Host and symbiont determinants of colonization by a co-evolved gut community Project Summary Host-specific gut bacteria are central to the biology and health of animals, but elucidating the processes that govern normal and atypical assembly of gut communities is challenging. Most gut communities, and specifically those of humans, are dauntingly complex;whereas others, such as that of Drosophila, have variable compositions dominated by opportunistic bacterial species from other environments. In the honey bee (Apis mellifera), the ileum region of the hindgut contains a dense but simple community dominated by only three specialized bacterial species that comprise >95% of bacteria despite the continual entry of diverse environmental microbes present in food. These three species are found only in bee guts, and distinct but related strains are found in related bee species. Our pilot work established axenic culture conditions, official nomenclature, and reference strains for all bee gut community members, transposon-based mutagenesis methods, protocols for controlling colonization with specific isolates or mutants, and methods for quantitative description of community composition. Furthermore, the host is amenable to genetic studies: sequenced genome and associated resources are available for the honey bee, and RNAi methods have been established. Building on these foundations, we will use the honey bee ileum as a model gut community to determine the specific bacterial and host factors that underlie the establishment of a persistent gut community characteristic of a host species. We will use expression analyses and genome-wide mutagenesis and mutant screening based on high-throughput sequencing to identify symbiont genes affecting colonization of the bee ileum and to elucidate the effects of host genes and pathways on colonization. We will examine how a focal pioneer symbiont influences the assembly and subsequent composition of the gut community. This will be achieved by monitoring succession in experimental gut communities and by identifying symbiont genes that affect colonization by other bacterial species and strains, including both the symbionts normally present in the community and the opportunistic or pathogenic bacteria that are typically excluded. These results will reveal host and symbiont-based processes that govern development of a normal, host- specific gut microbiota and will illuminate how and why gut communities sometimes develop abnormally, to the detriment of host health. !

Public Health Relevance

The establishment of a specialized community of gut bacteria is a critical process in animal and human development. It is governed by both bacterial and host factors, which form an immensely complex network in humans and other mammals. This project exploits a simple, experimentally tractable model to determine how interactions of host and bacteria govern development of a characteristic, host-specialized gut community, and how their disruption can lead to atypical gut communities characteristic of disease.

National Institute of Health (NIH)
National Institute of General Medical Sciences (NIGMS)
Research Project (R01)
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Special Emphasis Panel (ZGM1-GDB-2 (MC))
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Sledjeski, Darren D
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University of Texas Austin
Schools of Arts and Sciences
United States
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Raymann, Kasie; Coon, Kerri L; Shaffer, Zack et al. (2018) Pathogenicity of Serratia marcescens Strains in Honey Bees. MBio 9:
Raymann, Kasie; Moran, Nancy A (2018) The role of the gut microbiome in health and disease of adult honey bee workers. Curr Opin Insect Sci 26:97-104
Raymann, Kasie; Bobay, Louis-Marie; Moran, Nancy A (2018) Antibiotics reduce genetic diversity of core species in the honeybee gut microbiome. Mol Ecol 27:2057-2066
Raymann, Kasie; Motta, Erick V S; Girard, Catherine et al. (2018) Imidacloprid Decreases Honey Bee Survival Rates but Does Not Affect the Gut Microbiome. Appl Environ Microbiol 84:
Powell, J Elijah; Eiri, Daren; Moran, Nancy A et al. (2018) Modulation of the honey bee queen microbiota: Effects of early social contact. PLoS One 13:e0200527
Leonard, Sean P; Perutka, Jiri; Powell, J Elijah et al. (2018) Genetic Engineering of Bee Gut Microbiome Bacteria with a Toolkit for Modular Assembly of Broad-Host-Range Plasmids. ACS Synth Biol 7:1279-1290
Motta, Erick V S; Raymann, Kasie; Moran, Nancy A (2018) Glyphosate perturbs the gut microbiota of honey bees. Proc Natl Acad Sci U S A 115:10305-10310
Mockler, Blair K; Kwong, Waldan K; Moran, Nancy A et al. (2018) Microbiome structure influences infection by the parasite Crithidia bombi in bumble bees. Appl Environ Microbiol :
Kwong, Waldan K; Steele, Margaret I; Moran, Nancy A (2018) Genome Sequences of Apibacter spp., Gut Symbionts of Asian Honey Bees. Genome Biol Evol 10:1174-1179
Raymann, Kasie; Shaffer, Zack; Moran, Nancy A (2017) Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS Biol 15:e2001861

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