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Herbivorous turtle ants obtain essential nutrients from a conserved nitrogen-recycling gut microbiome.

ABSTRACT: Nitrogen acquisition is a major challenge for herbivorous animals, and the repeated origins of herbivory across the ants have raised expectations that nutritional symbionts have shaped their diversification. Direct evidence for N provisioning by internally housed symbionts is rare in animals; among the ants, it has been documented for just one lineage. In this study we dissect functional contributions by bacteria from a conserved, multi-partite gut symbiosis in herbivorous Cephalotes ants through in vivo experiments, metagenomics, and in vitro assays. Gut bacteria recycle urea, and likely uric acid, using recycled N to synthesize essential amino acids that are acquired by hosts in substantial quantities. Specialized core symbionts of 17 studied Cephalotes species encode the pathways directing these activities, and several recycle N in vitro. These findings point to a highly efficient N economy, and a nutritional mutualism preserved for millions of years through the derived behaviors and gut anatomy of Cephalotes ants.

SUBMITTER: Hu Y

PROVIDER: S-EPMC5840417 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Herbivorous turtle ants obtain essential nutrients from a conserved nitrogen-recycling gut microbiome.

Hu Yi Y Sanders Jon G JG Łukasik Piotr P D'Amelio Catherine L CL Millar John S JS Vann David R DR Lan Yemin Y Newton Justin A JA Schotanus Mark M Kronauer Daniel J C DJC Pierce Naomi E NE Moreau Corrie S CS Wertz John T JT Engel Philipp P Russell Jacob A JA

Nature communications 20180306 1

Nitrogen acquisition is a major challenge for herbivorous animals, and the repeated origins of herbivory across the ants have raised expectations that nutritional symbionts have shaped their diversification. Direct evidence for N provisioning by internally housed symbionts is rare in animals; among the ants, it has been documented for just one lineage. In this study we dissect functional contributions by bacteria from a conserved, multi-partite gut symbiosis in herbivorous Cephalotes ants throug ...[more]

PMID: 29511180

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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: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.

Project description:Marine herbivorous fish that feed primarily on macroalgae, such as those from the genus Kyphosus, are essential for maintaining coral health and abundance on tropical reefs. Here, deep metagenomic sequencing and assembly of gut compartment-specific samples from three sympatric, macroalgivorous Hawaiian kyphosid species have been used to connect host gut microbial taxa with predicted protein functional capacities likely to contribute to efficient macroalgal digestion. Bacterial community compositions, algal dietary sources, and predicted enzyme functionalities were analyzed in parallel for 16 metagenomes spanning the mid- and hindgut digestive regions of wild-caught fishes. Gene colocalization patterns of expanded carbohydrate (CAZy) and sulfatase (SulfAtlas) digestive enzyme families on assembled contigs were used to identify likely polysaccharide utilization locus associations and to visualize potential cooperative networks of extracellularly exported proteins targeting complex sulfated polysaccharides. These insights into the gut microbiota of herbivorous marine fish and their functional capabilities improve our understanding of the enzymes and microorganisms involved in digesting complex macroalgal sulfated polysaccharides. IMPORTANCE This work connects specific uncultured bacterial taxa with distinct polysaccharide digestion capabilities lacking in their marine vertebrate hosts, providing fresh insights into poorly understood processes for deconstructing complex sulfated polysaccharides and potential evolutionary mechanisms for microbial acquisition of expanded macroalgal utilization gene functions. Several thousand new marine-specific candidate enzyme sequences for polysaccharide utilization have been identified. These data provide foundational resources for future investigations into suppression of coral reef macroalgal overgrowth, fish host physiology, the use of macroalgal feedstocks in terrestrial and aquaculture animal feeds, and the bioconversion of macroalgae biomass into value-added commercial fuel and chemical products.

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.

Dataset Information

Herbivorous turtle ants obtain essential nutrients from a conserved nitrogen-recycling gut microbiome.

Publications

Herbivorous turtle ants obtain essential nutrients from a conserved nitrogen-recycling gut microbiome.

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