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Exploring the metabolic and digestive functions of bacterial gut symbionts in Cephalotes turtle ants
Dissertation   Open access

Exploring the metabolic and digestive functions of bacterial gut symbionts in Cephalotes turtle ants

Benoit Bechade
Doctor of Philosophy (Ph.D.), Drexel University
Dec 2022
DOI:
https://doi.org/10.17918/00001420
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Abstract

Enterobacteriaceae Gut bacteria Herbivory Turtle ants Biological Sciences Entomology Microbiology Symbiosis
Gut bacterial symbionts can support animal nutrition by facilitating digestion and providing valuable metabolites. Such associations have been extensively studied among termites and corbiculate bees, revealing the intricate integration of gut microbial communities as nutritional symbionts of their social insect host. In ants, while only a few clades are known to harbor prevalent specialized symbionts, some host abundant and diverse gut bacterial symbionts. The turtle ant lineage (sister genera Cephalotes and Procryptocerus) is one of these clades, which makes it an appealing model to study the nature and evolution of ant-bacteria nutritional symbioses. While the conserved turtle ant adult-associated symbionts recycle nitrogen, they may also participate in the digestion of their host's fiber-rich diet, while interacting with co-occurring microbes and hosts in unique, symbiotic ways. Additionally, nothing is known about the roles of the environmentally acquired bacterial symbionts of larvae. To explore bacterial contributions toward turtle ant nutrition, I used shotgun metagenomics, metatranscriptomics and metabolomics on turtle ant guts. Among larval gut bacteria, the Enterobacteriales could catabolize predominant dietary fibers including cellulose, hemicelluloses, lignins, starches and pectins (i.e., homogalacturonan, rhamnogalacturonan-I). At the adult stage, specialized gut symbionts encoded conserved capacities to deconstruct a similar set of dietary fibers. One adult-associated gut symbiont that was not able to digest fibers was highly prevalent among turtle ants and appeared as a central component of the nitrogen recycling, amino acid and sulfur metabolism pathways in turtle ant guts. The study on this newly described Ischyrobacter davidsoniae reveals a partitioned N-recycling uricolytic pathway likely regulated by fluxes of N-charged metabolites in the gut, and unveils, for the first time, intra-gut localization of a single turtle ant-associated symbiont. The diverse set of digestive enzymes and metabolic pathways encoded by individual symbionts among Cephalotes life stages suggests conserved and specialized symbiont-driven digestive and nutritional functions. Such roles have characterized >50 million years of Cephalotes evolution, shaping dietary exploitation and success of these diverse arboreal ants. Using state-of-the-art meta-omic techniques, this research project reveals how turtle ants, like other herbivorous social insects, have adopted symbiotic solutions to cope with limitations of plant-based diets.

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