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Bacteria contribute to plant secondary compound degradation in a generalist herbivore system

View ORCID ProfileCharlotte B. Francoeur, Lily Khadempour, Rolando D. Moreira-Soto, Kirsten Gotting, Adam J. Book, Adrian A. Pinto-Tomás, Ken Keefover-Ring, Cameron R. Currie
doi: https://doi.org/10.1101/865212
Charlotte B. Francoeur
aDepartment of Bacteriology, University of Wisconsin – Madison, Madison, Wisconsin, USA
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  • ORCID record for Charlotte B. Francoeur
Lily Khadempour
bDepartment of Biology, California State University, Northridge, Northridge, California, USA
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Rolando D. Moreira-Soto
cSección de Entomología Medica, Departamento de Parasitología, Facultad de Microbiología, Universidad de Costa Rica, San José, Costa Rica
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Kirsten Gotting
aDepartment of Bacteriology, University of Wisconsin – Madison, Madison, Wisconsin, USA
dLaboratory of Genetics, University of Wisconsin – Madison, Madison, Wisconsin, USA
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Adam J. Book
eExact Sciences, Madison, Wisconsin, USA
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Adrian A. Pinto-Tomás
fCentro de Investigación en Estructuras Microscópicas, Universidad de Costa Rica, San José, Costa Rica
gDepartamento de Bioquímica, Facultad de Medicina, Universidad de Costa Rica, San José, Costa Rica
hCentro de Investigación en Biología Celular y Molecular, Universidad de Costa Rica, San José, Costa Rica
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Ken Keefover-Ring
iDepartment of Botany and Geography, University of Wisconsin – Madison, Madison, Wisconsin, USA
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Cameron R. Currie
aDepartment of Bacteriology, University of Wisconsin – Madison, Madison, Wisconsin, USA
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  • For correspondence: currie@bact.wisc.edu
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Abstract

Insects and plants engage in a multitude of complex interactions. In antagonistic cases, such as herbivory, insects often specialize on a few closely related plant species to overcome physical and chemical defences. More rarely, herbivorous insects can feed on a range of plant species. Leaf-cutter ants are generalist herbivores that forage from a variety of plant species, which the ants bring to the fungus they farm, Leucoagaricus sp. While we show that anti-herbivory plant compounds can harm Leucoagaricus sp. in vitro, it is unknown how the ants’ fungus gardens are able to incorporate a large diversity of plants with differing plant chemistry. Here, we investigate the fungus garden bacterial community’s ability to degrade plant secondary compounds. We cultured fungus garden bacteria, sequenced the genomes of 42 isolates, and found genes involved in plant secondary compound degradation, including monoterpene epsilon-lactone hydrolase. Some of these genes show in situ expression in metatranscriptomes, such as limonene-1,2-monooxygenase. A majority of the bacterial isolates grew unhindered in the presence of plant secondary compounds and, using GC-MS, isolates from the genera Pseudomonas, Klebsiella, Enterobacter, and Bacillus could degrade either α-pinene, β-caryophyllene or linalool.

Additionally, using a headspace sampler, sub-colonies of fungus gardens reduced α-pinene and linalool over a 36-hour period, while Leucoagaricus sp. strains alone only reduced linalool, not α-pinene. Our study provides evidence that Leucoagaricus sp. has a variable ability to tolerate and degrade plant secondary compounds, indicating that it may depend on bacteria to detoxify the diversity of plant chemistry the system encounters.

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  • https://github.com/cfrancoeur/PSC

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted December 05, 2019.
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Bacteria contribute to plant secondary compound degradation in a generalist herbivore system
Charlotte B. Francoeur, Lily Khadempour, Rolando D. Moreira-Soto, Kirsten Gotting, Adam J. Book, Adrian A. Pinto-Tomás, Ken Keefover-Ring, Cameron R. Currie
bioRxiv 865212; doi: https://doi.org/10.1101/865212
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Bacteria contribute to plant secondary compound degradation in a generalist herbivore system
Charlotte B. Francoeur, Lily Khadempour, Rolando D. Moreira-Soto, Kirsten Gotting, Adam J. Book, Adrian A. Pinto-Tomás, Ken Keefover-Ring, Cameron R. Currie
bioRxiv 865212; doi: https://doi.org/10.1101/865212

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