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Microbial Symbionts Shape the Sterol Profile of the Xylem-Feeding Woodwasp, Sirex noctilio

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Abstract

The symbiotic fungus Amylostereum areolatum is essential for growth and development of larvae of the invasive woodwasp, Sirex noctilio. In the nutrient poor xylem of pine trees, upon which Sirex feeds, it is unknown whether Amylostereum facilitates survival directly through consumption (mycetophagy) and/or indirectly through digestion of recalcitrant plant polymers (external rumen hypothesis). We tested these alternative hypotheses for Amylostereum involvement in Sirex foraging using the innate dependency of all insects on dietary sources of sterol and the unique sterols indicative of fungi and plants. We tested alternative hypotheses by using GC-MS to quantify concentrations of free and bound sterol pools from multiple life-stages of Sirex, food sources, and waste products in red pine (Pinus resinosa). Cholesterol was the primary sterol found in all life-stages of Sirex. However, cholesterol was not found in significant quantities in either plant or fungal resources. Ergosterol was the most prevalent sterol in Amylostereum but was not detectable in either wood or insect tissue (<0.001 μg/g). Phytosterols were ubiquitous in both pine xylem and Sirex. Therefore, dealkylation of phytosterols (sitosterol and campesterol) is the most likely pathway to meet dietary demand for cholesterol in Sirex. Ergosterol concentrations from fungal-infested wood demonstrated low fungal biomass, which suggests mycetophagy is not the primary source of sterol or bulk nutrition for Sirex. Our findings suggest there is a potentially greater importance for fungal enzymes, including the external digestion of recalcitrant plant polymers (e.g., lignin and cellulose), shaping this insect-fungal symbiosis.

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Acknowledgments

Members of the Gruner and Barbosa labs, the Washington Plant Insect Group, P. Chaverri, R. St. Leger, M. Raupp, I. Forseth for constructive comments; Jake Bodart, Pat Tauber, Miriam and Jim Dunham, Abby Thompson, Pennsylvania DCNR Dept. of State Parks, and USDA-APHIS for permitting and sample collection; Dr. A. Adams for type fungal specimens and the United States Forest Service, Sigma Xi, The University of Maryland Gahan Fellowship and The National Explorers Club (Washington) for financial support. Special thanks to two helpful reviewers who significantly improved this manuscript.

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  1. Department of Entomology, University of Maryland, College Park, MD, 20742, USA

    Brian M. Thompson & Daniel S. Gruner

  2. Department of Biology, Canisius College, 2001 Main St., Buffalo, NY, 14208, USA

    Robert J. Grebenok

  3. Department of Entomology, Texas A&M University, TAMU 2475, College Station, TX, 77843, USA

    Spencer T. Behmer

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Thompson, B.M., Grebenok, R.J., Behmer, S.T. et al. Microbial Symbionts Shape the Sterol Profile of the Xylem-Feeding Woodwasp, Sirex noctilio . J Chem Ecol 39, 129–139 (2013). https://doi.org/10.1007/s10886-012-0222-7

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