Nancy A. Moran

PAST Research Projects

Host and Symbiont Determinants of Colonization by a Co-evolved Gut Community

(PI is Nancy Moran)

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.

Selected publications

• Cerqueira AES, Hammer TJ, Moran NA, Santana WC, Kasuya MCM, da Silva CC. 2021. Extinction of anciently associated gut bacterial symbionts in a clade of stingless bees. ISME J. 15(9):2813-2816. doi: 10.1038/s41396-021-01000-1.

• Steele MI, Moran NA. 2021. Evolution of interbacterial antagonism in bee gut microbiota reflects host and symbiont diversification. mSystems 6(3):e00063-21. doi: 10.1128/mSystems.00063-21

• Leonard SP, Powell JE, Perutka J, Geng P, Heckmann LC, Horak RD, Davies BW, Ellington AD, Barrick JE, Moran NA. 2020. Engineered symbionts activate honey bee immunity and limit pathogens. Science 367: 573-576. doi: 10.1126/science.aax9039

• Zheng H, Perreau J, Powell JE, Han B, Zhang Z, Kwong WK, Tringe SG, Moran NA. 2019. Division of labor in honey bee gut microbiota for plant polysaccharide digestion. Proc Natl Acad Sci U S A. 116: 25909-25916. doi: 10.1073/pnas.1916224116

• Raymann K, Coon KL, Shaffer Z, Salisbury S, Moran NA. 2018. Pathogenicity of Serratia marcescens Strains in Honey Bees. MBio. 9(5). pii: e01649-18. doi: 10.1128/mBio.01649-18.

• Motta EVS, Raymann K, Moran NA. 2018. Glyphosate perturbs the gut microbiota of honey bees. Proc Natl Acad Sci U S A. [epub ahead of print] September 24, 2018 https://doi.org/10.1073/pnas.1803880115
  

• Powell JE, Eiri D, Moran NA, Rangel J. 2018. Modulation of the honey bee queen microbiota: Effects of early social contact. PLoS One. 13(7) :e0200527. doi: 10.1371/journal.pone.0200527

• Raymann K, Moran NA. 2018. The role of the gut microbiome in health and disease of adult honey bee workers. Curr Opin Insect Sci. 26: 97-104. doi: 10.1016/j.cois.2018.02.012

• Raymann K, Motta EVS, Girard C, Riddington IM, Dinser JA, Moran NA. 2018. Imidacloprid decreases honey bee survival but does not affect the gut microbiome. Appl Environ Microbiol.84(13). pii: e00545-18. doi: 10.1128/AEM.00545-18

• Kwong WK, Steele MI, Moran NA. 2018. Genome sequences of Apibacter spp., gut symbionts of Asian honey bees. Genome Biol Evol.10: 1174-1179. doi: 10.1093/gbe/evy076.

• Mockler BK, Kwong WK, Moran NA, Koch H. 2018. Microbiome structure influences infection by the parasite Crithidia bombi in bumble bees. Appl Environ Microbiol. 2018 Jan 26. pii: AEM.02335-17. doi: 10.1128/AEM.02335-17. [Epub ahead of print]

• Raymann K, Bobay LM, Moran NA. 2017. Antibiotics reduce genetic diversity of core species in the honeybee gut microbiome. Mol Ecol. 2017 Nov 22. doi: 10.1111/mec.14434. [Epub ahead of print]

• Kwong WK, Zheng H, Moran NA. 2017. Convergent evolution of a modified, acetate-driven TCA cycle in bacteria. Nat Microbiol. 2:17067. doi: 10.1038/nmicrobiol.2017.67.

• Zheng H, Powell JE, Steele MI, Dietrich C, Moran NA. 2017. Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proc Natl Acad Sci U S A. 114: 4775-4780. doi: 10.1073/pnas.1701819114

• Raymann K, Shaffer Z, Moran NA. 2017. Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS Biol. 15(3):e2001861. doi: 10.1371/journal.pbio.2001861

• Kwong WK, Mancenido AL, Moran NA. 2017. Immune system stimulation by the native gut microbiota of honey bees. R Soc Open Sci. 4: 170003. doi.org/10.1098/rsos.170003

• Powell JE, Leonard SP, Kwong WK, Engel P, Moran NA. 2016. Genome-wide screen identifies host colonization determinants in a bacterial gut symbiont. Proc Natl Acad Sci U S A. 2016 Nov 14. pii: 201610856. [Epub ahead of print] doi: 10.1073/pnas.1610856113

• Moran NA. 2015. Genomics of the honey bee microbiome. Curr Opin Insect Sci. 10:22–28. doi: doi:10.1016/j.cois.2015.04.003

• Zheng H, Nishida A, Kwong WK, Koch H, Engel P, Steele MI, Moran NA. 2016. Metabolism of toxic sugars by strains of the bee gut symbiont Gilliamella apicola. mBio vol. 7 no. 6 e01326-16. doi: 10.1128/mBio.01326-16