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The First Entomophthoralean Killing Millipedes, Arthrophaga Myriapodina N. Gen. N. Sp., Causes Climbing Before Host Death

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The First Entomophthoralean Killing Millipedes, Arthrophaga Myriapodina N. Gen. N. Sp., Causes Climbing Before Host Death Journal of Invertebrate Pathology 149 (2017) 135–140 Contents lists available at ScienceDirect Journal of Invertebrate Pathology journal homepage: www.elsevier.com/locate/jip The first entomophthoralean killing millipedes, Arthrophaga myriapodina n. MARK gen. n. sp., causes climbing before host death ⁎ Kathie T. Hodgea, , Ann E. Hajekb, Andrii Gryganskyic a Section of Plant Pathology & Plant-Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, NY 14853, USA b Department of Entomology, Cornell University, Ithaca, NY 14853, USA c Department of Biology, Duke University, Durham, NC 27708, USA ARTICLE INFO ABSTRACT Keywords: A new species and genus of entomophthoralean fungus, Arthrophaga myriapodina kills polydesmid millipedes. Entomophthorales This species was first seen over a century ago but never described. It is the first millipede pathogen known from Apheloria the order Entomophthorales, species of which are best known as pathogens of a wide diversity of insects. The Myriapoda fungus induces pre-death climbing behavior in its hosts, enabling the fungus to broadcast its forcibly-discharged Pathogen conidia from a high vantage, which presumably increases the fitness of the fungus. Study of herbarium speci- Behavioral manipulation mens and photographic discoveries on the internet suggest the fungus occurs widely in eastern North America. 1. Introduction Phylogenetic studies reveal this lineage is ancient and evolutionarily distinct from other “zygomycete” groups. It is now placed in the fungal In the forests around Ithaca, New York, cadavers of the native phylum Zoopagomycota, subphylum Entomophthoromycotina millipede Apheloria virginiensis corrugata are frequently found dead in (Spatafora et al., 2016). odd places: on cement bridge abutments, on top of fence posts as high Most entomophthoralean fungi infect hosts in the Phylum as shoulder level, and on the elevated ends of fallen branches and logs Arthropoda, with the majority being insects (subphylum Hexapoda, (Fig. 1). Normally, this common millipede species is hidden in soil and Class Insecta) although a few species infect hosts in the Class leaf litter, or under or within logs on the ground (P. Marek, pers. Entognatha (e.g., Collembola; Keller and Steenberg, 1997). Others in- comm.; Eaton, 1943); living individuals do not visit the elevated and fect members of the phyla Tardigrada and Nematoda (e.g., Saikawa exposed locations where cadavers are found. The cause of death of et al., 1997). Species of the sister fungal order Neozygitales infect mites these millipedes is not apparent except during the short window of (subphylum Chelicerata) (Gryganskyi et al., 2013). Before now, no spore production, after the fungus kills its host and then erupts from entomophthoralean fungus had been reported from millipedes, in the between the body segments to produce conidia. At that time the mil- arthropod subphylum Myriapoda. In this paper we describe this milli- lipede bodies become distended, with prominent bulging interseg- pede-killing fungus for the first time, investigate its geographical range, mental zones of glassy conidiophores that forcibly discharge large and show that it was first observed in northeastern North America over conidia. Around the millipede a halo of discharged conidia may be seen a century ago. with a hand lens. Within a day of the millipede’s death, all conidia have been forcibly discharged and the structures that made them have col- 2. Methods lapsed, leaving an enigmatic husk of a millipede, or a pile of its dis- articulated, sclerotized segments. This phenomenon is typical of species 2.1. Microscopy of the fungal order Entomophthorales. Most members of the order Entomophthorales are deadly pathogens Fungal structures from fresh, dried, and alcohol-preserved speci- of insects. They infect by direct penetration through the cuticle and mens were observed and photographed in either lactic acid-cotton blue often induce behavioral changes in their hosts, which may perch in high (100 mL 85% lactic acid containing 0.025 g cotton blue), or aceto-or- places before dying (Roy et al., 2006). Presumably this behavioral cein (Humber, 2012a) using a Nikon E600 compound microscope with manipulation increases the fitness of the fungus, which in such a po- Differential Interference Contrast optics. Conidia and other structures sition can broadcast its forcibly discharged conidia over a larger area. were observed and measured in lactic acid-cotton blue; visualization ⁎ Corresponding author. E-mail addresses: [email protected] (K.T. Hodge), [email protected] (A.E. Hajek), [email protected] (A. Gryganskyi). http://dx.doi.org/10.1016/j.jip.2017.08.011 Received 7 April 2017; Received in revised form 3 August 2017; Accepted 9 August 2017 Available online 10 August 2017 0022-2011/ © 2017 Elsevier Inc. All rights reserved. K.T. Hodge et al. Journal of Invertebrate Pathology 149 (2017) 135–140 used as an outgroup. Sequences were aligned using MUSCLE (Edgar, 2004) and then concatenated. Alignments were visually inspected and ambiguous regions were excluded using Mesquite 3.3 (Maddison and Maddison, 2017). The alignment consisted of 2086 characters. The optimized nucleotide substitution model (GTR + U + I) was selected using ModelTest 3.06 (Posada and Crandall, 1998). The Maximum likelihood (ML) tree was estimated using Garli-2.0 (Bazinet et al., 2014). One thousand bootstrap replicates were computed and phylo- genetic support was assessed by bootstrap analysis using PAUP/ 4.0a109 (Swofford, 2002). 3. Results 3.1. Phylogenetic analysis The combined phylogenetic analysis suggests the two millipede-in- festing specimens from NY comprise a statistically well-supported clade that is closely related to Eryniopsis caroliniana (Fig. 2). Three En- tomophaga species form a well-separated sister group to that clade, and the next closest relatives are Entomophthora species. Representatives of the morphologically similar genus Batkoa form a well-supported monophyletic clade supported by a long branch. The positions of these clades on the tree each have strong statistical support, and reflect the results of previous studies (Gryganskyi et al., 2012, 2013). 3.2. Taxonomy Arthrophaga K.T. Hodge & A.E. Hajek, gen. nov. (MB 822065) Type Species: Arthrophaga myriapodina K.T. Hodge & A.E. Hajek Conidiophores unbranched, arising from hyphal bodies in the host Fig. 1. A millipede (Apheloria virginiensis corrugata) killed by Arthrophaga myraipodina. and piercing the cuticle of recently dead hosts. Conidiogenous cells multinucleate, club-shaped, apically inflated, tapering to a broad, short neck below a single primary conidium. Primary conidia uni- and counting of nuclei was accomplished with material mounted in cellular, forcibly discharged by papillar eversion, with papilla aceto-orcein. smoothly joining the conidial body and not sharply demarcated. Primary conidia unitunicate, multinucleate; nuclei en- 2.2. Molecular methods tomophthoroid and staining deeply with aceto-orcein. Secondary conidia multinucleate and resembling primary conidia, forcibly DNA sequences from three loci were used to investigate the place- discharged, arising singly from the lateral wall of a primary con- ment of the millipede fungus among other species in the subphylum idium, or basally near the papilla. Capilliconidia not observed. Entomophthoromycotina. For DNA extraction, freshly killed millipedes Rhizoids lacking. Resting spores not known. Most resembling with areas of profuse sporulation were collected and quickly processed. Entomophaga in its clavate conidiogenous cells and oligonucleate External mycelium and spores of the fungus were harvested from the primary conidia with rounded papillae but differing in its host and intersegmental areas of single millipedes, and immersed immediately in evolutionary lineage. Differing from Entomophthora in its pyriform DNA extraction buffer. The PowerSoil kit (MoBio Laboratories) for DNA primary conidia. Differing from Batkoa in its less abruptly bulbous extraction was used per instructions. conidiophores with much shorter necks. For 18S rDNA and 28s rDNA sequencing, we extracted genomic DNA from fungus cells harvested from specimens CUP-068238 and Arthrophaga myriapodina K.T. Hodge & A.E. Hajek, sp. nov. (MB CUP-068239 (Supplementary Tables 1, 2). The DNA was used as the 822067), Figs. 1, 3 and 4. ′ template for PCR reactions: The primers nu-LSU-0018-5 (Jensen and Holotype: Cornell Plant Pathology Herbarium, CUP-068238. NY: Eilenberg, 2001) and nu-LSU-0805-3′ (Kjøller and Rosendahl, 2000) Tompkins Co., Hickory Circle, on asphalt near center of road. June 1, were used to amplify a region of the 28S rDNA from specimens CUP- 2015, K.T. Hodge (from which DNA was extracted from fresh specimen for 068238 and CUP-068239. Primers NS24 (Gargas and Taylor, 1992) and SSU, LSU sequencing). nssu1088R (Kauff and Lutzoni, 2002) were used to amplify a region of Diagnosis: Conidiophores unbranched. Conidiogenous cells some- the 18S rDNA from specimens CUP-068238 and CUP-068239. Ampli- what inflated, tapering gradually to a wide neck. Primary conidia fied PCR products were sequenced at the Biotechnology Research pyriform, forcibly discharged with papilla smoothly joining the conidial Center at Cornell University, in both forward and reverse directions. body and not sharply demarcated. Basal scar sometimes visible at former attachment point to conidiophore. Each primary conidium 2.3. Phylogenetic analysis contained 8–18 nuclei (average of 14) that stain deeply with aceto-or- cein.
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