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A common antifungal defense strategy in Cryptocercus woodroaches and termites

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Abstract

We identified and characterized Gram-negative bacteria binding proteins (GNBPs) and their predicted antifungal activity in the woodroach Cryptocercus punctulatus. C. punctulatus is likely to share many characteristics with the subsocial ancestor of the Isoptera, including allogrooming, which facilitated the evolution of termite sociality. Based on a phylogenetic analysis, an ancestral GNBP with an intact β-1,3-glucanase active site appears to have duplicated in a common ancestor of subsocial Cryptocercus woodroaches and termites. In termites, the secreted β-1,3-glucanase activity of GNBPs provides important prophylactic protection from fungal pathogens such as Metarhizium anisopliae, which can evade the immune system after entering the insect. Here, we identify β-1,3-glucanase activity on the cuticular surface of C. punctulatus that originates from the salivary gland and is likely spread by allogrooming. Cuticular washes have antifungal activity against M. anisopliae conidia that is suppressed by an inhibitor (GDL) of termite GNBP β-1,3-glucanase activity. C. punctulatus nymphs that are treated with GDL and subsequently exposed to M. anisopliae conidia show significantly greater mortality than the untreated nymphs exposed to conidia. A molecular evolutionary analysis of GNBPs in two species of Parcoblatta, Periplaneta americana, C. punctulatus and representative termites indicates that selection-directed change in a glycosylphosphatidylinositol (GPI) anchor region. Modification of the GPI anchor region may have been instrumental in the evolution of an antifungal defense strategy that depends on the external secretion of GNBPs from the salivary gland and their dissemination by grooming. This strategy may have helped compensate for the vulnerability of a subsocial woodroach-like ancestor to fungal disease that results from prolonged development with a thin cuticle and facilitated the transition to termite eusociality.

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Acknowledgments

We thank T. Russ for assistance in identifying and sequencing GNBP cDNA in P. americana.

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  1. Department of Biological Sciences, Towson University, 341 Smith Hall, 8000 York Rd., Towson, MD, 21252, USA

    M. S. Bulmer, D. Denier, J. Velenovsky & C. Hamilton

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  1. M. S. Bulmer
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Correspondence to M. S. Bulmer.

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Bulmer, M.S., Denier, D., Velenovsky, J. et al. A common antifungal defense strategy in Cryptocercus woodroaches and termites. Insect. Soc. 59, 469–478 (2012). https://doi.org/10.1007/s00040-012-0241-y

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