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Environments and Hosts Structure the Bacterial Microbiomes of Fungus-Gardening Ants and their Symbiotic Fungus Gardens

  • Host Microbe Interactions
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Abstract 

The fungus gardening-ant system is considered a complex, multi-tiered symbiosis, as it is composed of ants, their fungus, and microorganisms associated with either ants or fungus. We examine the bacterial microbiome of Trachymyrmex septentrionalis and Mycetomoellerius turrifex ants and their symbiotic fungus gardens, using 16S rRNA Illumina sequencing, over a region spanning approximately 350 km (east and central Texas). Typically, microorganisms can be acquired from a parent colony (vertical transmission) or from the environment (horizontal transmission). Because the symbiosis is characterized by co-dispersal of the ants and fungus, elements of both ant and fungus garden microbiome could be characterized by vertical transmission. The goals of this study were to explore how both the ant and fungus garden bacterial microbiome are acquired. The main findings were that different mechanisms appear to explain the structure the microbiomes of ants and their symbiotic fungus gardens. Ant associated microbiomes had a strong host ant signature, which could be indicative of vertical inheritance of the ant associated bacterial microbiome or an unknown mechanism of active uptake or screening. On the other hand, the bacterial microbiome of the fungus garden was more complex in that some bacterial taxa appear to be structured by the ant host species, whereas others by fungal lineage or the environment (geographic region). Thus bacteria in fungus gardens appear to be acquired both horizontally and vertically.

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Data Availability

Raw microbiome sequences for all samples have been uploaded to NCBI under the BioProject PRJNA789907. Fungal ITS sequences from all applicable fungal garden samples have been uploaded to GenBank, with accession numbers found in Table 1. Our Qiime2 pipeline, along with sample R script used during the post-processing analysis, can be found at https://github.com/bsbringhurst/TS-and-MT-Microbiome-Files. The resulting OTU table output by our Qiime2 pipeline can be found in the DRYAD Digital Repository at https://doi.org/10.5061/dryad.7wm37pvv1.

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Acknowledgements

We thank two anonymous reviewers, Joshua Banta, Neil Ford, and Kate Hertweck, for constructive criticisms on earlier drafts of this manuscript. Ant collections and fungal genotyping were assisted by Leighanna Mindt and Joseph Luiso. We also thank the participants of the Texas Ecolab program for allowing access to privately owned lands throughout Texas.

Funding

Funding was provided by the National Science Foundation IOS-1552822 to JNS and DEB-1354629 to KK). Additional funding and logistic support was provided by Texas Ecolab (https://texasecolabprogram.org/).

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  1. Blake Bringhurst and Mattea Allert contributed equally to this work.

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  1. Department of Biology, University of Texas at Tyler, 3900 University Blvd, Tyler, TX, 75799, USA

    Blake Bringhurst, Mattea Allert, Matthew Greenwold, Katrin Kellner & Jon N. Seal

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Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Mattea Allert, Blake Bringhurst, Matthew Greenwold, Katrin Kellner, and Jon Seal. The manuscript was written by Mattea Allert, Blake Bringhurst, and Jon Seal. All authors read and approved the final manuscript.

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Correspondence to Jon N. Seal.

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Bringhurst, B., Allert, M., Greenwold, M. et al. Environments and Hosts Structure the Bacterial Microbiomes of Fungus-Gardening Ants and their Symbiotic Fungus Gardens. Microb Ecol 86, 1374–1392 (2023). https://doi.org/10.1007/s00248-022-02138-x

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