Moran Lab

About The Moran Lab

The Moran Lab's long-term interests are in the biology of symbiosis, particularly that between multicellular hosts and microbes. Symbioses are central in the evolution of complexity, have evolved many times and are critical to the lifestyles of many animals and plants and also to whole ecosystems, in which symbiotic organisms are key players. The primary reason that symbiosis research is suddenly active, after decades at the margins of mainstream biology, is that DNA technology and genomics give us enormous new ability to discover symbiont diversity, and more significantly, to reveal how microbial metabolic capabilities contribute to the functioning of hosts and biological communities.

Examples of the Moran Lab's ongoing projects include:

• Phylogenetic, genomic and experimental studies of previously unstudied insect symbioses.
• Study of aphid genes underlying carotenoid biosynthesis.
• Experiments on the interdependent metabolic functioning of Buchnera and aphids.
• Reconstruction of the evolutionary changes in genomes of bacterial symbionts.
• Experimental investigations of facultative symbionts of aphids.
• Studies of the functions, evolution and ecology of the bacteria living in the guts of honey bees and bumble bees.

2023 Research

• Li Z, Xue AZ, Maeda GP, Li Y, Nabity PD, Moran NA. Phylloxera and aphids show distinct features of genome evolution despite similar reproductive modes. Mol Biol Evol. 2023 Dec 9:msad271. Epub ahead of print. PMID: 38069672.

• Motta EVS, Moran NA. The honeybee microbiota and its impact on health and disease. Nat Rev Microbiol. 2023 Dec 4. Epub ahead of print. PMID: 38049554.

• Elston KM, Phillips LE, Leonard SP, Young E, Holley JC, Ahsanullah T, McReynolds B, Moran NA, Barrick JE. Correction to: The Pathfinder plasmid toolkit for genetically engineering newly isolated bacteria enables the study of Drosophila-colonizing Orbaceae. ISME Commun. 2023 Nov 16;3(1):119. Erratum for: ISME Commun. 2023 May 24;3(1):49. PMID: 37974005; PMCID: PMC10654726.

• Villabona N, Moran N, Hammer T, Reyes A. Conserved, yet disruption-prone, gut microbiomes in neotropical bumblebees. mSphere. 2023 Oct 19:e0013923. Epub ahead of print. PMID: 37855643.

• Lariviere PJ, Ashraf AHMZ, Leonard SP, Miller LG, Moran NA, Barrick JE. Single-step genome engineering in the bee gut symbiont Snodgrassella alvi. bioRxiv [Preprint]. 2023 Sep 20:2023.09.19.558440. PMID: 37786689; PMCID: PMC10541602.

• Huang Q, Lariviere PJ, Powell JE, Moran NA. Engineered gut symbiont inhibits microsporidian parasite and improves honey bee survival. Proc Natl Acad Sci U S A. 2023 Jun 20;120(25):e2220922120. Epub 2023 Jun 12. PMID: 37307477; PMCID: PMC10288570.

• Elston KM, Phillips LE, Leonard SP, Young E, Holley JC, Ahsanullah T, McReynolds B, Moran NA, Barrick JE. The Pathfinder plasmid toolkit for genetically engineering newly isolated bacteria enables the study of Drosophila- colonizing Orbaceae. ISME Commun. 2023 May 24;3(1):49. PMID: 37225918; PMCID: PMC10209150.

• Motta EVS, Arnott RLW, Moran NA. Caffeine Consumption Helps Honey Bees Fight a Bacterial Pathogen. Microbiol Spectr. 2023 May 22:e0052023. Epub ahead of print. PMID: 37212661.

• Powell JE, Lau P, Rangel J, Arnott R, De Jong T, Moran NA. The microbiome and gene expression of honey bee workers are affected by a diet containing pollen substitutes. PLoS One. 2023 May 19;18(5):e0286070. PMID: 37205696; PMCID: PMC10198554.

• Elston KM, Phillips LE, Leonard SP, Young E, Holley JC, Ahsanullah T, McReynolds B, Moran NA, Barrick JE. The Pathfinder plasmid toolkit for genetically engineering newly isolated bacteria enables the study of Drosophila-colonizing.... bioRxiv [Preprint]. 2023 Feb 16:2023.02.15.528778. Update in: ISME Commun. 2023 May 24;3(1):49. PMID: 36824770; PMCID: PMC9949093.

• Motta EVS, Moran NA. The effects of glyphosate, pure or in herbicide formulation, on bumble bees and their gut microbial communities. Sci Total Environ. 2023 May 10;872:162102. Epub 2023 Feb 9. PMID: 36764553.

• Miyake CY, Lay EJ, Soler-Alfonso C, Glinton KE, Houck KM, Tosur M, Moran NE, Stephens SB, Scaglia F, Howard TS, Kim JJ, Pham TD, Valdes SO, Li N, Murali CN, Zhang L, Kava M, Yim D, Beach C, Webster G, Liberman L, Janson CM, Kannankeril PJ, Baxter S, Singer-Berk M, Wood J, Mackenzie SJ, Sacher M, Ghaloul-Gonzalez L, Pedroza C, Morris SA, Ehsan SA, Azamian MS, Lalani SR. Natural history of TANGO2 deficiency disorder: Baseline assessment of 73 patients. Genet Med. 2023 Apr;25(4):100352. Epub 2022 Dec 5. PMID: 36473599.

2022 Research

• Motta EVS, Gage A, Smith TE, Blake KJ, Kwong WK, Riddington IM, Moran N. Host-microbiome metabolism of a plant toxin in bees. Elife. 2022 Dec 6;11:e82595. PMID: 36472498; PMCID: PMC9897726.

• Hammer TJ, Easton-Calabria A, Moran NA. Microbiome assembly and maintenance across the lifespan of bumble bee workers. Mol Ecol. 2022 Nov 5. Epub ahead of print. PMID: 36333950.

• Li Z, Li Y, Xue AZ, Dang V, Holmes VR, Johnston JS, Barrick JE, Moran NA. The Genomic Basis of Evolutionary Novelties in a Leafhopper. Mol Biol Evol. 2022 Sep 1;39(9):msac184. PMID: 36026509; PMCID: PMC9450646.

• Holley JC, Jackson MN, Pham AT, Hatcher SC, Moran NA. Carpenter Bees (Xylocopa) Harbor a Distinctive Gut Microbiome Related to That of Honey Bees and Bumble Bees. Appl Environ Microbiol. 2022 Jul 12;88(13):e0020322. Epub 2022 Jun 27. PMID: 35758673; PMCID: PMC9275229.

• TE Smith, L Yi, J Perreau and NA Moran. Elucidation of host and symbiont contributions to peptidoglycan metabolism based on comparative genomics of eight aphid subfamilies and their Buchnera. PLoS genetics 18 (5), e1010195. May 6, 2022.

• EVS Motta, JE Powell, SP Leonard and NA Moran. Prospects for probiotics in social bees. Philosophical Transactions of the Royal Society B 377 (1853), 20210156. May 2, 2022.

• Y Li, SP Leonard, JE Powell and NA Moran. Species divergence in gut-restricted bacteria of social bees. Proceedings of the National Academy of Sciences 119 (18), e2115013119. Apr 25, 2022

• A Nakabachi and NA Moran. Extreme Polyploidy of Carsonella, an Organelle-Like Bacterium with a Drastically Reduced Genome. Microbiology Spectrum, e00350-22. Apr 18, 2022.

• EVS Motta, JE Powell and NA Moran. Glyphosate induces immune dysregulation in honey bees. Animal microbiome 4 (1), 1-14. Feb 22, 2022.

• M Blaxter, JM Archibald, AK Childers, JA Coddington, KA Crandall, ... NA Moran ... Why sequence all eukaryotes?. Proceedings of the National Academy of Sciences 119 (4). Jan 18, 2022

• J Perreau and NA Moran. Genetic innovations in animal–microbe symbioses. Nature Reviews Genetics 23 (1), 23-39. 2022.

2021 Research

• NA Moran. Microbe Profile: Buchnera aphidicola: ancient aphid accomplice and endosymbiont exemplar. Microbiology 167 (12), 001127

• TE Smith, M Lee, MD Person, D Hesek, S Mobashery and NA Moran. Horizontal-Acquisition of a Promiscuous Peptidoglycan-Recycling Enzyme Enables Aphids To Influence Symbiont Cell Wall Metabolism. Mbio 12 (6), e02636-2.

• TJ Hammer and NA Moran. 2021. The gut microbiota of bumblebees. Insectes Soc. 68 (2-3). doi: 10.1007/s00040-021-00837-1

• MI Steele, EVS Motta, T Gattu, D Martinez and NA Moran. 2021. The gut microbiota protects bees from invasion by a bacterial pathogen. Microbiol Spectr. 2021 Sep 15;e0039421. doi: 10.1128/Spectrum.00394-21. [Online ahead of print.]

• J Perreau, B Zhang, GP Maeda, M Kirkpatrick and NA Moran. 2021. Strong within-host selection in a maternally inherited obligate symbiont: Buchnera and aphids. Proc Natl Acad Sci U S A. 118(35):e2102467118. doi: 10.1073/pnas.2102467118

• J Perreau and NA Moran. 2021. Genetic innovations in animal-microbe symbioses. Nat Rev Genet. 2021 Aug 13. doi: 10.1038/s41576-021-00395-z. [Online ahead of print]

• JE Powell, Z Carver, SP Leonard and NA Moran. 2021. Field-realistic tylosin exposure impacts honey bee microbiota and pathogen susceptibility, which is ameliorated by native gut probiotics. Microbiol Spectr. 9(1):e0010321. doi: 10.1128/Spectrum.00103-21.

• AES Cerqueira, TJ Hammer, NA Moran, WC Santana, MCM Kasuya and CC da Silva. 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. 

• MI Steele and NA Moran. 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

• MJ Schepers, JN Yelland, NA Moran and DW Taylor. 2021. Isolation of the Buchnera aphidicola flagellum basal body complexes from the Buchnera membrane. PLoS One 16(5):e0245710. doi: 10.1371/journal.pone.0245710

• J Perreau, DJ Patel, H Anderson, GP Maeda, KM Elston, JE Barrick and NA Moran. 2021. Vertical transmission at the pathogen-symbiont interface: Serratia symbiotica and aphids. mBio 12(2):e00359-21. doi: 10.1128/mBio.00359-21

• TJ Busby, CR Miller, NA Moran and JT Van Leuven. Global composition of the bacteriophage community in honeybees. bioRxiv. 2021.

• TJ Hammer, E Le and NA Moran. 2021. Thermal niches of specialized gut symbionts: the case of social bees. Proc Biol Sci. 288(1944): 20201480. doi: 10.1098/rspb.2020.1480

2020 Research

• KM Elston, J Perreau, GP Maeda, NA Moran and JE Barrick. 2020. Engineering a culturable Serratia symbiotica strain for aphid paratransgenesis. Appl Environ Microbiol. 87(4):e02245-20. doi: 10.1128/AEM.02245-20.

• C Rispe, F Legeai, PD Nabity, R Fernández, AK Arora, P Baa-Puyoulet, ... NA Moran. The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest. BMC biology 18 (1), 1-25. 2021.

• RD Horak, SP Leonard and NA Moran. 2020. Symbionts shape host innate immunity in honeybees. Proc Biol Sci. 287(1933):20201184. doi: 10.1098/rspb.2020.1184.

• EVS Motta and NA Moran. 2020. Impact of Glyphosate on the Honey Bee Gut Microbiota: Effects of Intensity, Duration, and Timing of Exposure. mSystems 5(4):e00268-20. doi: 10.1128/mSystems.00268-20.

• EVS Motta, M Mak, TK De Jong, JE Powell, A O'Donnell, KJ Suhr, IM Riddington and NA Moran. 2020. Oral and topical exposure to glyphosate in herbicide formulation impact the gut microbiota and survival rates of honey bees. Appl Environ Microbiol. 86(18):e01150-20. doi: 10.1128/AEM.01150-20.

• Y Li, B Zhang and NA Moran. 2020. The aphid X chromosome is a dangerous place for functionally important genes: Diverse evolution of Hemipteran genomes based on chromosome-level assemblies. Mol Biol Evol. 37: 2357-2368. doi: 10.1093/molbev/msaa095.

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

• TE Smith and NA Moran. 2020. Coordination of host and symbiont gene expression reveals a metabolic tug-of-war between aphids and Buchnera. Proc Natl Acad Sci U S A. 117: 2113-2121. doi: 10.1073/pnas.1916748117.