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Abstract

The complex dynamics between a host organism and its accompanying microbiota have long been understood as important to host health. Recent research has focused on uncovering general rules that broadly dictate microbial community composition and host consequences. However, this work is limited by a lack of low-cost models that can replicate the complexity of a mammalian gut microbiome while remaining tractable to manipulation. The American cockroach is a large and long-lived omnivorous insect that has served as a model for scientific pursuits in neurology and physiology, and more recently as an emerging model for the study of host-microbiome interactions. Despite its history, there is no complete genome assembly of this remarkable insect to guide molecular work. To fill this gap, we have sequenced and assembled the genome of Periplaneta americana to chromosomal resolution and identified genes of interest for future work in elucidating host factors involved in microbial community composition. The cockroach contains a diverse hindgut microbiome that resembles those of omnivorous mammals. Prior research has established the gut community of P. americana to be resilient in the face of extreme dietary shifts, so we tested this capacity with synthetic single-fiber diets. Our results demonstrated that these diets induced fiber-dependent shifts in microbiome composition due to overgrowth of individual taxa in response to specific polysaccharides. The utility of the cockroach as an in vivo culture system, where single-source purified components can be studied within the context of a complex community, has exciting prospects for future microbiome research. Cockroach hindgut microbiota encode functions for systematically degrading substrates. Genomes from culture, metagenomes, and single cells have increased knowledge of cockroach microbial members but how they functionally respond to different fibers is unexplored. To decipher microbial response to fiber, we gave xylan, cellulose, or a mixture as sole carbohydrate source in synthetic diets to adult cockroaches, then sequenced the 16S rRNA gene and metatranscriptomic activity. Our results uncovered different organismal responses to the shifting fiber gradient due to the diverse mechanisms they employed to survive or thrive. These findings showcase our host model for performing in-depth organism-centric microbiome analysis in complex gut communities.

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