[more]

PMID: 33514729

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Project description: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.

Project description:Microbial communities within the animal digestive tract often provide important functions for their hosts. The composition of eukaryotes' gut bacteria can be shaped by host diet, vertical bacterial transmission, and physiological variation within the digestive tract. In several ant taxa, recent findings have demonstrated that nitrogen provisioning by symbiotic bacteria makes up for deficiencies in herbivorous diets. Using 16S rRNA amplicon sequencing and qPCR, this study examined bacterial communities at a fine scale across one such animal group, the turtle ant genus Cephalotes We analyzed the composition and colonization density across four portions of the digestive tract to understand how bacterial diversity is structured across gut compartments, potentially allowing for specific metabolic functions of benefit to the host. In addition, we aimed to understand if caste differentiation or host relatedness influences the gut bacterial communities of Cephalotes ants. Microbial communities were found to vary strongly across Cephalotes gut compartments in ways that transcend both caste and host phylogeny. Despite this, caste and host phylogeny still have detectable effects. We demonstrated microbial community divergence across gut compartments, possibly due to the varying function of each gut compartment for digestion.IMPORTANCE Gut compartments play an important role in structuring the microbial community within individual ants. The gut chambers of the turtle ant digestive tract differ remarkably in symbiont abundance and diversity. Furthermore, caste type explains some variation in the microbiome composition. Finally, the evolutionary history of the Cephalotes species structures the microbiome in our study, which elucidates a trend in which related ants maintain related microbiomes, conceivably owing to co-speciation. Amazingly, gut compartment-specific signatures of microbial diversity, relative abundance, composition, and abundance have been conserved over Cephalotes evolutionary history, signifying that this symbiosis has been largely stable for over 50 million years.

Project description:BackgroundTo understand the patterns of biodiversity it is important to consider symbiotic interactions as they can shape animal evolution. In several ant genera symbiotic interactions with microbial communities have been shown to have profound impacts for the host. For example, we know that for Camponotini the gut community can upgrade the host's diet and is shaped by development and colony interactions. However, what is true for one ant group may not be true for another. For the microbial communities that have been examined across ants we see variation in the diversity, host factors that structure these communities, and the function these microbes provide for the host. In the herbivorous turtle ants (Cephalotes) their stable symbiotic interactions with gut bacteria have persisted for 50 million years with the gut bacteria synthesizing essential amino acids that are used by the host. Although we know the function for some of these turtle ant-associated bacteria there are still many open questions.ResultsIn the present study we examined microbial community diversity (16S rRNA and 18S rRNA amplicons) of more than 75 species of turtle ants across different geographic locations and in the context of the host's phylogenetic history. Our results show (1) that belonging to a certain species and biogeographic regions are relevant to structuring the microbial community of turtle ants; (2) both bacterial and eukaryotic communities demonstrated correlations and cooccurrence within the ant host; (3) within the core bacterial community, Burkholderiaceae bacterial lineage were the only group that showed strong patterns of codiversification with the host, which is remarkable since the core bacterial community is stable and persistent.ConclusionsWe concluded that for the turtle ants there is a diverse and evolutionarily stable core bacterial community, which leads to interesting questions about what microbial or host factors influence when these partner histories become evolutionarily intertwined.

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Gut bacteria are essential for normal cuticle development in herbivorous turtle ants.

Publications

Gut bacteria are essential for normal cuticle development in herbivorous turtle ants.

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