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Botanophila Flies, Vectors of Epichloë Fungal Spores, Are Infected by Wolbachia

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Botanophila Flies, Vectors of Epichloë Fungal Spores, Are Infected by Wolbachia Research Collection Journal Article Botanophila flies, vectors of Epichloë fungal spores, are infected by Wolbachia Author(s): Pagel, Lydia; Bultman, Thomas L.; Górzyńska, Karolina; Lembicz, Marlena; Leuchtmann, Adrian; Sangliana, Anne; Richards, Nicola Publication Date: 2019 Permanent Link: https://doi.org/10.3929/ethz-b-000328708 Originally published in: Mycology 10(1), http://doi.org/10.1080/21501203.2018.1515119 Rights / License: Creative Commons Attribution 4.0 International This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library Mycology An International Journal on Fungal Biology ISSN: 2150-1203 (Print) 2150-1211 (Online) Journal homepage: https://www.tandfonline.com/loi/tmyc20 Botanophila flies, vectors of Epichloë fungal spores, are infected by Wolbachia Lydia Pagel, Thomas Bultman, Karolina Górzyńska, Marlena Lembicz, Adrian Leuchtmann, Anne Sangliana & Nicola Richards To cite this article: Lydia Pagel, Thomas Bultman, Karolina Górzyńska, Marlena Lembicz, Adrian Leuchtmann, Anne Sangliana & Nicola Richards (2019) Botanophila flies, vectors of Epichloë fungal spores, are infected by Wolbachia, Mycology, 10:1, 1-5, DOI: 10.1080/21501203.2018.1515119 To link to this article: https://doi.org/10.1080/21501203.2018.1515119 © 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. Published online: 08 Sep 2018. Submit your article to this journal Article views: 175 View Crossmark data Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=tmyc20 MYCOLOGY 2019, VOL. 10, NO. 1, 1–5 https://doi.org/10.1080/21501203.2018.1515119 Botanophila flies, vectors of Epichloë fungal spores, are infected by Wolbachia Lydia Pagela, Thomas Bultman*a, Karolina Górzyńskab, Marlena Lembiczb, Adrian Leuchtmannc, Anne Sanglianaa and Nicola Richardsd aBiology Department, Hope College, Holland, MI, USA; bDepartment of Plant Taxonomy, A. Mickiewicz University, Poznan, Poland; cInstitute of Integrative Biology, ETH Zurich, Zurich, Switzerland; dBiocontrol & Biosecurity, AgResearch, Lincoln Science Centre, Lincoln, Canterbury, New Zealand ABSTRACT ARTICLE HISTORY Epichloë fungi are endophytes within grasses that can form stromata on culms of their hosts. Received 25 June 2018 Botanophila flies visit the stromata for egg laying and in the process can vector spermatial spores, Accepted 19 August 2018 thereby cross fertilising the fungus. Following egg hatch, larval flies consume fungal tissue and KEYWORDS spores. Thus, Epichloë individuals with traits that limit larval consumption could be at a selective Ascomycota; Diptera; fungal advantage. We assessed Botanophila fly larvae from sites within the United States and Europe for endophyte; sexual parasite infection by the bacterial sexual parasite Wolbachia through amplification of the Wolbachia surface protein gene (wsp). Nearly 70% of fly larvae in our samples were infected by Wolbachia. This is the first record of infection by Wolbachia within Botanophila and could have far reaching effects on not only the fly host, but also the Epichloë fungi upon which Botanophila feeds as well as the grass host within which the fungi live. For example, infection by Wolbachia could limit consumption of Epichloë spores by Botanophila larvae if the bacteria promoted premature larval death. Introduction An enigma regarding mutualisms is their observed stability (Bronstein 2001, 2009). What prevents one party The relationship between Botanophila flies and from over-exploiting the other and the mutualism dissol- Epichloë fungi has long been a subject of interest to ving into an antagonistic interaction? For yuccas this may researchers due to the fly’s peculiar pollinator-like be selective abortion of ovaries that receive numerous behaviour. This quasi-pollination interaction closely yucca moth eggs (Pelmyr and Hurth 1994). For Epichloë resembles that observed between some insects and the mechanism is not known, but a previous study their angiosperm hosts, such as the fig-fig wasp and showed larval death rate increased with Botanophila yucca-yucca moth interaction, but is uncommon egg density on a stroma (Bultman et al. 2000). among fungi (Bultman 1995). Flies find stromata by During past investigations, researchers observed tracking volatiles the fungi produce (Steinebrunner that male Botanophila flies are rare and that a sub- et al. 2008a.). Once they locate a stroma, they alight stantial proportion (as much as 30%) of eggs can be and feed on perithecial tissues containing spermatial non-viable at some sites (Górzyńska et al. 2011; spores, and then oviposit and defecate along the Lembicz et al. 2013). This could indicate the presence whole length of the stroma. Spermatia pass through of a sexual parasite in fly populations. As with fruit the gut of the fly unharmed and are deposited on abortion in yucca, a sexual parasite could promote subsequent stromata the fly visits. Epichloë fungi are stability of the interacting mutualists by limiting self-incompatible and thus, flies cross-fertilise fungi exploitation of Epichloë by Botanophila. One com- as they vector spermatia (Bultman et al. 1998). Fly mon type of sexual parasite in insects is Wolbachia, larvae remain on fungal stromata until just before a genus of rickettsiae bacteria that lives within the pupation and feed on the products of cross fertilisa- reproductive tissues of its hosts (Werren 1997). In tion; the ascospores (Bultman et al. 1995). general, these bacteria are thought to be reproduc- Botanophila flies appear to be the main vectors of tive parasites that may cause a variety of phenotypic spores although other vectors, like slugs, have been changes in their hosts including cytoplasmic implicated (Rao et al. 2012; Hoffman and Rao 2014). CONTACT Thomas Bultman [email protected] *Present affiliation for Thomas Bultman is Franklin Mountains State Park, El Paso, TX, USA. © 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Published online 08 Sep 2018 2 L. PAGEL ET AL. incompatibility, parthenogenesis induction, feminisa- electrophoresis in 1.5% agarose gels and visualised by tion, and male-killing (Werren et al. 2008). SYBR®Green I (Molecular Probes, Eugene, OR, USA) Wolbachia occurs in a vast number of arthropod under UV light to check for proper amplification. PCR species as well as filarial nematodes and may be one amplicons were then purified with Wizard® SV Gel and of the most abundant intracellular genera of bacteria PCR Clean-Up System (Promega Corp., Madison, WI, known (Fialho and Stevens 2000; Cordaux et al. 2001; USA) according to manufacturer’s instructions. Weeks and Breeuwer 2001; Goodacre et al. 2006), yet Sequencing reactions were performed in 10 µL volumes it has not been documented in Botanophila flies. If a using a BigDye Terminator Cycle Sequencing kit (PE cytoplasmic incompatibility or male-killing strain of Applied Biosystems) with recommended PCR condi- Wolbachia were to occur in Botanophila, it could tions. Both strands of the product were sequenced have important implications for the interaction and were separated on a capillary 3130 Genetic between the flies and Epichloë, such as reducing Analyzer (Applied Biosystems). Sequences were identi- larval feeding on the fungus. The purpose of our fied to species using a nucleotide BLAST (Altschul et al. study was to screen Botanophila flies for Wolbachia 1990) to compare them to reference sequences of infection. Botanophila distinguished by Leuchtmann (2007)and Leuchtmann and Michelsen (2016). Negative controls withoutDNAwererunwitheachtesttoensurethe Materials and methods absence of contamination in reagents. Sample collection and DNA extraction We collected Epichloë-infected grass stems contain- Assessing Wolbachia infection ing stroma with Botanophila brood chambers from We analysed total DNA extracted from larvae for the sites in both Europe and the USA in May and June presence of Wolbachia by using PCR to amplify the and stored them in 80% ethanol for transportation. Wolbachia surface protein gene (wsp) with primers The larvae were removed by cutting open the brood wsp-F1 (GTCCAATARSTGATGARGAAAC) and wsp-R1 chambers and using forceps to transfer larvae to vials (CYGCACCAAYAGYRCTRTAAA) (Baldo et al. 2006). of 80% ethanol for storage until DNA extraction Reactions were performed in 10 µl volumes contain- could be performed. DNA extraction was performed ing 5 µl Taq PCR Master Mix (Qiagen Inc., Valencia, on single larvae using the DNeasy Blood and Tissue CA, USA). Amplification was conducted in an Kit (Qiagen Inc., Valencia, CA, USA) according to Eppendorf Pro thermocycler using a program with ’ manufacturer s instructions, but using a final elution the following parameters: 2 min at 95°C; 30 s at 95°C, volume of 50 µL. 45 s at 53°C, and 1 min at 72°C, repeated 35 times; 6 min at 72°C; hold at 4°C. Amplicons were separated using gel electrophoresis in a 1.5% agarose gel and Identifying Botanophila species visualised by SYBR®Green I (Molecular Probes, To determine the species of Botanophila larvae we Eugene, OR, USA) under UV light to determine pre- amplified the mitochondrial
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