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Ecological Succession in the Honey Bee Gut: Shift in Lactobacillus Strain Dominance During Early Adult Development

  • Host Microbe Interactions
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Abstract

In many vertebrates, social interactions and nutrition can affect the colonization of gut symbionts across generations. In the highly social honey bee, it is unknown to what extent the hive environment and older worker individuals contribute to the generational transmission of core gut bacteria. We used high-throughput sequencing to investigate the effect of nest materials and social contact on the colonization and succession of core hindgut microbiota in workers. With only brief exposure to hive materials following natural eclosion, gut bacterial communities at 3 and 7 days contained phylotypes typically found in the guts of mature adults regardless of treatment. Continuous exposure to nest materials or direct social interactions with mature adults did not affect the diversity or abundance of gut bacterial communities at the scale examined. Similarly, a common pollen supplement fed by beekeepers during pollen dearth had no effect. A consideration of unique OTUs revealed extensive microbial succession independent of treatment. The dominant Lactobacillus strain at 3 days was largely replaced by a different strain at day 7, revealing the colonization signature of a pioneer species. Similar but less pronounced patterns were evident in less abundant OTU’s, many of which may influence community succession via alteration of the gut environment. Our results indicate that the process of bacterial community colonization in the hindgut is resilient to changes in the nutritional, hive, and social environment. Greater taxonomic resolution is needed to accurately resolve questions of ecological succession and typical proportional variation within and between core members of the gut bacterial community.

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Acknowledgments

The authors acknowledge Jay Evans and Randy Oliver for comments on a previous version of the manuscript and the members of the Anderson lab for technical assistance. The corresponding author thanks Belynda Starr, Ariel Calypso, and Isaak Edward for their valuable input. We thank the Bio5 Institute at the University of Arizona Genomics Core for the generation of 454 amplicons. The USDA is an equal opportunity employer and provider.

Author Contributions

PAPR, BMM, and KEA conceived and designed research, PAPR, PM, and KEA performed research, PAPR, VCH, and KEA analyzed data, and KEA wrote the paper.

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    Authors and Affiliations

    1. USDA-ARS Carl Hayden Bee Research Center, 2000 E. Allen Rd, Tucson, AZ, 85719, USA

      Kirk E. Anderson, Brendon M. Mott & Vanessa Corby-Harris

    2. Graduate Interdisciplinary Program in Entomology and Insect Science, University of Arizona, Tucson, AZ, 85721, USA

      Kirk E. Anderson, Pedro A. P. Rodrigues, Patrick Maes & Vanessa Corby-Harris

    3. Department of Entomology, University of Arizona, Tucson, AZ, 85721, USA

      Kirk E. Anderson, Pedro A. P. Rodrigues, Patrick Maes & Vanessa Corby-Harris

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    Correspondence to Kirk E. Anderson.

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    The first authorship is shared between Kirk E. Anderson and Pedro A. P. Rodrigues

    Kirk E. Anderson and Pedro A. P. Rodrigues contributed equally to this work.

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    Anderson, K.E., Rodrigues, P.A.P., Mott, B.M. et al. Ecological Succession in the Honey Bee Gut: Shift in Lactobacillus Strain Dominance During Early Adult Development. Microb Ecol 71, 1008–1019 (2016). https://doi.org/10.1007/s00248-015-0716-2

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